Examining plant physiological responses to climate ...

Plant Physiology Preview. Published on September 2, 2016, as DOI:10.1104/pp.16.00793

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Short Title: Plant evolutionary physiology and climate change

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Corresponding Author: Joy K. Ward ([email protected])

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Examining plant physiological responses to climate change through an evolutionary lens

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Katie M. Becklin1, Jill T. Anderson2, Laci M. Gerhart3, Susana M. Wadgymar2, Carolyn A. Wessinger1,

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and Joy K. Ward1

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Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045; 2Odum

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School of Ecology and Department of Genetics, University of Georgia, Athens, GA 30602; 3Geography

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Department, Kansas State University, Manhattan, KS 66506

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Summary: Integrating knowledge from physiological ecology, evolutionary biology, phylogenetics, and

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paleobiology provides novel insights into factors driving plant physiological responses to both past and

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future climate change.

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Author Contributions: All authors contributed equally to this work including intellectual input, design

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of the manuscript, and writing of the text.

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Funding: J.T.A and S.M.W are supported on NSF DEB #1553408; C.A.W is supported on NIH

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5F32GM110988-03; K.M.B and J.K.W are supported on NSF IOS #1457236 and a Research Investment

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Council grant from the University of Kansas. LMG is supported on NSF DEB #1455894.

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Keywords: climate change, eco-evolutionary dynamics, evolution, paleobiology, phylogenetics, plant

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ecophysiology, species interactions

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Copyright 2016 by the American Society of Plant Biologists

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Introduction Since the Industrial Revolution began approximately 200 years ago, global atmospheric carbon

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dioxide concentration ([CO2]) has increased from 270 to 401 ppm, and average global temperatures have

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risen by 0.85 °C, with the most pronounced effects occurring near the poles (IPCC, 2013). In addition, the

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last 30 years were the warmest decades in 1400 years (PAGES 2k Consortium, 2013). By the end of this

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century, [CO2] is expected to reach at least 700 ppm, and global temperatures are projected to rise by 4 °C

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or more based on greenhouse gas scenarios (IPCC, 2013). Precipitation regimes are also expected to shift

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on a regional scale as the hydrologic cycle intensifies, resulting in greater extremes in dry versus wet

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conditions (Medvigy and Beaulieu, 2012). Such changes are already having profound impacts on the

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physiological functioning of plants that scale up to influence interactions between plants and other

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organisms and ecosystems as a whole (Figure 1). Shifts in climate may also alter selective pressures on

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plants, and therefore have the potential to influence evolutionary processes. In some cases, evolutionary

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responses can occur as rapidly as only a few generations (Ward et al. 2000; Franks et al. 2007; Lau and

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Lennon, 2012; but there is still much to learn in this area as pointed out by Franks et al., 2014). Such

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responses have the potential to alter ecological processes, including species interactions, via eco-

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evolutionary feedbacks (Shefferson and Salguero-Gómez, 2015). In this review, we discuss micro- and

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macroevolutionary processes that can shape plant responses to climate change, as well as direct

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physiological responses to climate change during the recent geologic past as recorded in the fossil record.

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We also present work that documents how plant physiological and evolutionary responses influence

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interactions with other organisms as an example of how climate change effects on plants can scale to

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influence higher order processes within ecosystems. Thus, this review combines findings in plant

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physiological ecology and evolutionary biology for a comprehensive view of plant responses to climate

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change, both past and present.

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Due to rapid climate change, plants have become increasingly exposed to novel environmental

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conditions that are outside of their physiological limits and beyond the range to which they are adapted


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(Ward and Kelly, 2004; Shaw and Etterson, 2012). Plant migration may not keep pace with the

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unprecedented rate of current climate change (e.g., Loarie et al., 2009), and therefore rapid evolutionary

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responses may be the major process by which plants persist in the future (Franks et al., 2007; Alberto et

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al., 2013). In addition, although plants may have evolved physiological plasticity that produces a fitness

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advantage in novel environments, climate change may be so extreme as to push plants beyond tolerance

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ranges even in the most plastic of genotypes (Anderson et al., 2012).

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Understanding the potential for evolutionary responses at the physiological level is a key

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challenge that must be met in order to improve predictions of plant response to climate change. A focus

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on physiology is critical because these processes scale from individual to ecosystem levels. For example,

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[CO2] rise and climate change that alter photosynthetic rates may shift plant growth rates, overall

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productivity, and resource use (Ainsworth and Rogers, 2007; Norby, 2011; Medeiros and Ward, 2013).

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Other physiological responses to altered climate include increasing leaf sugars with elevated [CO2], which

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may influence major life history traits such as flowering time and fitness via sugar sensing mechanisms

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(Springer et al., 2008; Wahl et al., 2013). At higher scales, shifts in source/sink relationships of

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photosynthate can influence seedling survival, whole-plant growth, competitive ability within the broader

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plant community, symbiotic interactions, and fitness. Therefore, the potential for physiological

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functioning to evolve in response to climate change will be a key indicator of plant resiliency (or lack

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thereof) in future environments. Defining physiological components that correlate with fitness,

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particularly in newly emerging environments, will allow us to identify candidate processes that may be

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under strong selection in future environments, and to predict the composition and functioning of future

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plant populations and communities (Kimball et al., 2012).

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It is clear that long-term changes in the environment spanning millions of years of plant evolution

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have shaped the major physiological pathways that are present in modern plants (Edwards et al., 2010;

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Sage et al., 2012), and these pathways will determine the range of physiological tolerances for response to

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novel environments of the future. In addition, relatively recent conditions in the geologic record have

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shaped selective pressures on plant physiology (Ward et al., 2000) and may influence the ability of plants


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to respond to future conditions. For example, the peak of the last ice age (20,000 years ago) represents a

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fascinating time when low [CO2] (180-200 ppm) likely constrained the physiological functioning of C3

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plants. During that period, [CO2] was among the lowest values that occurred during the evolution of land

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plants (Berner, 2006). Modern C3 annuals grown at glacial [CO2] exhibit an average 50% reduction in

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photosynthesis and growth as well as high levels of mortality and reproductive failure relative to plants

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grown at modern [CO2] (Polley et al., 1993; Dippery et al., 1995; Sage and Coleman, 2001; Ward and

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Kelly, 2004). Thus, this period likely imposed strong selective pressures on plants as evidenced directly

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by artificial selection experiments (Ward et al., 2000) and in the recent geologic record (Gerhart and

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Ward, 2010).

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A series of key questions have now emerged: (1) How will plants evolve in response to rapid

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climate change? (2) How will evolutionary history and species interactions influence this evolutionary

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trajectory? (3) How have past responses to climate change in the geologic record influenced current and

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potentially future responses to a rapidly changing environment? To address these questions, we report on

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emerging concepts in the broad field of evolutionary physiology, paying specific attention to processes

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ranging from micro- to macroevolution, the influence of species interactions on these processes, and

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insights from paleobiology (where we provide new findings). This review is not intended to cover all of

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the current ground-breaking work in this area, but rather to provide an overview of how a multitude of

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approaches can influence our overall understanding of how plant physiological evolution has altered past

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ecosystems as well as those that will emerge during the Anthropocene epoch.

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Microevolutionary responses of plant physiology to climate change By altering thermal and precipitation regimes and [CO2], climate change is disrupting long-

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standing patterns of natural selection on plant physiology, morphology, and life history. Novel

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environmental pressures could reduce germination success, plant viability, and fecundity in the short-term

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as mediated through effects on physiology (Anderson, 2016). Phenotypic plasticity can temporarily

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alleviate the effects of directional selection pressures that are expected to arise with climate change


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(Figure 1) (Nicotra et al., 2010), but may not enable long-term population persistence as conditions fall

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outside of the bounds of historical variability. Species will ultimately have to evolve or migrate in pace

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with climate change to avoid extinction (Figure 1). Many species have already shifted their distributions

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to higher latitudes and elevations (Perry et al., 2005; Lenoir et al., 2008), yet evidence for evolution in

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response to climate change remains sparse at best (Franks et al., 2007; Merilä, 2012). Here, we discuss

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conditions that may promote or impede physiological and morphological adaptation to climate change in

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plants.

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Phenotypic plasticity: Phenotypic plasticity is a fundamental mechanism by which species respond to a

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changing environment. Climate change has prompted plastic responses in physiological traits for a wide

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variety of plant taxa (Gunderson et al., 2010; Liancourt et al., 2015), yet few studies examine the fitness

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consequences of plastic responses. The direction and adaptive value of plasticity can be assessed

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experimentally, where common genotypes are exposed to contrasting conditions designed to simulate a

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changing climate (Figure 2). In the context of climate change, adaptive plasticity results in equivalent or

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higher fitness of induced phenotypes relative to the original phenotype in the novel environment. The

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response to selection depends on the strength of selection on plasticity, the degree of heritable variation in

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plasticity, and the strength and direction of selection on other traits that are genetically correlated with the

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plastic response (Lande and Arnold, 1983).

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The cumulative effects of plasticity throughout a plant’s life cycle can be extensive. For example,

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a plant that is being shaded by a canopy will sense a red-to-far-red ratio below optimum, triggering

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physiological, molecular, and developmental adjustments that enhance light capture (Keuskamp et al.,

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2010). This ‘shade-avoidance’ syndrome (Schmitt and Wulff, 1993) can induce plastic responses in traits

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expressed later in life history (e.g., accelerations in the onset of flowering), and indirectly influence the

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strength or form of selection on these traits (Donohue, 2003). Furthermore, these types of plastic

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responses can be far-reaching, as the maternal environment can influence offspring phenotype and fitness

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(transgenerational plasticity or maternal effects) (e.g., Galloway and Etterson, 2007).


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Plasticity can facilitate evolution by alleviating the immediate selection pressures imposed by

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climate change, providing more time for evolutionary responses (Chevin et al., 2010). For instance,

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adaptive plasticity in water-use efficiency (WUE; carbon uptake per water loss) enabled plants from three

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genetically differentiated populations of the annual Polygonum persicaria L. to maintain high fitness in

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both drought and well-watered environments (Heschel et al., 2004). The maintenance of fitness under

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drought stress may allow this species more time to respond to other stressors. Plasticity can also promote

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genetic change if the phenotypes exposed to selection become fixed through genetic assimilation

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(Badyaev, 2005). Additionally, increased environmental variation projected under climate change may

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favor the evolution of higher levels of plasticity in physiological traits (Nicotra et al., 2010). Nevertheless,

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costs or limits to producing plastic responses can constrain the ongoing evolution of plasticity, ironically

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(DeWitt et al., 1998). Despite the ubiquity with which climate change is eliciting plastic responses in

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plant physiology, the potential contributions of plasticity to evolutionary processes remain largely

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underexplored in natural systems.

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Adaptive evolution: For adaptive evolution to occur, a population must have sufficient genetic variation in

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traits targeted by selection, including physiological traits. Estimates of heritability for physiological traits

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can vary widely by trait type (Geber and Griffen, 2003; Johnson et al., 2009), with lower heritability in

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physiological traits that are instantaneously measured than in those that represent broader temporal

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integration (Ackerly et al., 2000). The strength and form of selection, coupled with rates of gene flow and

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mutation, ultimately determine whether genetic variation in a population is replenished or depleted over

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time (Mitchell-Olds et al., 2007). Small fragmented plant populations are particularly susceptible to

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diminished genetic variation, and consequently may undergo increased extinction risks associated with

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climate change (Jump and Peñuelas, 2005; Leimu et al., 2006). To improve our ability to assess the

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capacity for rapid evolution in plant physiology, additional investigations must estimate the degree of

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genetic variation and the strength of selection under simulated climate change.

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Genetic correlations can constrain evolution if the direction of the correlation opposes that of


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selection. For example, Etterson and Shaw (2001) detected additive genetic correlations that were

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antagonistic to the direction of selection in the annual legume Chamaecrista fasciculata, and concluded

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that these correlations would likely impede adaptation to climate change. Furthermore, recent evolution of

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drought avoidance via early flowering increased Brassica rapa’s vulnerability to pathogens (O'Hara et al.,

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2016), demonstrating that climate change can restrict the joint evolution of plant physiological traits.

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Genetic correlations generated by pleiotropy (influence of a single gene on multiple traits), are generally

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stable and can restrict the rate of evolution (Mitchell-Olds, 1996). The same is true of genetic correlations

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maintained by linkage disequilibrium when loci are in close proximity (Falconer and Mackay, 1996).

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However, artificial selection studies have demonstrated that rapid evolution is still possible in spite of

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pleiotropic genetic correlations (Conner et al., 2011), and linkage disequilibrium decays quickly in large,

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outcrossing populations with high recombination rates (Flint-Garcia et al., 2003). Genetic constraints

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have been invoked as a considerable barrier to adaptive evolution in response to climate change, and

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characterizing the genetic architecture of functional traits in natural populations is paramount for

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predicting evolutionary change.

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Gene flow: Plant populations are connected over spatial scales by pollen and seed dispersal. If local

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populations lack sufficient genetic variation to respond to novel selection, gene flow can expand genetic

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variation, reduce inbreeding, and facilitate evolutionary responses to selection (Frankham, 2005). For

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instance, budburst phenology of two Scottish birch species may not evolve in pace with climate change

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without gene flow from populations with earlier phenologies (Billington and Pelham, 1991). Some plant

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species, including trees in the genera Quercus and Eucalyptus, display genetically based clinal variation

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across climatic gradients in physiological traits such as stomatal conductance and drought and frost

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tolerance (Kremer et al., 2014). Under climate change, gene flow from central populations may benefit

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peripheral populations at the leading edge of the range by introducing alleles pre-adapted to warm

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conditions (Aitken and Whitlock, 2013; Kremer et al., 2014).

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Gene flow can also restrict evolutionary responses to climate change by introducing maladapted


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alleles into populations that are already lagging in their adaptive responses to changing conditions

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(Lenormand, 2002). High rates of gene flow from central populations may overwhelm selection in the

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trailing-edge populations, preventing adaptation to novel conditions (Kirkpatrick and Barton, 1997; Bridle

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and Vines, 2007). The potential evolutionary consequences of gene flow for adaptation to climate change

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are variable and require further examination in appropriate ecological contexts. This is especially true in

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the context of plant physiology, for which we need additional data on genetic variation in natural

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populations and more information about the extent to which populations are connected by gene flow.

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Microevolution: Unanswered questions and future directions: Experiments that simultaneously

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manipulate multiple climate change factors hold great promise for elucidating the physiological processes

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that underlie climate change responses (Eller et al., 2011) and for improving our ability to predict plant

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evolution. However, few empirical studies directly evaluate microevolution of physiology under climate

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change. Future efforts should quantify multiple physiological traits and fitness components in plants of

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known origin to assess genetic constraints on climate change response and to evaluate the adaptive nature

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of physiological plasticity. Additionally, common garden experiments across spatial climatic gradients

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can reveal whether climate change disrupts local adaptation in physiology (Wang et al., 2010; Wilczek et

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al., 2014). Studies that integrate population and quantitative genetics can test whether gene flow hastens

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physiological adaptation through introgression of alleles from populations that have evolved under

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conditions that reflect climate projections. Finally, field studies can illuminate the role of biotic

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interactions in shaping physiological plasticity and evolution in natural systems.

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Macroevolutionary responses of plant physiology to climate change Climate change expands certain ecological niches at the expense of others. The availability of

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ecological opportunities and the ability of species to exploit these opportunities can dictate the tempo of

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species diversification as well as patterns of phenotypic evolution (Simpson, 1953). Therefore, climate

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change has the potential to alter patterns of species diversification and generate macroevolutionary trends


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in plant physiology. Comparative work has established that physiological traits can provide an

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evolutionary advantage in a novel environment (Givnish, 1987), potentially allowing access to a new

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ecological niche or improving competitive advantage in an expanded niche. Either of these situations may

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boost population density, geographic range size, or the success of peripherally isolated populations. These

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changes can in turn decrease the probability of extinction or increase the rate of speciation (Heard and

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Hauser, 1995), stimulating plant species diversification.

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A phylogenetic approach can identify associations between environmental change, trait evolution,

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and macroevolutionary patterns of species diversification. This approach relies on fossil-calibrated

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phylogenetic trees that estimate divergence events in absolute time. Using trait data for each tip in the

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phylogenetic tree and a model for trait evolution, the evolutionary history of traits can be reconstructed on

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the time-calibrated tree (Schluter et al., 1997). When the evolution of more than one trait is modeled on

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the tree, phylogenetic comparative methods can test for patterns of correlated evolution between traits

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(Pagel, 1994). These correlations may signal constraints on the evolution of key traits, where their origin

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is contingent on the presence of preexisting 'enabling' traits. Model-based approaches can identify shifts

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in diversification rate on time-calibrated trees (e.g., Rabosky, 2014) and test whether diversification rates

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are influenced by trait evolution (Maddison et al., 2007). As a case study, we discuss how a phylogenetic

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approach has connected innovations in plant photosynthesis to species diversification following climate

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change during the Miocene.

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Miocene climate change and innovations in photosynthesis: A significant decline in [CO2] that began in

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the early Oligocene (~32 Ma) coincided with global cooling and aridification in the mid-Miocene (~14

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Ma) (Tripati et al., 2009); these environmental changes imposed physiological stress on plants,

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particularly those living in warm or arid habitats (Ehleringer and Monson, 1993). As atmospheric

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[CO2]:[O2] declines and temperatures rise, the oxygenation reaction with Rubisco (ribulose-1,5-

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bisphosphate-carboxylase/oxygenase) increases relative to carboxylation (Ehleringer and Monson, 1993),

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reducing the efficiency of photosynthesis. Photorespiration scavenges some of the lost carbon from this


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process, but net losses of carbon and energy still occur. Evaporative water loss increases with

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photorespiration rates because greater stomatal conductance is necessary to make up for carbon losses

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(Monson et al., 1983).

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CO2-concentrating mechanisms (CCMs) are physiological pathways that increase the ratio of

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[CO2]:[O2] near the site of CO2 fixation, thus reducing photorespiration (Hatch, 1987; Winter and Smith,

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1996). There are two main types of CCMs: crassulacean acid metabolism (CAM) and C4 photosynthesis.

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Both separate initial carbon fixation from the rest of photosynthesis by using phosphoenolpyruvate

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carboxylase (PEPC) rather than Rubisco to fix atmospheric CO2 into a 4-carbon (C4) acid. The C4 acid is

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later decarboxylated to release CO2 within photosynthetic cells where Rubisco refixes it in the standard

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Calvin cycle in the absence or near absence of photorespiratory carbon losses. In CAM plants, the diurnal

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pattern of stomatal opening is inverted, such that PEPC fixes CO2 at night and the C4 acids are

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decarboxylated during the day, allowing Rubisco to refix CO2. Since stomata are closed during the day,

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CAM greatly improves WUE in arid habitats (Winter and Smith, 1996). In C4 plants, PEPC and Rubisco

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function during the day, but PEPC is active in mesophyll cells and C4 acids are transported to bundle

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sheath cells where Rubisco and the Calvin cycle operate (Hatch, 1987).

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CCMs have evolved numerous times in higher plants (Edwards and Ogburn, 2012) and are key

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traits that increased diversification of certain lineages following the Miocene climate change, and

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ultimately contributed to the dominance of these groups in arid landscapes (Sage et al., 2012). Recent

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studies have used a phylogenetic approach to examine the relationship between Miocene climate change,

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CCM evolution, and diversification rate.

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Phylogenetic patterns of CCM evolution and diversification rate: The evolution of CCMs has been

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reconstructed for several plant groups. In grasses, sedges, and eudicots, the origins of C4 photosynthesis

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date to the Oligocene through the Miocene (Besnard et al., 2009; Christin et al., 2011; Spriggs et al.,

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2014). In bromeliads, orchids, and Euphorbia, origins of CAM photosynthesis date to the early Miocene

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to the late Pliocene (Horn et al., 2014; Silvestro et al., 2014; Bone et al., 2015). The timing of CCM


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origins in these groups is consistent with the hypothesis that CCM evolution is associated with declining

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[CO2].

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Based on current distributions, the evolution of CCMs appears to occur most often in semi-arid to

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arid regions (Sage et al., 2011). Phylogenetic studies demonstrate that the evolution of C4 photosynthesis

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in grasses is significantly correlated with shifts to open and drier habitats (e.g., Edwards and Smith,

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2010). The evolution of CAM in terrestrial Eulophiinae orchids is associated with shifts from occupation

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of humid habitats to hot and dry habitats (Bone et al., 2015), as is true for orchids and bromeliads that

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evolve an epiphytic habit in forest canopies where water availability is diurnally and seasonally

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intermittent (e.g., Silvestro et al., 2014; Givnish et al., 2015). These patterns are consistent with the

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hypothesis that CCMs confer the greatest advantage in water-limited habitats.

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Phylogenetic studies have identified significant shifts towards increased diversification rate in

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clades that evolved CCMs, predominantly in the Miocene following the initial evolution of CCMs (e.g.,

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Arakaki et al., 2011; Table 1). Thus the Miocene climate change appears to have created an ecological

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opportunity allowing species that evolved CCMs to diversify. Recent studies find that the evolution of

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CCMs is associated with elevated net diversification rates compared to C3 plants (Table 1). In these

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studies, evolution of CCMs increases both speciation and extinction rates, suggesting that the evolution of

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CCMs is associated with greater species turnover.

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CCMs repeatedly evolved in some clades inhabiting warm and arid environments, yet genetic and

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developmental factors may have constrained the evolution of this innovation in other clades. The

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evolution of CCMs may be contingent on prior physiological adaptations: in grasses, C4 photosynthesis

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evolves from species that already have increased proportions of bundle sheath cells (Christin et al., 2013).

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CAM photosynthesis may evolve in species with succulence, as this trait enables a greater capacity for

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storing water and C4 acids at night (Edwards and Ogburn, 2012). The evolution of CCMs may also be

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contingent on the presence of extra copies of genes encoding enzymes such as PEPC that are recruited

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into the CCM biochemical pathway. These extra copies may be obtained through gene duplication

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followed by neofunctionalization (e.g., Christin et al., 2013) or introgression (e.g., Besnard et al., 2009;


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Christin et al., 2012).

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Insights from phylogenetic patterns of CCM evolution: The case of CCM evolution is a particularly

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compelling example where diverse yet complementary approaches are focused on understanding

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macroevolutionary patterns in plant physiology and the underlying mechanisms for these patterns. An

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emerging consensus from these studies is that the evolution of CCMs following climate change alters

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patterns of species diversification in similar ways across diverse angiosperm clades, yet the origin of

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CCMs may depend on the ancestral ecological niche or even the ancestral genomic content. These general

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themes may be true for other plant physiological traits that mediate plant responses to environmental

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change. For example, recent work using a phylogenetic approach suggests that adaptation in leaf stomatal

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ratio is associated with environmental conditions and selection for fast growth rate, yet is also subject to

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constraints mediated by trade-offs between photosynthetic rate and biotic interactions (Muir, 2015). As

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studies on evolutionary patterns in plant physiology accumulate, an important goal will be to synthesize

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mechanistic, phylogenetic studies, and fossil evidence in order to characterize and predict

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macroevolutionary responses to climate change (Rothwell et al., 2014).

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Plant evolutionary physiology inferred from the fossil record Investigations that reconstruct plant physiological functioning of the past using ancient plant

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specimens enhance our understanding of plant evolutionary physiology, provide powerful information on

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how plants responded to long-term changes in climate, and generate insights into how past environments

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have shaped the current physiological structure of plants. The study of ancient plant specimens allows for

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a direct assessment of physiological responses across time scales where physiological traits may have

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been responding to selective agents. These studies are particularly powerful when (1) modern plant

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equivalents exist for comparison, (2) specimens are compared in controlled locations where local climates

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are known over time, and (3) preservation is high enough to allow for measurements on organic tissue

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(e.g., stable isotopes and DNA analyses) and/or high-resolution of anatomical structures. Additionally,


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ancient plants that have no modern analogs can provide important examples of physiologies that did not

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persist in response to climate shifts, as well as physiologies that evolved in extreme environments.

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Approaches that allow for the study of ancient plant physiology in the fossil record can involve plants that

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perished thousands or even millions of years ago (Gulbranson and Ryberg, 2013). Below we discuss

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examples where stable isotope analysis of ancient tissue and assessments of structure-function

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relationships in the geologic record have advanced our understanding of evolutionary patterns of plant

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physiology. We focus on plant responses to low [CO2] during the last glacial period, which is likely to

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have been a strong selective agent due to limiting carbon for photosynthesis (Ward et al. 2000; Gerhart

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and Ward, 2010).

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Measurements of stable carbon isotope ratios are an excellent technique for assessing plant

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physiology over time in an evolutionary context and are commonly expressed relative to an international

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standard using per mil notation: δ = (Rsample/Rstandard – 1)*1000, where R is the ratio of the heavy isotope

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(13C) to the lighter isotope (12C) and the standard is PDB (Pee Dee Belemnite). The carbon isotope ratio of

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leaf tissue (or other tissue types corrected to leaf values) is a function of (a) the different diffusion rates of

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13

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inter-cellular [CO2] (ci) to atmospheric [CO2] (ca) (Farquhar et al., 1989). Since the first two components

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are constants, leaf ci/ca can be calculated from carbon discrimination values (1) when the carbon isotope

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ratio of source air (for photosynthesis) is known:

CO2 versus 12CO2, (b) the fractionation effect of Rubisco, and (c) leaf ci/ca, representing the ratio of leaf

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,

(1)

where δ13Cair is adjusted for the age of the ancient specimen. From Δ, ci/ca can be calculated as:

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,

(2)

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where a and b are constant fractionation factors that account for slower diffusion of 13CO2 relative to

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1989). Additionally, ci can be determined if ca is known (Ward, 2005).

CO2 (4.4‰) and the net discrimination effects of Rubisco (27-30‰), respectively (Farquhar et al.,


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ci/ca ratios are dependent on the dual effects of leaf stomatal conductance (gs) that influences the

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supply of CO2 to the leaf and the demand for CO2 that is determined via photosynthetic capacity (Vcmax)

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(Ehleringer and Cerling, 1995; see Fig. 4 within). Higher ci/ca is indicative of higher stomatal

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conductance and/or lower photosynthetic capacity, which serve to reduce 13C in leaf tissue. This effect is

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indicated by reductions in carbon isotope values (1) or increases in carbon discrimination (2). Measures of

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ci/ca over evolutionary time indicate how incoming carbon through stomata is balanced with water loss,

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and provide information on responses of photosynthetic capacity to environmental stimuli (e.g., light,

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nutrient availability; Ehleringer et al., 1997). Moreover, stable carbon isotope ratios have provided

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evidence of the first CO2-assimilating mechanisms to arise during early autotrophic evolution in the

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Earth’s history (3.8 Byr ago) and influenced our understanding of the effects of anthropogenic climate

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change on plant physiological functioning (e.g., Battipaglia et al., 2013).

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Ehleringer and Cerling (1995) proposed that ci/ca might serve as a physiological and possibly

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evolutionary set point for photosynthesis within C3 plants (see highlighted box for an original case study

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of this from our own research). This ratio does not express absolute gas flux rates, but rather, indicates

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overall plant functioning as integrated from the dual influences of stomatal regulation (CO2 supply to the

352

leaf) and investment in photosynthetic machinery (CO2 demand in photosynthesis) (Farquhar et al., 1989).

353

Furthermore, leaf carbon isotope ratios provide a time-integrated measure of physiological responses

354

since they capture carbon fixation over the course of leaf development, and therefore serve as an excellent

355

phenotypic proxy for physiology in evolutionary studies. Plants with shorter life histories and faster

356

growth rates exhibit higher ci/ca values compared with perennials (Dawson et al., 2002). In addition,

357

carbon isotope ratios tend to exhibit high levels of heritability within species (Dawson et al., 2002).

358

Hausmann et al. (2005) mapped five QTL that influence carbon isotope ratios in Arabidopsis thaliana,

359

which co-localized with QTL controlling flowering time. Furthermore, genotypes of crops and natural

360

species have shown stability in ci/ca across differing environments, and rank order of ci/ca is often

361

maintained among plant genotypes across different weather extremes through time (e.g., Sandquist and

362

Ehleringer, 2003). Such a response is not surprising given that stomatal conductance and photosynthetic


14

363

capacity are linearly and positively related across a wide range of taxa from clubmosses to herbaceous

364

forbs and grasses (Franks and Beerling, 2009). In this sense, increases in both stomatal conductance and

365

photosynthetic capacity have opposing effects on ci/ca that may serve to stabilize this ratio across wide

366

ranging conditions. Such responses have also been observed within species, allowing for a balance in

367

stomatal and non-stomatal limitations on leaf-level physiology in response to climate change and shifts in

368

resource availability across contemporary and geologic time scales (Ehleringer and Cerling, 1995; Ward,

369

2005; Gerhart and Ward, 2010; Gerhart et al., 2012; Easlon et al., 2015). These findings suggest that ci/ca

370

may have interesting evolutionary pathways, whereby this trait appears to be evolutionarily homeostatic

371

in some cases. The combination of alleles that maintain this response will be important to understand in

372

future studies.

373

Box 1: Case Study Testing Ehleringer et al. (1995) Set-point Hypothesis for ci/ca (Note that

374

Juniperus data was previously published in Gerhart et al. (2012), and that Agathis data is original

375

to this review.)

376

To test the set-point hypothesis for ci/ca proposed by Ehleringer et al. (1995) in controlled locations over

377

geologic time scales, we compared the physiological patterns of modern and glacial trees preserved

378

within the La Brea tar pits in southern California, USA (Juniperus sp.) and peat bogs in the North Island,

379

New Zealand (Agathis australis; new data). This allowed us to evaluate the responses of two coniferous

380

species from different hemispheres, which experienced different environmental changes since the last

381

glacial period. Juniperus experienced climate conditions that were cooler and wetter than present. Modern

382

high-elevation trees serve as an environmental control and allowed us to isolate the effects of changing

383

[CO2] from other environmental changes (Gerhart et al., 2012). Unlike the Juniperus in our study, glacial

384

Agathis experienced warmer and wetter conditions during the last glacial period compared to modern

385

climates (Elliot et al., 2005; Horrocks et al., 2007; D'Costa et al., 2008). We examined the effects of

386

increasing [CO2] in controlled locations in both study systems; the full Juniperus sampling scheme

387

additionally enabled us to determine the independent effects of rising [CO2] from glacial to present.

388

Interestingly, both Juniperus and Agathis showed constant ci/ca throughout the last 50,000 years


15

389

(Figure 3), supporting the set-point hypothesis proposed by Ehleringer and Cerling (1995). Constant ci/ca

390

likely resulted from decreases in both stomatal conductance and photosynthetic capacity as [CO2]

391

increased from past to present. Furthermore, constant ci/ca, coupled with reduced [CO2] in glacial periods,

392

resulted in dramatic reductions in ci for glacial trees. For both Juniperus and Agathis, glacial ci values

393

were on average 50-60 ppm below modern values. Additionally, glacial ci values exhibited only a narrow

394

overlapping window with modern values of 3-6 ppm, with less than 1% of all annual rings (glacial and

395

modern) falling in this range. Therefore, despite experiencing different environmental changes, both

396

Juniperus and Agathis show stability in ci/ca with increasing [CO2]. Additionally, both species show

397

unprecedented low levels of ci during the last glacial period relative to modern plants, suggesting the

398

likelihood of physiological carbon starvation in these trees (Gerhart et al., 2012). Minimum ci values of

399

each species (95 ppm for glacial Juniperus and 110 ppm for glacial Agathis) may represent a

400

physiological carbon compensation point for survival, below which trees may not be able to maintain a

401

positive carbon balance for maintenance respiration, growth, and survival (Gerhart et al., 2012).

402

With regard to changing atmospheric [CO2] concentration, Gerhart et al. (2012) found that

403

interannual variability in ci/ca (from annual tree rings) was significantly higher in modern versus glacial

404

Juniperus, despite similar levels of climatic variability in these time periods (Mayewski et al., 2004).

405

Significantly, reduced interannual variation in Juniperus during the last glacial period was attributed to

406

the constraints of low [CO2] on physiological function, while high variation in modern Juniperus was

407

attributed to effects of water availability that differ on an annual basis (Gerhart et al., 2012). Thus,

408

Juniperus shows evidence of physiological shifts that appear to reflect changes in limiting factors that

409

likely influenced evolutionary processes across geologic time.

410 411

When surveying studies with ancient plants as well as modern plants, it has been noted that ci/ca

412

is maintained across [CO2] gradients in the majority of cases as was shown in the examples above

413

(Gerhart and Ward, 2010). There are, however, a number of notable exceptions. For example, Becklin et

414

al. (2014) measured ci/ca in an intact plant community in the southwestern U.S. between the last glacial


16

415

period and present (185 to 400 ppm CO2 gradient) by sampling packrat middens. They found some

416

evidence of stability in ci/ca during limited time periods, but more pronounced evidence of increasing ci/ca

417

from past to present in the majority of species. Decreases in both stomatal conductance and

418

photosynthetic capacity from past to present could explain such a result. Specifically, photosynthetic

419

capacity may have been proportionally more reduced in response to declining nitrogen (N) availability

420

from past to present, as evidenced by lower leaf N in modern specimens relative to glacial ones. In

421

response to these and other exceptions, Voelker et al. (2016) conducted a modeling analysis to describe

422

the homeostatic leaf gas exchange response to glacial through future changes in [CO2]. These authors

423

concluded that plants may not directly maintain constant ci/ca per se, but may be modulating their

424

physiologies to maximize carbon gain at low [CO2] (glacial periods) with a shift towards reducing water

425

loss as photosynthesis approaches CO2-saturation at elevated [CO2] (future levels). In support of this idea,

426

glacial plants often have higher stomatal density/index relative to modern plants (reviewed in Royer,

427

2001); enhanced CO2 diffusion into leaves at the expense of additional water loss may have been a

428

beneficial trade-off during periods when [CO2] was highly limiting. In one example, Beerling et al. (1993)

429

found that Salix herbacea exhibited some of the highest stomatal densities in the fossil record during the

430

Wolstonian and most recent glacial stages. Beerling (2005) also found that Selaginella selagenoides and

431

S. kraussiana showed a 30% reduction in stomatal density from the last glacial period to the present as

432

[CO2] rose from 280 to 400 ppm. However, Becklin et al. (2014) did not find evidence for shifts in

433

stomatal index or stomatal pore size in Juniperus osteosperma or Pinus longaeva in a controlled location

434

in the Great Basin across 20,000 years of evolutionary time. Nonetheless, these empirical and modeling

435

efforts highlight the diverse evolutionary strategies of plants to overcome carbon, water, and nutrient

436

limitations through modulation of leaf-level characteristics that are clearly preserved in the fossil record.

437

Moreover, Sage (1999) hypothesized that evolutionary innovations to enhance CO2 uptake during glacial

438

periods may have produced selection pressures that could limit the ability of plants to benefit from rising

439

[CO2] in modern and future atmospheres.

440


17

441

Species interactions and the evolution of plant physiology in response to climate change

442

Plant species evolve in complex environments with networks of interacting species. Climate

443

change will affect plant physiology and evolution indirectly by altering interactions with mutualists,

444

antagonists, and competitors (Fig. 1) (e.g., Gilman et al., 2010; Lau et al., 2014; Kiers et al. 2010).

445

Interacting species are potent agents of selection that can drive the evolution of plant physiology through

446

direct effects on physiological processes (e.g., effects of mycorrhizal fungi on plant carbon and nutrient

447

dynamics) or through shifts in physiological trade-offs (e.g., investment in defensive compounds vs.

448

growth). The eco-evolutionary consequences of altered species interactions with climate change may, in

449

some cases, be more important than the direct effects of climate change on plant physiology (e.g.,

450

Alexander et al., 2015). Below, we use plant-herbivore, plant-pollinator, and mycorrhizal associations as

451

case studies to illustrate several mechanisms by which climate change is altering species interactions, and

452

thereby influencing plant evolutionary and physiological responses to complex environmental changes.

453 454

Plant-herbivore interactions: Plants have evolved elaborate defenses against diverse and abundant

455

herbivore assemblages (e.g., Núñez-Farfán et al., 2007). By altering plant physiology, climate change

456

could disrupt the production of secondary metabolites that provide anti-herbivore defense (Alnsour and

457

Ludwig-Muller, 2015), alter the strength of physiological trade-offs between herbivore defense and plant

458

growth, and reduce the nutritional value of plant tissues (Robinson et al., 2012). For example, meta-

459

analysis reveals that elevated [CO2] reduces plant nutritional quality for many herbivore species by

460

increasing leaf carbon:nitrogen ratios (Robinson et al., 2012). Consequently, herbivores will need to

461

consume more plant tissue to meet their nutritional demands (DeLucia et al., 2008; Robinson et al., 2012),

462

which may alter selection for plant defensive and tolerance traits.

463

Direct climate change effects on herbivore physiology and population dynamics can also generate

464

eco-evolutionary feedbacks that impact selection on plant traits. First, higher temperatures may accelerate

465

insect population growth rates, potentially increasing the frequency and severity of plant damage (e.g.,

466

Liu et al., 2011; Mitton et al., 2012). Indeed, foliar damage from insect herbivores increased dramatically


18

467

with mean annual temperature across millions of years in the fossil record (Currano et al., 2010). Warmer

468

winter temperatures may also reduce overwinter mortality among herbivores (e.g.,Bale et al., 2002) and

469

increase foraging opportunities during prolonged growing seasons (Brodie et al., 2012 ). Second, climate

470

change may increase herbivory by disrupting herbivore-predator interactions. If predators can no longer

471

forage during certain periods of the day because temperatures exceed their thermal tolerances, then

472

herbivores may inflict greater damage on plants (Barton et al., 2009). Third, owing to their fast generation

473

times and high mobility, insect herbivores may have a greater capacity than plants to adapt to ongoing

474

climate change or to migrate to more suitable locations. For example, rapid migration of natural enemies

475

into previously inhospitable habitats could expose naïve plant populations to increased levels of damage

476

(e.g., Kurz et al., 2008), thereby imposing novel selection on these populations

477

Increased rates of herbivory with climate change could alter plant physiology, reduce plant fitness

478

and population growth rates, deplete genetic diversity, and diminish adaptive potential (Maron and Crone,

479

2006). It remains to be seen whether plants can counter rapid responses of herbivores to changing

480

climates. Pre-existing genetic diversity in plant defense (Rasmann and Agrawal, 2011) and gene flow

481

among populations could facilitate adaptation to novel herbivore communities. Additionally, plant

482

populations that have historically experienced spatiotemporal variation in herbivore damage may have

483

evolved multiple defense strategies (Carmona and Fornoni, 2013), which may decrease susceptibility to

484

altered herbivore assemblages, especially if projected increases in climate variability translate into greater

485

temporal variation in herbivory. Finally, simultaneous changes in both [CO2] and climate will likely

486

mediate plant and herbivore responses in surprising ways (e.g., Copolovici et al., 2014), resulting in novel

487

eco-evolutionary dynamics.

488 489

Plant-pollinator interactions: Pollinators influence the evolution of plant traits and the diversification of

490

flowering plant lineages (e.g., Cardinal and Danforth, 2013). Climate change may alter pollination

491

mutualisms via effects on plant physiology and physiological trade-offs. For example, many pollinators

492

prefer larger flowers, however, increased frequency or severity of drought may impose selection for


19

493

smaller flowers that reduce water loss (Galen, 2000). Elevated [CO2] alters the nutritional quality of

494

nectar rewards through direct effects on photosynthesis and sugar production (Watanabe et al., 2014).

495

Increases in [CO2] over the past 170 years also reduced pollen protein concentration in Solidago

496

canadensis (Ziska et al., 2016). Such changes in either nectar or pollen rewards could adversely affect

497

pollinators and the strength of pollinator-mediated selection on plant traits. Over longer periods of time,

498

climate change effects on water stress and sugar production in plants could restrict evolutionary shifts in

499

pollination syndrome if changes in nectar traits alter pollinator selection.

500

Climate change effects on plant and pollinator physiology may also result in mismatches between

501

flowering time and pollinator activity (Forrest, 2015). Many plant species are emerging and reproducing

502

earlier in the year due to increasing temperature and [CO2] (e.g., Amano et al., 2010; Ward et al., 2012;

503

CaraDonna et al., 2014), while some species are delaying phenological events or are unresponsive to

504

climate change (Sherry et al., 2007; Cook et al., 2012). The timing of these life history transitions depends

505

on complex environmental cues that affect plant physiology (Forrest and Miller-Rushing, 2010). Climate

506

change may alter such cues, resulting in dramatic shifts in flowering time (Springer et al., 2008; Wahl et

507

al., 2013). If plants and their pollinators differ in their environmental sensitivities, then climate change

508

could induce asynchronous phenologies, which could modify patterns of gene flow (Elzinga et al., 2007),

509

alter coevolutionary dynamics between pollinators and plants (Gilman et al., 2012), reduce seed

510

production (Forrest, 2015), and limit resource availability for pollinators (Memmott et al., 2007; but see

511

Forrest and Thomson, 2011). Predicting the extent of temporal asynchrony under future climates will

512

require physiological studies that determine the specific environmental cues that elicit life history

513

transitions in plants and pollinators.

514

Asynchronous migration of (specialist) plant or pollinator mutualists with climate change could

515

limit the pace of migration for the partner species, reduce the fitness of both interacting species, and alter

516

eco-evolutionary dynamics within pollination mutualisms (Gilman et al., 2010). For example, bee

517

diversity in alpine ecosystems in Colorado has increased with the influx of lower elevation bee species

518

over the past 40 years (Miller-Struttmann and Galen, 2014). Additionally, some alpine bee species


20

519

evolved significantly shorter tongues, which allow these bees to forage on a wider variety of plant species

520

(Miller-Struttmann et al., 2015). These changes in the pollinator community have led to a functional

521

mismatch between alpine plants and their pollinators since average flower size in this system has not

522

changed with warming temperatures (Miller-Struttmann et al., 2015). In this case, climate-induced shifts

523

in the pollination network may have cascading effects on the evolution of plant traits. It remains unclear

524

how changes in pollinator-mediated selection will interact with physiological constraints of increasing

525

temperature and drought to drive plant physiological and evolutionary responses.

526 527

Mycorrhizal associations: Mycorrhizal associations are widespread symbioses involving plants and root-

528

colonizing fungi (Smith and Read, 2008). Physiological mechanisms that control carbon and nutrient

529

acquisition are tightly linked in mycorrhizal plant species; thus, climate change effects on plant

530

physiology can alter the functioning of these ancient and ubiquitous interactions (Kiers et al., 2010;

531

Mohan et al., 2014). Since plants supply mycorrhizal fungi with sugars, genetic and environmental factors

532

that limit photosynthesis can reduce the amount of carbohydrates available to support fungal symbionts

533

(Johnson et al., 2015). For example, C3 plants are generally more carbon-limited than C4 plants, especially

534

in dry environments. This physiological constraint may explain the higher responsiveness of C4 plants to

535

mycorrhizal fungi (Reinhart et al., 2012). In exchange for carbohydrates, mycorrhizal fungi supply their

536

hosts with soil nutrients (Smith and Read, 2008); some fungi also enhance plant drought tolerance (Lehto

537

and Zwiazek, 2011), pathogen resistance (Powell et al., 2009), and herbivore defense (Johnson and

538

Gilbert, 2015).

539

Mutually beneficial mycorrhizal associations are hypothesized to occur in nutrient limited

540

ecosystems where plants can effectively trade surplus carbohydrates for soil nutrients (Johnson et al.,

541

2015). However, climate change may shift relative resource limitations within host plants, thereby

542

altering mycorrhizal dynamics and plant investment in these mutualisms (Kiers et al., 2010; Mohan et al.,

543

2014). For example, increased photosynthesis under elevated [CO2] reduces the relative cost of

544

supporting mycorrhizal fungi, but plants require more nutrients to maintain high rates of photosynthesis


21

545

and growth. To meet their nutrient demands, plants generally allocate more resources to fungal symbionts

546

under elevated [CO2], resulting in increased fungal growth and more beneficial partnerships (Compant et

547

al., 2010). In some cases, mycorrhizal responses to elevated [CO2] decrease over time, possibly due to

548

progressive nitrogen limitation of photosynthesis and competition between plants and fungi for this

549

critical resource (Alberton et al., 2007). Climate conditions that limit photosynthesis (e.g., drought) could

550

also reduce net mycorrhizal benefits and potentially cause growth depressions within host plants (Correa

551

et al., 2006; Johnson et al., 2015). Delineating the independent and synergistic effects of increasing

552

[CO2], temperature, and drought will provide novel insights into environmental and physiological drivers

553

of mycorrhizal dynamics.

554

Functional diversity and rapid evolution in fungal populations can mediate plant physiological

555

responses to climate change and the evolution of plant traits within complex environments. For example,

556

increasing herbivory or pathogen load with climate change may strengthen the importance of mycorrhizal

557

fungi to plant defenses (Pineda et al., 2013). Some mycorrhizal functions, such as pathogen protection,

558

are phylogenetically conserved within fungal lineages (Powell et al., 2009). Thus, variation in fungal

559

community composition within and among plant communities could generate selection mosaics that alter

560

plant adaptation to novel environmental stressors. Furthermore, plants can preferentially allocate

561

carbohydrates to more beneficial mycorrhizal fungi (Bever, 2015), which could enable plants to maintain

562

beneficial partnerships across variable environments and strengthen eco-evolutionary feedbacks within

563

these symbioses.

564 565

Species interactions: Unanswered questions and future directions: Our understanding of climate change

566

effects on species interactions has grown considerably in recent years (Kiers et al., 2010; Robinson et al.,

567

2012; Forrest, 2015); however, the potential for climate change to affect plant physiological evolution

568

through species interactions is less clear. Given the complexity of plant-species interactions and their

569

potential to drive evolution, studies that simulate climate change under realistic natural conditions with a

570

full complement of interacting species could reveal plant physiological and evolutionary responses to


22

571

direct and indirect effects of novel climates (Barton et al., 2009). Studies that take advantage of genetic

572

mutants or natural variation in plant traits, such as herbivore defenses, can provide further insights into

573

the genetic basis of traits under selection by interacting species. Pairing these mechanistic experiments

574

with phylogenetic analysis of the evolution of plant traits and species interactions following historic

575

climate change events could provide a framework for predicting how species interactions will shape plant

576

physiological and evolutionary responses to climate change in the future.

577 578

Conclusions

579

In the introduction, we set out a series of questions that are critical to the field of evolutionary

580

physiology and we provide examples of how these questions are being addressed in highly innovative

581

ways (see Outstanding Questions). Moreover, the field of evolutionary physiology can inform us about

582

the future trajectory of plant responses to climate change, as well as provide insights into how

583

evolutionary history has shaped the current responses of plants to their environment. This is a field that

584

has provided a foundation for our understanding of the resiliency (or lack thereof) of plants to survive

585

rapid climate change. Moreover, continued work in this area as well as application of new knowledge is

586

critical for our own adaptive potential to climate change since food and water security and ecosystem

587

services are highly dependent on the evolutionary and physiological responses of plants to future

588

conditions. We argue that the interception of plant physiological studies coupled with evolutionary

589

approaches will enhance our understanding of past and future plant communities and the roles they play

590

in driving ecosystem functioning through time.

591 592 593

Acknowledgements We thank Robert Teisberg, president of Ancientwood Ltd., for his generous contribution of

594

glacial and modern Agathis specimens for research purposes. We also thank John Southon at the

595

University of California-Irvine W. M. Keck Carbon Cycle Accelerator Mass Spectrometry Laboratory

596

for radiocarbon dating of ancient specimens.


23

597 598

Advances

599

•

Rapid climate change is disrupting long-standing patterns of natural selection on plant physiological

600

traits. Microevolutionary responses to these changes can occur over time scales relevant to ecological

601

processes.

602

•

Emerging macroevolutionary analyses using large, time-calibrated phylogenies provide insight into

603

evolutionary changes in plant physiology and species diversification rates following past climate

604

change events.

605

•

606 607

Past conditions, such as low [CO2] during glacial cycles, likely produced lingering adaptations that could limit plant physiological responses to current and future climate change.

•

Climate change can affect plant traits, fitness, and survival indirectly via shifts in biotic interactions.

608

The eco-evolutionary consequences of altered species interactions can be as important as the direct

609

effects of climate change on plant physiology.

610 611

Outstanding Questions

612

•

613 614

physiological traits? •

615 616

•

621

How have plant responses to past climate conditions influenced physiological and evolutionary responses to rapid climate change during contemporary time periods?

•

619 620

What microevolutionary and ecological mechanisms contribute to altered species diversification rates following environmental change?

617 618

To what degree will phenotypic plasticity or gene flow enhance or impede adaptive evolution in plant

What are the relative influences of direct effects of climate change versus indirect effects via shifts in biotic interactions on the evolution of plant physiological traits?

•

How will potential physiological constraints interact with evolutionary history and species interactions to mediate plant responses to future changes in multiple environmental factors?


24

622

•

To what degree can we predict the resiliency of plants to survive rapid climate change?


25

623

Table 1. Estimated speciation rates (λ), extinction rates (μ), and net diversification rates (r = λ - μ)

624

associated with C3 photosynthesis and CCM-based photosynthesis. Missing values (NA) indicate rates

625

that were not reported in the original study. Clade

λC3

λCCM

μC3

μCCM

rC3

rCCM

Reference

Poales

0.996

1.454

0.954

1.242

0.042

0.212

(Bouchenak‐ Khelladi et al., 2014)

Poaceaea

0.6924

0.5667

0.5539

0.3267

0.1386

0.24

(Spriggs et al.,

(0.3627)

(0.3011)

(0.2857)

(0.1667)

(0.077)

(0.1344)

2014)

Euphorbia

NA

NA

NA

NA

0.062

0.177

(Horn et al., 2014)

Orchidaceae

0.362

1.482

0.381

1.356

- 0.019

0.13

(Givnish et al., 2015)

Bromelioideae

0.52

1.249

0.115

0.482

0.405

0.767

(Silvestro et al., 2014)

a

Spriggs et al. (2014) included analyses based on two different dating hypotheses. Parentheses show

values for the second phytolith-based dating hypothesis.


26

626

Figure Legends

627 628

Figure 1. (A) Abiotic conditions directly affect plant physiological traits, and the probability that a given

629

species persists with climate change (both in the past and future) is influenced by the degree of

630

phenotypic plasticity in these traits, the ability of populations to migrate and track environmental

631

conditions in space, and the potential for populations to evolve traits that are adaptive in the novel

632

environment. Interactions between plants and other organisms also affect plant physiology, the strength of

633

selection on plants traits, and the probability of persistence. Climate change alters species interactions via

634

direct effects on plant antagonists and mutualists, and via changes in plant traits that influence the

635

dynamics of these interactions. (B) Following an environmental perturbation (vertical dashed line), plant

636

populations with low genetic and/or phenotypic variability are unlikely to persist (red line). Phenotypic

637

plasticity can facilitate tolerance of environmental change over the short term (blue line). Migration to a

638

more favorable environment and/or the evolution of adaptive traits (including greater plasticity) can

639

facilitate long-term responses to environmental change (orange line).

640 641

Figure 2: Consider a hypothetical population that is experiencing increasing aridity owing to climate

642

change. Adaptive plasticity in water use efficiency (WUE) may allow the population to withstand

643

changing conditions. To examine the adaptive value of plasticity, researchers quantify WUE in well

644

watered and drought treatments. In well-watered historical conditions, stabilizing selection favors

645

intermediate WUE because plants with low WUE risk desiccation and plants with high WUE have

646

reduced growth. Drought stress shifts the fitness function, such that optimal fitness now occurs at higher

647

levels of WUE. Plasticity is adaptive when the novel trait values produce similar or higher fitness than the

648

former trait values could have achieved under drought conditions. If WUE does not change in drought,

649

then trait canalization could restrict population persistence. Maladaptive plasticity reduces fitness and

650

could lead to population declines.

651


27

652

Figure 3: Physiological and growth responses of glacial and modern Juniperus sp. and Agathis. A)

653

Juniperus ci/ca, B) Agathis ci/ca, C) Juniperus ci, D) Agathis ci. Data are shown as group mean with error

654

bars of one standard deviation. Letters above the error bars represent significance, with different letters

655

indicating p52.8 kyr BP. Modern Agathis were obtained from

658

remnants of old buildings and piers throughout the Awanui region (n=8). Consequently, modern

659

specimens ranged in age from 0.9 to 3.7 kyr BP.

660


28

661

Literature Cited

662

Ackerly DD, Dudley SA, Sultan SE, Schmitt J, Coleman JS, Linder CR, Sandquist DR, Geber MA,

663

Evans AS, Dawson TE, Lechowicz MJ (2000) The evolution of plant ecophysiological traits:

664

Recent advances and future directions. Bioscience 50: 979-995

665

Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising

666

[CO2]: Mechanisms and environmental interactions. Plant, Cell & Environment 30: 258-270

667

Aitken SN, Whitlock MC (2013) Assisted gene flow to facilitate local adaptation to climate change.

668 669

Annual Review of Ecology, Evolution, and Systematics 44: 367-388 Alberto F, Aitken SN, Alía R, González-Martínez SC, Hänninen H, Kremer A, Lefèvre F,

670

Lenormand T, Yeaman S, Whetten R, Savolainen O (2013) Potential for evolutionary

671

responses to climate change - evidence from tree populations. Global Change Biology 19: 1645-

672

1661

673

Alberton O, Kuyper TW, Gorissen A (2007) Competition for nitrogen between Pinus sylvestris and

674

ectomycorrhizal fungi generates potential for negative feedback under elevated CO2. Plant Soil

675

296: 159-172

676 677 678

Alexander JM, Diez JM, Levine JM (2015) Novel competitors shape species' responses to climate change. Nature 525: 515-518 Alnsour M, Ludwig-Muller J (2015) Potentiail effects of climate chagne on plant primary and

679

secondary metabolism and its influence on plant ecological interactions. Endocytobiosis and Cell

680

Research 26: 90-99

681 682

Amano T, Smithers R, Sparks T, Sutherland W (2010) A 250-year index of first flowering dates and its response to temperature changes. Proceedings of the Royal Society B 277: 2451-2457

683

Anderson JT (2016) Plant fitness in a rapidly changing world. New Phytologist 210: 81-87

684

Anderson JT, Inouye D, McKinney A, Colautti R, Mitchell-Olds T (2012) Phenotypic plasticity and

685

adaptive evolution contribute to advancing flowering phenology in response to climate change.

686

Proceedings of the Royal Society B 279: 3843-3852


29

687

Arakaki M, Christin PA, Nyffeler R, Lendel A, Eggli U, Ogburn RM, Spriggs E, Moore MJ,

688

Edwards EJ (2011) Contemporaneous and recent radiations of the world's major succulent plant

689

lineages. Proceedings of the National Academy of Sciences 108: 8379-8384

690 691 692

Badyaev AV (2005) Stress-induced variation in evolution: From behavioural plasticity to genetic assimilation. Proceedings of the Royal Society B 272: 877-886 Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, Butterfield J, Buse A,

693

Coulson JC, Farrar J, Good JEG, Harrington R, Hartley S, Jones TH, Lindroth RL, Press

694

MC, Symrnioudis I, Watt AD, Whittaker JB (2002) Herbivory in global climate change

695

research: direct effects of rising temperature on insect herbivores. Global Change Biology 8: 1-16

696

Barton BT, Beckerman AP, Schmitz OJ (2009) Climate warming strengthens indirect interactions in an

697 698

old-field food web. Ecology 90: 2346-2351 Battipaglia G, Saurer M, Cherubini P, Calfapietra C, McCarthy H, Norby R, Cotrufo M (2013)

699

Elevated CO2 increases tree-level intrinsic water use efficiency: insights from carbon and oxygen

700

isotope analyses in tree rings across three forest FACE sites. New Phytologist 197: 544-554

701

Becklin KM, Medeiros JS, Sale KR, Ward JK (2014) Evolutionary history underlies plant

702

physiological responses to global change since the last glacial maximum. Ecology Letters 17:

703

691-699

704 705 706 707 708 709 710

Beerling DJ (2005) Evolutionary responses of land plants to atmospheric CO2. In A history of atmospheric CO2 and its effects on plants, animals, and ecosystems. Springer, pp 114-132 Beerling DJ, Chaloner WG, Huntley B, Pearson JA, Tooley MJ (1993) Stomatal density responds to the glacial cycle of environmental change. Proceedings of the Royal Society B 251: 133-138 Berner R (2006) GEOCARBSULF: a combined model for Phanerozoic atmospheric O2 and CO2. Geochimica et Cosmochimica Acta 70: 5653-5664 Besnard G, Muasya AM, Russier F, Roalson EH, Salamin N, Christin PA (2009) Phylogenomics of

711

C4 photosynthesis in sedges (Cyperaceae): multiple appearances and genetic convergence.

712

Molecular Biology and Evolution 26: 1909-1919


30

713

Bever JD (2015) Preferential allocation, physio-evolutionary feedbacks, and the stability and

714

environmental patterns of mutualism between plants and their root symbionts. New Phytologist

715

205: 1503-1514

716 717 718

Billington HL, Pelham J (1991) Genetic variation in the date of budburst in Scottish birch populations: Implications for climate change. Functional Ecology 5: 403-409 Bone RE, Smith JA, Arrigo N, Buerki S (2015) A macro-ecological perspective on crassulacean acid

719

metabolism (CAM) photosynthesis evolution in Afro-Madagascan drylands: Eulophiinae orchids

720

as a case study. New Phytologist 208: 469-481

721 722 723 724 725 726 727 728 729 730 731 732 733 734 735

Bouchenak‐Khelladi Y, Muasya AM, Linder HP (2014) A revised evolutionary history of Poales: origins and diversification. Botanical Journal of the Linnean Society 175: 4-16 Bridle J, Vines T (2007) Limits to evolution at range margins: when and why does adaptation fail? Trends in Ecology & Evolution 22: 140-147 Brodie JF, Post E, Watson F, Berger J (2012 ) Climate change intensification of herbivore impacts on tree recruitment. Proceedings of the Royal Society B 279: 1366-1370 CaraDonna PJ, Iler AM, Inouye D (2014) Shifts in flowering phenology reshape a subalpine plant community. Proceedings of the National Academy of Sciences 111: 4916-4921 Cardinal S, Danforth BN (2013) Bees diversified in the age of eudicots. Proceedings of the Royal Society B 280: DOI: 10.1098/rspb.2012.2686 Carmona D, Fornoni J (2013) Herbivores can select for mixed defensive strategies in plants. New Phytologist 197: 576-585 Chevin L-M, Lande R, Mace G (2010) Adaptation, plasticity, and extinction in a changing environment: Towards a predictive theory. PLOS Biology 8: e1000357 Christin P-A, Osborne CP, Chatelet DS, Columbus JT, Besnard G, Hodkinson TR, Garrison LM,

736

Vorontsova MS, Edwards EJ (2013) Anatomical enablers and the evolution of C4

737

photosynthesis in grasses. Proceedings of the National Academy of Sciences 110: 1381-1386


31

738

Christin PA, Boxall SF, Gregory R, Edwards EJ, Hartwell J, Osborne CP (2013) Parallel recruitment

739

of multiple genes into C4 photosynthesis. Genome Biology and Evolution 5: 2174-2187

740

Christin PA, Edwards EJ, Besnard G, Boxall SF, Gregory R, Kellogg EA, Hartwell J, Osborne CP

741

(2012) Adaptive evolution of C4 photosynthesis through recurrent lateral gene transfer. Current

742

Biology 22: 445-449

743 744 745 746 747

Christin PA, Osborne CP, Sage RF, Arakaki M, Edwards EJ (2011) C4 eudicots are not younger than C4 monocots. Journal of Experimental Botany 62: 3171-3181 Compant S, Van Der Heijden MG, Sessitsch A (2010) Climate change effects on beneficial plant– microorganism interactions. FEMS Microbiology Ecology 73: 197-214 Conner JK, Karoly K, Stewart C, Koelling VA, Sahli HF, Shaw FH (2011) Rapid independent trait

748

evolution despite a strong pleiotropic genetic correlation. The American Naturalist 178: 429-441

749

Cook BI, Wolkovich EM, Parmesan C (2012) Divergent responses to spring and winter warming drive

750

community level flowering trends. Proceedings of the National Academy of Sciences 109: 9000-

751

9005

752

Copolovici L, Kannaste A, Remmel T, Niinemets U (2014) Volatile organic compound emissions from

753

Alnus glutinosa under interacting drought and herbivory stresses. Environmental and

754

Experimental Botany 100: 55-63

755 756 757 758 759

Correa A, Strasser RJ, Martins-Loucao MA (2006) Are mycorrhiza always beneficial? Plant & Soil 279: 65-73 Currano ED, Labandeira CC, Wilf P (2010) Fossil insect folivory tracks paleotemperature for six million years. Ecological Monographs 80: 547-567 D'Costa DM, Palmer J, Hogg A, Turney C, Fifield LK, Ogen J (2008) Stratigraphy, pollen, and 14C

760

dating of Johnston's Gum Hole, a late Quaternary fossil kauri (Agathis australis) site, Northland,

761

New Zealand. Journal of Quaternary Science 24: 47-59

762 763

Dawson T, Mambelli S, Plamboeck A, Templer P, Tu K (2002) Stable isotopes in plant ecology. Annual Review of Ecology and Systematics 33: 507-559


32

764

DeLucia EH, Casteel CL, Nabity PD, O'Neill BF (2008) Insects take a bigger bite out of plants in a

765

warmer, higher carbon dioxide world. Proceedings of the National Academy of Sciences 105:

766

1781-1782

767 768 769 770 771 772

DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution 13: 77-81 Dippery JK, Tissue DT, Thomas RB, Strain BR (1995) Effects of low and elevated CO2 on C3 and C4 annuals: 1. Growth and biomass allocation. Oecologia 101: 13-20 Donohue K (2003) Setting the stage: Phenotypic plasticity as habitat selection. International Journal of Plant Sciences 164: S79-S92

773

Dupont YL, Hansen DM, Rasmussen JT, Olesen JM (2004) Evolutionary changes in nectar sugar

774

composition associated with switches between bird and insect pollination: the Canarian bird-

775

flower element revisited. Functional Ecology 18: 670-676

776 777 778

Easlon H, Carlisle E, McKay J, Bloom A (2015) Does low stomatal conductance or photosynthetic capacity enhance growth at elevated CO2 in Arabidopsis? Plant Physiology 167: 793-799 Edwards EJ, Ogburn RM (2012) Angiosperm responses to a low-CO2 world: CAM and C4

779

photosynthesis as parallel evolutionary trajectories. International Journal of Plant Sciences 173:

780

724-733

781 782 783 784 785 786 787 788

Edwards EJ, Osborne CP, Strömberg CAE, Smith SA, Consortium CG (2010) The origins of C4 grasslands: Integrating evolutionary and ecosystem science. Science 328: 587-591 Edwards EJ, Smith SA (2010) Phylogenetic analyses reveal the shady history of C4 grasses. Proceedings of the National Academy of Sciences 107: 2532-2537 Ehleringer JR, Cerling TE (1995) Atmospheric CO2 and the ratio of intercellular to ambient CO2 concentrations in plants. Tree Physiology 15: 105-111 Ehleringer JR, Cerling TE, Helliker BR (1997) C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112: 285-299


33

789 790 791

Ehleringer JR, Monson RK (1993) Evolutionary and ecological aspects of photosynthetic pathway variation. Annual Review of Ecology and Systematics: 411-439 Eller ASD, McGuire KL, Sparks JP (2011) Responses of sugar maple and hemlock seedlings to

792

elevated carbon dioxide under altered above- and belowground nitrogen sources. Tree Physiology

793

31: 391-401

794 795 796 797 798 799 800 801 802 803 804 805 806

Elliot M, Neall V, Wallace C (2005) A Late Quaternary pollen record from Lake Tongonge, far northern New Zealand. Review of Palaeobotany and Palynology 136: 143-158 Elzinga JA, Atlan A, Biere A, Gigord L, Weis A, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. Trends in Ecology & Evolution 22: 432-439 Etterson JR, Shaw RG (2001) Constraint to adaptive evolution in response to global warming. Science 294: 151-154 Falconer D, Mackay T (1996) Introduction to Quantitative Genetics, Ed 4. Harlow: Addison Wesley Longman Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40: 503-537 Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annual Review of Plant Biology 54: 357-374 Forrest J, Miller-Rushing AJ (2010) Toward a synthetic understanding of the role of phenology in

807

ecology and evolution. Philosophical Transactions of the Royal Society of London B 365: 3101-

808

3112

809 810 811

Forrest J, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecological Monographs 81: 469-491 Forrest JRK (2015) Plant–pollinator interactions and phenological change: what can we learn about

812

climate impacts from experiments and observations? Oikos 124: 4-13

813

Frankham R (2005) Genetics and extinction. Biological Conservation 126: 131-140


34

814 815

Franks P, Beerling D (2009) CO2-forced evolution of plant gas exchange capacity and water-use efficiency over the Phanerozoic. Geobiology 7: 227-236

816

Franks S, Sim S, Weis A (2007) Rapid evolution of flowering time by an annual plant in response to a

817

climate fluctuation. Proceedings of the National Academy of Sciences 104: 1278-1282

818 819 820

Franks SJ, Weber JJ, Aitken SN (2014) Evolutionary and plastic responses to climate change in terrestrial plant populations. Evolutionary Applications 7: 123-139 Galen C (2000) High and dry: Drought stress, sex-allocation trade-offs, and selection on flower size in

821

the alpine wildflower Polemonium viscosum (Polemoniaceae). The American Naturalist 156: 72-

822

83

823 824 825 826 827 828

Galloway LF, Etterson JR (2007) Transgenerational plasticity is adaptive in the wild. Science 318: 1134-1136 Geber M, Griffen LR (2003) Inheritance and natural selection on functional traits. International Journal of Plant Science 164: S21-S42 Gerhart LM, Harris JM, Nippert JB, Sandquist DR, Ward JK (2012) Glacial trees from the La Brea tar pits show physiological constraints of low CO2. New Phytologist 194: 63-69

829

Gerhart LM, Ward JK (2010) Plant responses to low [CO2] of the past. New Phytologist 188: 674-695

830

Gilman RT, Fabina NS, Abbott KC, Rafferty NE (2012) Evolution of plant–pollinator mutualisms in

831 832 833 834 835 836

response to climate change. Evolutionary Applications 5: 2-16 Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD (2010) A framework for community interactions under climate change. Trends in Ecology & Evolution 25: 325-331 Givnish TJ (1987) Comparative studies of leaf form: Assessing the relative roles of selective pressures and phylogenetic constraints. New Phytologist 106: 131-160 Givnish TJ, Spalink D, Ames M, Lyon SP, Hunter SJ, Zuluaga A, Iles WJ, Clements MA, Arroyo

837

MT, Leebens-Mack J, Endara L, Kriebel R, Neubig KM, Whitten WM, Williams NH,

838

Cameron KM (2015) Orchid phylogenomics and multiple drivers of their extraordinary

839

diversification. Proceedings of the Royal Society B 282: DOI: 10.1098/rspb.2015.1553


35

840

Gulbranson E, Ryberg P (2013) Paleobotanical and geochemical approaches to studying fossil tree

841

rings: Quantitative interpretations of paleoenvironment and ecophysiology. Palaios 28: DOI:

842

10.2110/palo.2013.SO2112

843

Gunderson CA, O'Hara KH, Campion CM, Walker AV, Edwards NT (2010) Thermal plasticity of

844

photosynthesis: the role of acclimation in forest responses to a warming climate. Global Change

845

Biology 16: 2272-2286

846 847

Hatch MD (1987) C4 photosynthesis: a unique elend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta (BBA)-Reviews on Bioenergetics 895: 81-106

848

Hausmann N, Juenger T, Sen S, Stowe K, Dawson T, Simms E (2005) Quantitative trait loci affecting

849

delta13C and response to differential water availibility in Arabidopsis thaliana. Evolution 59: 81-

850

96

851 852 853

Heard SB, Hauser DL (1995) Key evolutionary innovations and their ecological mechanisms. Historical Biology 10: 151-173 Heschel MS, Sultan S, Glover S, Sloan D (2004) Population differentiation and plastic responses to

854

drought stress in the generalist annual Polygonum persicaria. International Journal of Plant

855

Sciences 165: 817-824

856

Horn JW, Xi Z, Riina R, Peirson JA, Yang Y, Dorsey BL, Berry PE, Davis CC, Wurdack KJ (2014)

857

Evolutionary bursts in Euphorbia (Euphorbiaceae) are linked with photosynthetic pathway.

858

Evolution 68: 3485-3504

859 860 861

Horrocks M, Nichol SL, Augustinus PC, Barber IG (2007) Late Quaternary environments, vegetation and agriculture in northern New Zealand. Journal of Quaternary Science 22: 267-279 IPCC (2013) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the

862

Fifth Assessment Report of the Intergovernmental Panel on Climate Change. In TF Stocker, D

863

Qin, G-K Plattner, M Tignor, SK Allen, J Boschung, A Nauels, Y Xia, V Bex, PM Midgley, eds,

864

Cambridge, United Kingdom and New York, NY, USA, p 1535


36

865 866 867

Johnson D, Gilbert L (2015) Interplant signalling through hyphal networks. New Phytologist 205: 14481453 Johnson MTJ, Agrawal AA, Maron JL, Salminen JP (2009) Heritability, covariation and natural

868

selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment.

869

Journal of Evolutionary Biology 22: 1295-1307

870 871 872 873 874 875 876 877 878 879

Johnson NC, Wilson GWT, Wilson JA, Miller RM, Bowker MA (2015) Mycorrhizal phenotypes and the Law of the Minimum. New Phytologist 205: 1473-1484 Jump AS, Peñuelas J (2005) Running to stand still: Adaptation and the response of plants to rapid climate change. Ecology Letters 8: 1010-1020 Keuskamp DH, Sasidharan R, Pierik R (2010) Physiological regulation and functional significance of shade avoidance responses to neighbors. Plant Signaling & Behavior 5: 655-662 Kiers TE, Palmer TM, Ives AR, Bruno JF, Bronstein JL (2010) Mutualisms in a changing world: an evolutionary perspective. Ecology Letters 13: 1459-1474 Kimball S, Gremer JR, Angert AL, Huxman TE, Venable DL (2012) Fitness and physiology in a variable environment. Oecologia 169: 319-329

880

Kirkpatrick M, Barton NH (1997) Evolution of a species' range. American Naturalist 150: 1-23

881

Kremer A, Potts BM, Delzon S (2014) Genetic divergence in forest trees: understanding the

882 883

consequences of climate change. Functional Ecology 28: 22-36 Kurz WA, Dymond CC, Stinson G, Rampley GJ, Neilson ET, Carroll AL, Ebata T, Safranyik L

884

(2008) Mountain pine beetle and forest carbon feedback to climate change. Nature 452: 987-990

885

Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37: 1210-

886

1226

887

Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel

888

environments. Proceedings of the National Academy of Sciences 109: 14058-14062

889 890

Lau J, Shaw R, Reich P, Tiffin P (2014) Indirect effects drive evolutionary responses to global change. New Phytologist 201: 335-343


37

891 892

Lehto T, Zwiazek JJ (2011) Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21: 7190

893

Leimu R, Mutikainen PIA, Koricheva J, Fischer M (2006) How general are positive relationships

894

between plant population size, fitness and genetic variation? Journal of Ecology 94: 942-952

895

Lenoir J, Gégout J, Marquet P, de Ruffray P, Brisse H (2008) A significant upward shift in plant

896 897 898 899

species optimum elevation during the 20th Century. Science 320: 1768-1771 Lenormand T (2002) Gene flow and the limits to natural selection. Trends in Ecology & Evolution 17: 183-189 Liancourt P, Boldgiv B, Song DS, Spence LA, Helliker BR, Petraitis PS, Casper BB (2015) Leaf-trait

900

plasticity and species vulnerability to climate change in a Mongolian steppe. Global Change

901

Biology 21: 3489-3498

902 903 904 905 906 907 908 909 910

Liu Y, Reich PB, Li G, Sun S (2011) Shifting phenology and abundance under experimental warming alters trophic relationships and plant reproductive capacity. Ecology 92: 1201-1207 Loarie SR, Duffy PB, Hamilton H, Asner GP, Field CB, Ackerly DD (2009) The velocity of climate change. Nature 462: 1052-1055 Maddison WP, Midford PE, Otto SP (2007) Estimating a binary character's effect on speciation and extinction. Systematic Biology 56: 701-710 Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proceedings of the Royal Society of London B: Biological Sciences 273: 2575-2584 Mayewski PA, Rohling EE, Curt Stager J, Karlén W, Maasch KA, David Meeker L, Meyerson EA,

911

Gasse F, van Kreveld S, Holmgren K, Lee-Thorp J, Rosqvist G, Rack F, Staubwasser M,

912

Schneider RR, Steig EJ (2004) Holocene climate variability. Quaternary Research 62: 243-255

913

Medeiros J, Ward J (2013) Increasing atmospheric [CO2] from glacial to future concentrations affects

914

drought tolerance via impacts on leaves, xylem and their integrated function. New Phytologist

915

199: 738-748


38

916 917 918 919 920 921 922 923 924

Medvigy D, Beaulieu C (2012) Trends in daily solar radiation and precipitation coefficients of variation since 1984. Journal of Climate 25: 1330-1339 Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant– pollinator interactions. Ecology Letters 10: 710-717 Merilä J (2012) Evolution in response to climate change: In pursuit of the missing evidence. BioEssays 34: 811-818 Miller-Struttmann N, Galen C (2014) High-altitude multi-taskers: bumble bee food plant use broadens along an altitudinal productivity gradient. Oecologia 176: 1033-1045 Miller-Struttmann NE, Geib JC, Franklin JD, Kevan PG, Holdo RM, Ebert-May D, Lynn AM,

925

Kettenbach JA, Hedrick E, Galen C (2015) Functional mismatch in a bumble bee pollination

926

mutualism under climate change. Science 349: 1541-1544

927 928 929 930 931

Mitchell-Olds T (1996) Pleiotropy causes long-term genetic constraints on life-history evolution in Brassica rapa. Evolution 50: 1849-1858 Mitchell-Olds T, Willis JH, Goldstein DB (2007) Which evolutionary processes influence natural genetic variation for phenotypic traits? Nature Reviews Genetics 8: 845-856 Mitton JB, Ferrenberg SM, Natural History Editor: Craig WB (2012) Mountain pine beetle develops

932

an unprecedented summer generation in response to climate warming. The American Naturalist

933

179: E163-E171

934

Mohan JE, Cowden CC, Baas P, Dawadi A, Frankson PT, Helmick K, Hughes E, Khan S, Lang A,

935

Machmuller M, Taylor M, Witt CA (2014) Mycorrhizal fungi mediation of terrestrial

936

ecosystem responses to global change: Mini-review. Fungal Ecology 10: 3-19

937

Monson RK, Littlejohn Jr RO, Williams Iii GJ (1983) Photosynthetic adaptation to temperature in four

938

species from the Colorado shortgrass steppe: A physiological model for coexistence. Oecologia

939

58: 43-51

940 941

Muir CD (2015) Making pore choices: Repeated regime shifts in stomatal ratio. Proceedings of the Royal Society B 282: 20151498


39

942

Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan

943

M, Richards CL, Valladares F, van Kleunen M (2010) Plant phenotypic plasticity in a

944

changing climate. Trends in Plant Science 15: 684-692

945 946

Norby RJZ, Donald R. (2011) Ecological lessons from free-air CO2 enrichment (FACE) experiments. Annual Review of Ecology, Evolution, and Systematics 42: 181-203

947

Núñez-Farfán J, Fornoni J, Valverde PL (2007) The Evolution of Resistance and Tolerance to

948

Herbivores. Annual Review of Ecology, Evolution, and Systematics 38: 541-566

949

O'Hara NB, Rest JS, Franks SJ (2016) Increased susceptibility to fungal disease accompanies

950 951 952 953 954 955 956 957 958 959 960

adaptation to drought in Brassica rapa. Evolution 70: 241-248 Pagel M (1994) Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proceedings of the Royal Society B 255: 37-45 PAGES 2k Consortium (2013) Continental-scale temperature variability during the past two millennia. Nature Geoscience 6: 339-346 Perry A, Low P, Ellis J, Reynolds J (2005) Climate Change and Distribution Shifts in Marine Fishes. Science 308: 1912-1915 Pineda A, Dicke M, Pieterse CMJ, Pozo MJ (2013) Beneficial microbes in a changing environment: are they always helping plants to deal with insects? Functional Ecology 27: 574-586 Polley HW, Johnson HB, Marino BD, Mayeux HS (1993) Increase in C3 plant water-use efficiency and biomass over glacial to present CO2 concentrations. Nature 361: 61-64

961

Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H (2009) Phylogenetic trait

962

conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi.

963

Proceedings of the Royal Society B: Biological Sciences 276: 4237-4245

964 965 966 967

Rabosky DL (2014) Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLOS ONE 9: e89543 Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecology Letters 14: 476-483


40

968 969 970

Reinhart KO, Wilson GWT, Rinella MJ (2012) Predicting plant responses to mycorrhizae: integrating evolutionary history and plant traits. Ecology Letters 15: 689-695 Robinson EA, Ryan GD, Newman JA (2012) A meta-analytic review of the effects of elevated CO2 on

971

plant-arthropod interactions highlights the importance of interacting environmental and biological

972

variables. New Phytologist 194: 321-336

973

Rothwell GW, Wyatt SE, Tomescu AMF (2014) Plant evolution at the interface of paleontology and

974

developmental biology: An organism-centered paradigm. American Journal of Botany 101: 899-

975

913

976 977 978 979 980 981 982

Royer D (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Review of Palaeobotany and Palynology 114: 1-28 Sage RF, Christin P-A, Edwards EJ (2011) The C4 plant lineages of planet Earth. Journal of Experimental Botany 62: 3155-3169 Sage RF, Coleman JR (2001) Effects of low atmospheric CO2 on plants: More than a thing of the past. Trends in Plant Science 6: 18-24 Sage RF, Cowling SA (1999) Implications of stress in low CO2 atmospheres of the past: Are today's

983

plants too conservative for a high CO2 world? In Y Luo, HA Mooney, eds, Carbon dioxide and

984

environmental stress. Academic Press, New York, NY

985 986 987

Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Annual Review of Plant Biology 63: 19-47 Sandquist D, Ehleringer J (2003) Carbon isotope discrimination differences within and between

988

contrasting populations of Encelia farinosa raised under common-environment conditions.

989

Oecologia: 463-470

990 991 992 993

Schluter D, Price T, Mooers AØ, Ludwig D (1997) Likelihood of ancestor states in adaptive radiation. Evolution 51: 1699-1711 Schmitt J, Wulff RD (1993) Light spectral quality, phytochrome and plant competition. Trends in Ecology & Evolution 8: 47-51


41

994 995 996 997 998 999 1000 1001

Shaw RG, Etterson JR (2012) Rapid climate change and the rate of adaptation: insight from experimental quantitative genetics. New Phytologist 195: 752-765 Shefferson RP, Salguero-Gómez R (2015) Eco-evolutionary dynamics in plants: Interactive processes at overlapping time-scales and their implications. Journal of Ecology 103: 789-797 Sherry R, Zhou X, Gu S, Arnone III J, Schimel D, Verburg P, Wallace L, Luo Y (2007) Divergence of reproductive phenology under climate warming. Proceedings of the National Academy of Sciences 104: 198-202 Silvestro D, Zizka G, Schulte K (2014) Disentangling the effects of key innovations on the

1002

diversification of Bromelioideae (bromeliaceae). Evolution 68: 163-175

1003

Simpson GG (1953) Major features of evolution. Columbia University Press, New York

1004

Smith SE, Read D (2008) Mycorrhizal Symbiosis, Ed 3rd. Academic Press, London

1005

Spriggs EL, Christin PA, Edwards EJ (2014) C4 photosynthesis promoted species diversification

1006 1007 1008 1009 1010 1011

during the Miocene grassland expansion. PLOS ONE 9: e97722 Springer CJ, Orozco RA, Kelly JK, Ward JK (2008) Elevated CO2 influences the expression of floralinitiation genes in Arabidopsis thaliana. New Phytologist 178: 63-67 Tripati AK, Roberts CD, Eagle RA (2009) Coupling of CO2 and ice sheet stability over major climate transitions of the last 20 million years. Science 326: 1394-1397 Voelker SL, Brooks JR, Meinzer FC, Anderson R, Bader MKF, Battipaglia G, Becklin KM,

1012

Beerling D, Bert D, Betancourt JL, Dawson TE, Domec J-C, Guyette RP, Körner C, Leavitt

1013

SW, Linder S, Marshall JD, Mildner M, Ogée J, Panyushkina I, Plumpton HJ, Pregitzer

1014

KS, Saurer M, Smith AR, Siegwolf RTW, Stambaugh MC, Talhelm AF, Tardif JC, Van de

1015

Water PK, Ward JK, Wingate L (2016) A dynamic leaf gas-exchange strategy is conserved in

1016

woody plants under changing ambient CO2: evidence from carbon isotope discrimination in paleo

1017

and CO2 enrichment studies. Global Change Biology 22: 889-902


42

1018

Wahl V, Ponnu J, Schlereth A, Arrivault Sp, Langenecker T, Franke A, Feil R, Lunn JE, Stitt M,

1019

Schmid M (2013) Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis

1020

thaliana. Science 339: 704-707

1021 1022 1023 1024 1025

Wang T, O'Neill GA, Aitken SN (2010) Integrating environmental and genetic effects to predict responses of tree populations to climate. Ecological Applications 20: 153-163 Ward J, Roy DS, Chatterjee I, Bone CR, Springer C, Kelly JK (2012) Identification of a major QTL that alters flowering time at elevated [CO2] in Arabidopsiss thaliana. PLOS ONE 7: e49028 Ward JK (2005) Evolution and growth of plants in a low CO2 world. In J Ehleringer, T Cerling, D

1026

Dearing, eds, A History of Atmospheric CO2 and Its Effects on Plants, Animals, and Ecosystems.

1027

Springer-Verlag, pp 232-257

1028 1029 1030 1031

Ward JK, Antonovics J, Thomas RB, Strain BR (2000) Is atmospheric CO2 a selective agent on model C3 annuals? Oecologia 123: 330-341 Ward JK, Kelly J (2004) Scaling up evolutionary responses to elevated CO2: Lessons from Arabidopsis. Ecology Letters 7: 427-440

1032

Watanabe CK, Sato S, Yanagisawa S, Uesono Y, Terashima I, Noguchi K (2014) Effects of elevated

1033

CO2 on levels of primary metabolites and transcripts of genes encoding respiratory enzymes and

1034

their diurnal patterns in Arabidopsis thaliana: Possible relationships with respiratory rates. Plant

1035

and Cell Physiology 55: 341-357

1036

Wilczek AM, Cooper MD, Korves TM, Schmitt J (2014) Lagging adaptation to warming climate in

1037

Arabidopsis thaliana. Proceedings of the National Academy of Sciences 111: 7906-7913

1038

Winter K, Smith JAC (1996) An introduction to crassulacean acid metabolism. Biochemical principles

1039 1040

and ecological diversity. In Crassulacean acid metabolism. Springer, pp 1-13 Ziska LH, Pettis JS, Edwards J, Hancock JE, Tomecek MB, Clark A, Dukes JS, Loladze I, Polley

1041

HW (2016) Rising atmospheric CO2 is reducing the protein concentration of a floral pollen

1042

source essential for North American bees. Proceedings of the Royal Society B 283: DOI:

1043

10.1098/rspb.2016.0414


43

A

Plant physiology Climate change

Biotic community

Probability of persistence

B

Plasticity Migration Evolution

Species persistence

Low genetic and/or phenotypic variability Phenotypic plasticity Migration and/or adaptive evolution

Environmental perturbation Time

Figure 1. (A) Abiotic conditions directly affect plant physiological traits, and the probability that a given species persists with climate change (both in the past and future) is influenced by the degree of phenotypic plasticity in these traits, the ability of populations to migrate and track environmental conditions in space, and the potential for populations to evolve traits that are adaptive in the novel environment. Interactions between plants and other organisms also affect plant physiology, the strength of selection on plants traits, and the probability of persistence. Climate change alters species interactions via direct effects on plant antagonists and mutualists, and via changes in plant traits that influence the dynamics of these interactions. (B) Following an environmental perturbation (vertical dashed line), plant populations with low genetic and/or phenotypic variability are unlikely to persist (red line). Phenotypic plasticity can facilitate tolerance of environmental change over the short term (blue line). Migration to a more favorable environment and/or the evolution of adaptive traits (including greater plasticity) can facilitate long-term responses to environmental change (orange line).

Maladaptive

Canalized

Fitness

Adaptive

Well-watered Drought Water-use efficiency

Figure 2: Consider a hypothetical population that is experiencing Figure 2: Consider a hypothetical population increasing aridity owing to climate change. Adaptive plasticity inthat i water use efficiencyincreasing (WUE) may allow the population to withstand experiencing aridity in its home site ow changing conditions. To examine the adaptive value of plasticity, climate change. Adaptive plasticity in water use ef researchers quantify WUE in well-watered and drought treatments. In well-watered historical conditions,tostabilizing (WUE) may allow the population withstand cha selection favors intermediate WUE because plants with low WUE conditions. To plants examine theWUE adaptive valuegrowth. of plast risk dessication and with high have reduced Drought shifts the fitness function, suchunder that optimal WUEstress is assessed experimentally bothfitness now occurs at higher levels of WUE. Plasticity is adaptive when well-watered and drought the novel trait values produce similarconditions. or higher fitnessUnder than thethe former trait values could have achieved under drought conditions. well-watered historical conditions, stabilizing sele If WUE does not change in drought, then trait canalization could favors intermediate values of WUE because restrict population persistence. Maladaptive plasticity reducesplants fitness and could lead to population declines. low WUE risk mortality and plants with high WUE

0.9

ci/ca

0.8

A

B a

a

0.7 a

0.6

a a

0.5 0.4 0.3 200

C

b

D

ci (ppm)

180 160

a

140 120

a

100 Juniperus Glacial Modern

Agathis Glacial Modern

Figure 3: Physiological and growth responses of glacial and modern Juniperus sp. and Agathis. A) Juniperus ci/ca, B) Agathis ci/ca, C) Juniperus ci, D) Agathis ci. Data are shown as group mean with error bars of one standard deviation. Letters above the error bars represent significance, with different letters indicating p52.8 kyr BP. Modern Agathis were obtained from remnants of old buildings and piers throughout the Awanui region (n=8). Consequently, modern specimens ranged in age from 0.9 to 3.7 kyr BP.

Parsed Citations Ackerly DD, Dudley SA, Sultan SE, Schmitt J, Coleman JS, Linder CR, Sandquist DR, Geber MA, Evans AS, Dawson TE, Lechowicz MJ (2000) The evolution of plant ecophysiological traits: Recent advances and future directions. Bioscience 50: 979-995 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: Mechanisms and environmental interactions. Plant, Cell & Environment 30: 258-270 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Aitken SN, Whitlock MC (2013) Assisted gene flow to facilitate local adaptation to climate change. Annual Review of Ecology, Evolution, and Systematics 44: 367-388 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Alberto F, Aitken SN, Alía R, González-Martínez SC, Hänninen H, Kremer A, Lefèvre F, Lenormand T, Yeaman S, Whetten R, Savolainen O (2013) Potential for evolutionary responses to climate change - evidence from tree populations. Global Change Biology 19: 1645-1661 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Alberton O, Kuyper TW, Gorissen A (2007) Competition for nitrogen between Pinus sylvestris and ectomycorrhizal fungi generates potential for negative feedback under elevated CO2. Plant Soil 296: 159-172 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Alexander JM, Diez JM, Levine JM (2015) Novel competitors shape species' responses to climate change. Nature 525: 515-518 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Alnsour M, Ludwig-Muller J (2015) Potentiail effects of climate chagne on plant primary and secondary metabolism and its influence on plant ecological interactions. Endocytobiosis and Cell Research 26: 90-99 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Amano T, Smithers R, Sparks T, Sutherland W (2010) A 250-year index of first flowering dates and its response to temperature changes. Proceedings of the Royal Society B 277: 2451-2457 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Anderson JT (2016) Plant fitness in a rapidly changing world. New Phytologist 210: 81-87 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Anderson JT, Inouye D, McKinney A, Colautti R, Mitchell-Olds T (2012) Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proceedings of the Royal Society B 279: 3843-3852 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Arakaki M, Christin PA, Nyffeler R, Lendel A, Eggli U, Ogburn RM, Spriggs E, Moore MJ, Edwards EJ (2011) Contemporaneous and recent radiations of the world's major succulent plant lineages. Proceedings of the National Academy of Sciences 108: 8379-8384 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Badyaev AV (2005) Stress-induced variation in evolution: From behavioural plasticity to genetic assimilation. Proceedings of the Royal Society B 272: 877-886 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, Butterfield J, Buse A, Coulson JC, Farrar J, Good JEG, Harrington R, Hartley S, Jones TH, Lindroth RL, Press MC, Symrnioudis I, Watt AD, Whittaker JB (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology 8: 1-16 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Barton BT, Beckerman AP, Schmitz OJ (2009) Climate warming strengthens indirect interactions in an old-field food web. Ecology 90: 2346-2351 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Battipaglia G, Saurer M, Cherubini P, Calfapietra C, McCarthy H, Norby R, Cotrufo M (2013) Elevated CO2 increases tree-level intrinsic water use efficiency: insights from carbon and oxygen isotope analyses in tree rings across three forest FACE sites. New Phytologist 197: 544-554 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Becklin KM, Medeiros JS, Sale KR, Ward JK (2014) Evolutionary history underlies plant physiological responses to global change since the last glacial maximum. Ecology Letters 17: 691-699 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Beerling DJ (2005) Evolutionary responses of land plants to atmospheric CO2. In A history of atmospheric CO2 and its effects on plants, animals, and ecosystems. Springer, pp 114-132 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Beerling DJ, Chaloner WG, Huntley B, Pearson JA, Tooley MJ (1993) Stomatal density responds to the glacial cycle of environmental change. Proceedings of the Royal Society B 251: 133-138 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Berner R (2006) GEOCARBSULF: a combined model for Phanerozoic atmospheric O2 and CO2. Geochimica et Cosmochimica Acta 70: 5653-5664 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Besnard G, Muasya AM, Russier F, Roalson EH, Salamin N, Christin PA (2009) Phylogenomics of C4 photosynthesis in sedges (Cyperaceae): multiple appearances and genetic convergence. Molecular Biology and Evolution 26: 1909-1919 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Bever JD (2015) Preferential allocation, physio-evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts. New Phytologist 205: 1503-1514 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Billington HL, Pelham J (1991) Genetic variation in the date of budburst in Scottish birch populations: Implications for climate change. Functional Ecology 5: 403-409 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Bone RE, Smith JA, Arrigo N, Buerki S (2015) A macro-ecological perspective on crassulacean acid metabolism (CAM) photosynthesis evolution in Afro-Madagascan drylands: Eulophiinae orchids as a case study. New Phytologist 208: 469-481 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Bouchenak-Khelladi Y, Muasya AM, Linder HP (2014) A revised evolutionary history of Poales: origins and diversification. Botanical Journal of the Linnean Society 175: 4-16 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Bridle J, Vines T (2007) Limits to evolution at range margins: when and why does adaptation fail? Trends in Ecology & Evolution 22: 140-147 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Brodie JF, Post E, Watson F, Berger J (2012 ) Climate change intensification of herbivore impacts on tree recruitment. Proceedings of the Royal Society B 279: 1366-1370 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

CaraDonna PJ, Iler AM, Inouye D (2014) Shifts in flowering phenology reshape a subalpine plant community. Proceedings of the

National Academy of Sciences 111: 4916-4921 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Cardinal S, Danforth BN (2013) Bees diversified in the age of eudicots. Proceedings of the Royal Society B 280: DOI: 10.1098/rspb.2012.2686 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Carmona D, Fornoni J (2013) Herbivores can select for mixed defensive strategies in plants. New Phytologist 197: 576-585 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Chevin L-M, Lande R, Mace G (2010) Adaptation, plasticity, and extinction in a changing environment: Towards a predictive theory. PLOS Biology 8: e1000357 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Christin P-A, Osborne CP, Chatelet DS, Columbus JT, Besnard G, Hodkinson TR, Garrison LM, Vorontsova MS, Edwards EJ (2013) Anatomical enablers and the evolution of C4 photosynthesis in grasses. Proceedings of the National Academy of Sciences 110: 1381-1386 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Christin PA, Boxall SF, Gregory R, Edwards EJ, Hartwell J, Osborne CP (2013) Parallel recruitment of multiple genes into C4 photosynthesis. Genome Biology and Evolution 5: 2174-2187 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Christin PA, Edwards EJ, Besnard G, Boxall SF, Gregory R, Kellogg EA, Hartwell J, Osborne CP (2012) Adaptive evolution of C4 photosynthesis through recurrent lateral gene transfer. Current Biology 22: 445-449 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Christin PA, Osborne CP, Sage RF, Arakaki M, Edwards EJ (2011) C4 eudicots are not younger than C4 monocots. Journal of Experimental Botany 62: 3171-3181 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Compant S, Van Der Heijden MG, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiology Ecology 73: 197-214 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Conner JK, Karoly K, Stewart C, Koelling VA, Sahli HF, Shaw FH (2011) Rapid independent trait evolution despite a strong pleiotropic genetic correlation. The American Naturalist 178: 429-441 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Cook BI, Wolkovich EM, Parmesan C (2012) Divergent responses to spring and winter warming drive community level flowering trends. Proceedings of the National Academy of Sciences 109: 9000-9005 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Copolovici L, Kannaste A, Remmel T, Niinemets U (2014) Volatile organic compound emissions from Alnus glutinosa under interacting drought and herbivory stresses. Environmental and Experimental Botany 100: 55-63 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Correa A, Strasser RJ, Martins-Loucao MA (2006) Are mycorrhiza always beneficial? Plant & Soil 279: 65-73 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Currano ED, Labandeira CC, Wilf P (2010) Fossil insect folivory tracks paleotemperature for six million years. Ecological Monographs 80: 547-567 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

D'Costa DM, Palmer J, Hogg A, Turney C, Fifield LK, Ogen J (2008) Stratigraphy, pollen, and 14C dating of Johnston's Gum Hole, a late Quaternary fossil kauri (Agathis australis) site, Northland, New Zealand. Journal of Quaternary Science 24: 47-59 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Dawson T, Mambelli S, Plamboeck A, Templer P, Tu K (2002) Stable isotopes in plant ecology. Annual Review of Ecology and Systematics 33: 507-559 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

DeLucia EH, Casteel CL, Nabity PD, O'Neill BF (2008) Insects take a bigger bite out of plants in a warmer, higher carbon dioxide world. Proceedings of the National Academy of Sciences 105: 1781-1782 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution 13: 77-81 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Dippery JK, Tissue DT, Thomas RB, Strain BR (1995) Effects of low and elevated CO2 on C3 and C4 annuals: 1. Growth and biomass allocation. Oecologia 101: 13-20 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Donohue K (2003) Setting the stage: Phenotypic plasticity as habitat selection. International Journal of Plant Sciences 164: S79S92 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Dupont YL, Hansen DM, Rasmussen JT, Olesen JM (2004) Evolutionary changes in nectar sugar composition associated with switches between bird and insect pollination: the Canarian bird-flower element revisited. Functional Ecology 18: 670-676 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Easlon H, Carlisle E, McKay J, Bloom A (2015) Does low stomatal conductance or photosynthetic capacity enhance growth at elevated CO2 in Arabidopsis? Plant Physiology 167: 793-799 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Edwards EJ, Ogburn RM (2012) Angiosperm responses to a low-CO2 world: CAM and C4 photosynthesis as parallel evolutionary trajectories. International Journal of Plant Sciences 173: 724-733 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Edwards EJ, Osborne CP, Strömberg CAE, Smith SA, Consortium CG (2010) The origins of C4 grasslands: Integrating evolutionary and ecosystem science. Science 328: 587-591 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Edwards EJ, Smith SA (2010) Phylogenetic analyses reveal the shady history of C4 grasses. Proceedings of the National Academy of Sciences 107: 2532-2537 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Ehleringer JR, Cerling TE (1995) Atmospheric CO2 and the ratio of intercellular to ambient CO2 concentrations in plants. Tree Physiology 15: 105-111 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Ehleringer JR, Cerling TE, Helliker BR (1997) C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112: 285-299 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Ehleringer JR, Monson RK (1993) Evolutionary and ecological aspects of photosynthetic pathway variation. Annual Review of Ecology and Systematics: 411-439 Pubmed: Author and Title CrossRef: Author and Title

Google Scholar: Author Only Title Only Author and Title

Eller ASD, McGuire KL, Sparks JP (2011) Responses of sugar maple and hemlock seedlings to elevated carbon dioxide under altered above- and belowground nitrogen sources. Tree Physiology 31: 391-401 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Elliot M, Neall V, Wallace C (2005) A Late Quaternary pollen record from Lake Tongonge, far northern New Zealand. Review of Palaeobotany and Palynology 136: 143-158 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Elzinga JA, Atlan A, Biere A, Gigord L, Weis A, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. Trends in Ecology & Evolution 22: 432-439 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Etterson JR, Shaw RG (2001) Constraint to adaptive evolution in response to global warming. Science 294: 151-154 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Falconer D, Mackay T (1996) Introduction to Quantitative Genetics, Ed 4. Harlow: Addison Wesley Longman Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40: 503-537 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annual Review of Plant Biology 54: 357-374 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Forrest J, Miller-Rushing AJ (2010) Toward a synthetic understanding of the role of phenology in ecology and evolution. Philosophical Transactions of the Royal Society of London B 365: 3101-3112 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Forrest J, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecological Monographs 81: 469-491 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Forrest JRK (2015) Plant-pollinator interactions and phenological change: what can we learn about climate impacts from experiments and observations? Oikos 124: 4-13 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Frankham R (2005) Genetics and extinction. Biological Conservation 126: 131-140 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Franks P, Beerling D (2009) CO2-forced evolution of plant gas exchange capacity and water-use efficiency over the Phanerozoic. Geobiology 7: 227-236 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Franks S, Sim S, Weis A (2007) Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proceedings of the National Academy of Sciences 104: 1278-1282 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Franks SJ, Weber JJ, Aitken SN (2014) Evolutionary and plastic responses to climate change in terrestrial plant populations. Evolutionary Applications 7: 123-139 Pubmed: Author and Title CrossRef: Author and Title


Galen C (2000) High and dry: Drought stress, sex-allocation trade-offs, and selection on flower size in the alpine wildflower Polemonium viscosum (Polemoniaceae). The American Naturalist 156: 72-83 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Galloway LF, Etterson JR (2007) Transgenerational plasticity is adaptive in the wild. Science 318: 1134-1136 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Geber M, Griffen LR (2003) Inheritance and natural selection on functional traits. International Journal of Plant Science 164: S21S42 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Gerhart LM, Harris JM, Nippert JB, Sandquist DR, Ward JK (2012) Glacial trees from the La Brea tar pits show physiological constraints of low CO2. New Phytologist 194: 63-69 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Gerhart LM, Ward JK (2010) Plant responses to low [CO2] of the past. New Phytologist 188: 674-695 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Gilman RT, Fabina NS, Abbott KC, Rafferty NE (2012) Evolution of plant-pollinator mutualisms in response to climate change. Evolutionary Applications 5: 2-16 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD (2010) A framework for community interactions under climate change. Trends in Ecology & Evolution 25: 325-331 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Givnish TJ (1987) Comparative studies of leaf form: Assessing the relative roles of selective pressures and phylogenetic constraints. New Phytologist 106: 131-160 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Givnish TJ, Spalink D, Ames M, Lyon SP, Hunter SJ, Zuluaga A, Iles WJ, Clements MA, Arroyo MT, Leebens-Mack J, Endara L, Kriebel R, Neubig KM, Whitten WM, Williams NH, Cameron KM (2015) Orchid phylogenomics and multiple drivers of their extraordinary diversification. Proceedings of the Royal Society B 282: DOI: 10.1098/rspb.2015.1553 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Gulbranson E, Ryberg P (2013) Paleobotanical and geochemical approaches to studying fossil tree rings: Quantitative interpretations of paleoenvironment and ecophysiology. Palaios 28: DOI: 10.2110/palo.2013.SO2112 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Gunderson CA, O'Hara KH, Campion CM, Walker AV, Edwards NT (2010) Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate. Global Change Biology 16: 2272-2286 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Hatch MD (1987) C4 photosynthesis: a unique elend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta (BBA)-Reviews on Bioenergetics 895: 81-106 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Hausmann N, Juenger T, Sen S, Stowe K, Dawson T, Simms E (2005) Quantitative trait loci affecting delta13C and response to differential water availibility in Arabidopsis thaliana. Evolution 59: 81-96 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Heard SB, Hauser DL (1995) Key evolutionary innovations and their ecological mechanisms. Historical Biology 10: 151-173 Pubmed: Author and Title

CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Heschel MS, Sultan S, Glover S, Sloan D (2004) Population differentiation and plastic responses to drought stress in the generalist annual Polygonum persicaria. International Journal of Plant Sciences 165: 817-824 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Horn JW, Xi Z, Riina R, Peirson JA, Yang Y, Dorsey BL, Berry PE, Davis CC, Wurdack KJ (2014) Evolutionary bursts in Euphorbia (Euphorbiaceae) are linked with photosynthetic pathway. Evolution 68: 3485-3504 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Horrocks M, Nichol SL, Augustinus PC, Barber IG (2007) Late Quaternary environments, vegetation and agriculture in northern New Zealand. Journal of Quaternary Science 22: 267-279 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

IPCC (2013) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. In TF Stocker, D Qin, G-K Plattner, M Tignor, SK Allen, J Boschung, A Nauels, Y Xia, V Bex, PM Midgley, eds, Cambridge, United Kingdom and New York, NY, USA, p 1535 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Johnson D, Gilbert L (2015) Interplant signalling through hyphal networks. New Phytologist 205: 1448-1453 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Johnson MTJ, Agrawal AA, Maron JL, Salminen JP (2009) Heritability, covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment. Journal of Evolutionary Biology 22: 1295-1307 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Johnson NC, Wilson GWT, Wilson JA, Miller RM, Bowker MA (2015) Mycorrhizal phenotypes and the Law of the Minimum. New Phytologist 205: 1473-1484 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Jump AS, Peñuelas J (2005) Running to stand still: Adaptation and the response of plants to rapid climate change. Ecology Letters 8: 1010-1020 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Keuskamp DH, Sasidharan R, Pierik R (2010) Physiological regulation and functional significance of shade avoidance responses to neighbors. Plant Signaling & Behavior 5: 655-662 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Kiers TE, Palmer TM, Ives AR, Bruno JF, Bronstein JL (2010) Mutualisms in a changing world: an evolutionary perspective. Ecology Letters 13: 1459-1474 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Kimball S, Gremer JR, Angert AL, Huxman TE, Venable DL (2012) Fitness and physiology in a variable environment. Oecologia 169: 319-329 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Kirkpatrick M, Barton NH (1997) Evolution of a species' range. American Naturalist 150: 1-23 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Kremer A, Potts BM, Delzon S (2014) Genetic divergence in forest trees: understanding the consequences of climate change. Functional Ecology 28: 22-36 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Kurz WA, Dymond CC, Stinson G, Rampley GJ, Neilson ET, Carroll AL, Ebata T, Safranyik L (2008) Mountain pine beetle and forest

carbon feedback to climate change. Nature 452: 987-990 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37: 1210-1226 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proceedings of the National Academy of Sciences 109: 14058-14062 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Lau J, Shaw R, Reich P, Tiffin P (2014) Indirect effects drive evolutionary responses to global change. New Phytologist 201: 335343 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Lehto T, Zwiazek JJ (2011) Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21: 71-90 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Leimu R, Mutikainen PIA, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? Journal of Ecology 94: 942-952 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Lenoir J, Gégout J, Marquet P, de Ruffray P, Brisse H (2008) A significant upward shift in plant species optimum elevation during the 20th Century. Science 320: 1768-1771 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Lenormand T (2002) Gene flow and the limits to natural selection. Trends in Ecology & Evolution 17: 183-189 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Liancourt P, Boldgiv B, Song DS, Spence LA, Helliker BR, Petraitis PS, Casper BB (2015) Leaf-trait plasticity and species vulnerability to climate change in a Mongolian steppe. Global Change Biology 21: 3489-3498 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Liu Y, Reich PB, Li G, Sun S (2011) Shifting phenology and abundance under experimental warming alters trophic relationships and plant reproductive capacity. Ecology 92: 1201-1207 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Loarie SR, Duffy PB, Hamilton H, Asner GP, Field CB, Ackerly DD (2009) The velocity of climate change. Nature 462: 1052-1055 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Maddison WP, Midford PE, Otto SP (2007) Estimating a binary character's effect on speciation and extinction. Systematic Biology 56: 701-710 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proceedings of the Royal Society of London B: Biological Sciences 273: 2575-2584 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Mayewski PA, Rohling EE, Curt Stager J, Karlén W, Maasch KA, David Meeker L, Meyerson EA, Gasse F, van Kreveld S, Holmgren K, Lee-Thorp J, Rosqvist G, Rack F, Staubwasser M, Schneider RR, Steig EJ (2004) Holocene climate variability. Quaternary Research 62: 243-255 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Medeiros J, Ward J (2013) Increasing atmospheric [CO2] from glacial to future concentrations affects drought tolerance via

impacts on leaves, xylem and their integrated function. New Phytologist 199: 738-748 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Medvigy D, Beaulieu C (2012) Trends in daily solar radiation and precipitation coefficients of variation since 1984. Journal of Climate 25: 1330-1339 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecology Letters 10: 710-717 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Merilä J (2012) Evolution in response to climate change: In pursuit of the missing evidence. BioEssays 34: 811-818 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Miller-Struttmann N, Galen C (2014) High-altitude multi-taskers: bumble bee food plant use broadens along an altitudinal productivity gradient. Oecologia 176: 1033-1045 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Miller-Struttmann NE, Geib JC, Franklin JD, Kevan PG, Holdo RM, Ebert-May D, Lynn AM, Kettenbach JA, Hedrick E, Galen C (2015) Functional mismatch in a bumble bee pollination mutualism under climate change. Science 349: 1541-1544 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Mitchell-Olds T (1996) Pleiotropy causes long-term genetic constraints on life-history evolution in Brassica rapa. Evolution 50: 1849-1858 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Mitchell-Olds T, Willis JH, Goldstein DB (2007) Which evolutionary processes influence natural genetic variation for phenotypic traits? Nature Reviews Genetics 8: 845-856 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Mitton JB, Ferrenberg SM, Natural History Editor: Craig WB (2012) Mountain pine beetle develops an unprecedented summer generation in response to climate warming. The American Naturalist 179: E163-E171 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Mohan JE, Cowden CC, Baas P, Dawadi A, Frankson PT, Helmick K, Hughes E, Khan S, Lang A, Machmuller M, Taylor M, Witt CA (2014) Mycorrhizal fungi mediation of terrestrial ecosystem responses to global change: Mini-review. Fungal Ecology 10: 3-19 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Monson RK, Littlejohn Jr RO, Williams Iii GJ (1983) Photosynthetic adaptation to temperature in four species from the Colorado shortgrass steppe: A physiological model for coexistence. Oecologia 58: 43-51 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Muir CD (2015) Making pore choices: Repeated regime shifts in stomatal ratio. Proceedings of the Royal Society B 282: 20151498 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan M, Richards CL, Valladares F, van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends in Plant Science 15: 684-692 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Norby RJZ, Donald R. (2011) Ecological lessons from free-air CO2 enrichment (FACE) experiments. Annual Review of Ecology, Evolution, and Systematics 42: 181-203 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Núñez-Farfán J, Fornoni J, Valverde PL (2007) The Evolution of Resistance and Tolerance to Herbivores. Annual Review of Ecology, Evolution, and Systematics 38: 541-566 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

O'Hara NB, Rest JS, Franks SJ (2016) Increased susceptibility to fungal disease accompanies adaptation to drought in Brassica rapa. Evolution 70: 241-248 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Pagel M (1994) Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proceedings of the Royal Society B 255: 37-45 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

PAGES 2k Consortium (2013) Continental-scale temperature variability during the past two millennia. Nature Geoscience 6: 339346 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Perry A, Low P, Ellis J, Reynolds J (2005) Climate Change and Distribution Shifts in Marine Fishes. Science 308: 1912-1915 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Pineda A, Dicke M, Pieterse CMJ, Pozo MJ (2013) Beneficial microbes in a changing environment: are they always helping plants to deal with insects? Functional Ecology 27: 574-586 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Polley HW, Johnson HB, Marino BD, Mayeux HS (1993) Increase in C3 plant water-use efficiency and biomass over glacial to present CO2 concentrations. Nature 361: 61-64 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proceedings of the Royal Society B: Biological Sciences 276: 4237-4245 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Rabosky DL (2014) Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLOS ONE 9: e89543 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecology Letters 14: 476-483 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Reinhart KO, Wilson GWT, Rinella MJ (2012) Predicting plant responses to mycorrhizae: integrating evolutionary history and plant traits. Ecology Letters 15: 689-695 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Robinson EA, Ryan GD, Newman JA (2012) A meta-analytic review of the effects of elevated CO2 on plant-arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytologist 194: 321-336 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Rothwell GW, Wyatt SE, Tomescu AMF (2014) Plant evolution at the interface of paleontology and developmental biology: An organism-centered paradigm. American Journal of Botany 101: 899-913 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Royer D (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Review of Palaeobotany and Palynology 114: 1-28 Pubmed: Author and Title

CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Sage RF, Christin P-A, Edwards EJ (2011) The C4 plant lineages of planet Earth. Journal of Experimental Botany 62: 3155-3169 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Sage RF, Coleman JR (2001) Effects of low atmospheric CO2 on plants: More than a thing of the past. Trends in Plant Science 6: 18-24 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Sage RF, Cowling SA (1999) Implications of stress in low CO2 atmospheres of the past: Are today's plants too conservative for a high CO2 world? In Y Luo, HA Mooney, eds, Carbon dioxide and environmental stress. Academic Press, New York, NY Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Annual Review of Plant Biology 63: 19-47 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Sandquist D, Ehleringer J (2003) Carbon isotope discrimination differences within and between contrasting populations of Encelia farinosa raised under common-environment conditions. Oecologia: 463-470 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Schluter D, Price T, Mooers AØ, Ludwig D (1997) Likelihood of ancestor states in adaptive radiation. Evolution 51: 1699-1711 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Schmitt J, Wulff RD (1993) Light spectral quality, phytochrome and plant competition. Trends in Ecology & Evolution 8: 47-51 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Shaw RG, Etterson JR (2012) Rapid climate change and the rate of adaptation: insight from experimental quantitative genetics. New Phytologist 195: 752-765 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Shefferson RP, Salguero-Gómez R (2015) Eco-evolutionary dynamics in plants: Interactive processes at overlapping time-scales and their implications. Journal of Ecology 103: 789-797 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Sherry R, Zhou X, Gu S, Arnone III J, Schimel D, Verburg P, Wallace L, Luo Y (2007) Divergence of reproductive phenology under climate warming. Proceedings of the National Academy of Sciences 104: 198-202 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Silvestro D, Zizka G, Schulte K (2014) Disentangling the effects of key innovations on the diversification of Bromelioideae (bromeliaceae). Evolution 68: 163-175 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Simpson GG (1953) Major features of evolution. Columbia University Press, New York Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Smith SE, Read D (2008) Mycorrhizal Symbiosis, Ed 3rd. Academic Press, London Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Spriggs EL, Christin PA, Edwards EJ (2014) C4 photosynthesis promoted species diversification during the Miocene grassland expansion. PLOS ONE 9: e97722 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Springer CJ, Orozco RA, Kelly JK, Ward JK (2008) Elevated CO2 influences the expression of floral-initiation genes in Arabidopsis thaliana. New Phytologist 178: 63-67 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Tripati AK, Roberts CD, Eagle RA (2009) Coupling of CO2 and ice sheet stability over major climate transitions of the last 20 million years. Science 326: 1394-1397 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Voelker SL, Brooks JR, Meinzer FC, Anderson R, Bader MKF, Battipaglia G, Becklin KM, Beerling D, Bert D, Betancourt JL, Dawson TE, Domec J-C, Guyette RP, Körner C, Leavitt SW, Linder S, Marshall JD, Mildner M, Ogée J, Panyushkina I, Plumpton HJ, Pregitzer KS, Saurer M, Smith AR, Siegwolf RTW, Stambaugh MC, Talhelm AF, Tardif JC, Van de Water PK, Ward JK, Wingate L (2016) A dynamic leaf gas-exchange strategy is conserved in woody plants under changing ambient CO2: evidence from carbon isotope discrimination in paleo and CO2 enrichment studies. Global Change Biology 22: 889-902 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Wahl V, Ponnu J, Schlereth A, Arrivault Sp, Langenecker T, Franke A, Feil R, Lunn JE, Stitt M, Schmid M (2013) Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339: 704-707 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Wang T, O'Neill GA, Aitken SN (2010) Integrating environmental and genetic effects to predict responses of tree populations to climate. Ecological Applications 20: 153-163 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Ward J, Roy DS, Chatterjee I, Bone CR, Springer C, Kelly JK (2012) Identification of a major QTL that alters flowering time at elevated [CO2] in Arabidopsiss thaliana. PLOS ONE 7: e49028 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Ward JK (2005) Evolution and growth of plants in a low CO2 world. In J Ehleringer, T Cerling, D Dearing, eds, A History of Atmospheric CO2 and Its Effects on Plants, Animals, and Ecosystems. Springer-Verlag, pp 232-257 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Ward JK, Antonovics J, Thomas RB, Strain BR (2000) Is atmospheric CO2 a selective agent on model C3 annuals? Oecologia 123: 330-341 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Ward JK, Kelly J (2004) Scaling up evolutionary responses to elevated CO2: Lessons from Arabidopsis. Ecology Letters 7: 427-440 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Watanabe CK, Sato S, Yanagisawa S, Uesono Y, Terashima I, Noguchi K (2014) Effects of elevated CO2 on levels of primary metabolites and transcripts of genes encoding respiratory enzymes and their diurnal patterns in Arabidopsis thaliana: Possible relationships with respiratory rates. Plant and Cell Physiology 55: 341-357 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Wilczek AM, Cooper MD, Korves TM, Schmitt J (2014) Lagging adaptation to warming climate in Arabidopsis thaliana. Proceedings of the National Academy of Sciences 111: 7906-7913 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Winter K, Smith JAC (1996) An introduction to crassulacean acid metabolism. Biochemical principles and ecological diversity. In Crassulacean acid metabolism. Springer, pp 1-13 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Ziska LH, Pettis JS, Edwards J, Hancock JE, Tomecek MB, Clark A, Dukes JS, Loladze I, Polley HW (2016) Rising atmospheric CO2 is reducing the protein concentration of a floral pollen source essential for North American bees. Proceedings of the Royal Society B 283: DOI: 10.1098/rspb.2016.0414 Pubmed: Author and Title CrossRef: Author and Title
