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Sex allocation theory predicts that parents are selected to bias their progeny sex ratio (SR) toward the sex that will benefit the most from parental quality.
B R I E F C O M M U N I C AT I O N doi:10.1111/evo.12908

Better-surviving barn swallow mothers produce more and better-surviving sons Andrea Romano,1,2 Alessandra Costanzo,1 Manuela Caprioli,1 Marco Parolini,1 Roberto Ambrosini,3 Diego Rubolini,1 and Nicola Saino1,4 1

Department of Biosciences, University of Milan, I-20133, Milan, Italy 2


E-mail: [email protected]

Department of Earth and Environmental Sciences (DISAT), University of Milano-Bicocca, I-20126, Milan, Italy 4

E-mail: [email protected]

Received October 21, 2015 Accepted March 8, 2016 Sex allocation theory predicts that parents are selected to bias their progeny sex ratio (SR) toward the sex that will benefit the most from parental quality. Because parental quality may differentially affect survival of sons and daughters, a pivotal test of the adaptive value of SR adjustment is whether parents overproduce offspring of the sex that accrues larger fitness advantages from high parental quality. However, this crucial test of the long-term fitness consequences of sex allocation decisions has seldom been performed. In this study of the barn swallow (Hirundo rustica), we showed a positive correlation between the proportion of sons and maternal annual survival. We then experimentally demonstrated that this association did not depend on the differential costs of rearing offspring of either sex. Finally, we showed that maternal lifespan positively predicted lifespan of sons but not of daughters. Because in barn swallows lifespan is a strong determinant of lifetime reproductive success, the results suggest that mothers overproduce offspring of the sex that benefits the most from maternal quality. Hence, irrespective of mechanisms causing the SR bias and mother–son covariation in lifespan, we provide strong evidence that sex allocation decisions of mothers can highly impact on their lifetime fitness. KEY WORDS:

Barn swallow, lifespan, lifetime fitness, sex allocation, sex ratio, survival.

In most populations of sexually reproducing organisms, offspring are approximately equally likely to be male or female (Fisher 1930; West 2009). Balanced population sex ratios are believed to evolve because of frequency-dependent selection for the production of offspring of the underrepresented sex (Fisher 1930). However, individual parents can diverge in their interests in the production of sons or daughters (Frank 1990; Kokko and Jennions 2008; West 2009). Facultative adjustment of allocation of parental investment to either sex, resulting in unbalanced progeny sex ratio (SR), is predicted to evolve whenever differences exist in the relative parental fitness returns from producing sons or daughters, and cues exist that allow parents to anticipate sex-dependent differences in offspring fitness, or variation in ecological conditions at the time of breeding predicts sex-dependent differences in offspring fitness (Frank 1990; West 2009; Komdeur 2012).  C


2016 The Author(s). Evolution

The reproductive value of sons relative to daughters can vary according to several factors. These include social effects mediated by the SR of the siblings or of sexually mature adults in the population, which affects mating opportunities (Owens and Thompson 1994; Uller 2006), environmental quality, which differently influence quality of sons and daughters (Tschirren et al. 2003; Bize et al. 2005), and parents’ general body condition, because this will differentially affect their ability to produce better-surviving sons or daughters (Trivers and Willard 1973; Nager et al. 1999; Westerdahl et al. 2000). Relative reproductive value of sons and daughters can also depend on the genetic quality of biological parents in terms of heritable sexually selected traits (Fawcett et al. 2007; Roulin et al. 2010; Booksmythe et al. 2013, 2015), as well as on relatedness between parents (Sardell and DuVal 2014). Trivers and Willard (1973) originally suggested that mothers in relatively good conditions should overproduce sons, because variance in


reproductive success is often larger for males than females, and mothers in good condition may disproportionately increase breeding success of sons as compared to daughters. The scope of this “maternal-quality” hypothesis has subsequently been expanded to include not only the direct influences of maternal condition on the offspring when they reach independence or sexual maturity, but also any influence that the quality of the mother and the environmental conditions that she sets for her offspring have on their survival and reproductive success (West 2009; Komdeur 2012). Many studies of sex allocation refer to birds, where female heterogamety may relax mechanistic constraints to sex allocation arising because of chromosomal sex determination (Komdeur and Pen 2002; West and Sheldon 2002). While adaptive sex allocation has thus been shown to depend on the social, environmental, or sexual selection context (Ellegren et al. 1996; Komdeur et al. 1997; Komdeur 1998; Nager et al. 1999; Westerdahl et al. 2000; Roulin et al. 2010; Bowers et al. 2015; Romano et al. 2015), several other studies have not identified adaptive patterns of sex allocation (Pagliani et al. 1999; Saino et al. 1999b; Radford and Blakey 2000; Leech et al. 2001). Hence, generalizations on the conditions under which adaptive sex allocation occurs have proven elusive (Hewison and Gaillard 1999; West and Sheldon 2002; Cassey et al. 2006). In many species, lifespan is a good proxy for lifetime fitness, since lifespan predicts the number of reproductive events (Newton 1989). Because high parental quality may differentially contribute to lifespan of male and female offspring, a crucial test of hypotheses on adaptive sex allocation is whether parents skew the offspring SR in favor of the sex that benefits the most from high parental lifespan. Due to the difficulty of simultaneously gathering information on lifespan of parents and SR and lifespan of the offspring, variation in sex allocation in relation to parental contribution to lifespan of sons and daughters has very seldom been tested (Komdeur 1998; Roulin et al. 2010). In addition, the evolutionary interpretation of individual-level variation in sex allocation decisions of parents in relation to their survival rests on the discrimination between the alternative pathways of causation that can produce this association. First, those parents that happen to produce more sons or, conversely, daughters pay different survival costs of reproduction. Alternatively, bettersurviving parents overproduce offspring of the sex that will profit the most from the factors that enhance parental survival. These alternative mechanisms have profoundly different evolutionary implications, and can only be ascertained using an experimental approach. In this study of the barn swallow (Hirundo rustica), a socially monogamous, semicolonial, migratory passerine bird, we used correlational data to test if parental annual survival is associated with offspring SR. Because this analysis showed that bettersurviving mothers produced more sons, we relied on experiments



where the SR and the size of the brood were manipulated to test if the positive covariation between maternal survival and brood SR reflected an effect of brood sex composition on maternal survival. Because annual maternal survival did not depend on manipulation of brood SR, we speculated that the covariation between maternal survival and brood SR might rather reflect adaptive allocation by better-surviving mothers toward male offspring, which are the sex that accrue larger fitness benefits from maternal longevity. We therefore specifically tested the prediction that any positive correlation of maternal lifespan on offspring lifespan was stronger for sons compared to daughters.

Materials and Methods Full methodological details are given in the Supplementary Information. We studied barn swallows in Northern Italy (Lombardia and Piemonte) over the period 1994–2015 at 23 breeding colonies ( = farms), where we did intensive capture and individual marking of the breeding adults. Breeding pairs were identified by direct observation of markings of the adults attending their nest. Capture efficacy, in terms of proportion of adults captured relative to the individuals that were present at the colony, was likely very high, as determined by the small proportion ( 0.39). However, in a different analysis where brood SR was related to parental survival in binomial linear-mixed models with year as random effect, the proportion of male offspring increased with annual maternal survival (F1,410 = 11.98, P = 0.0006, binomial coefficient: 0.345 (0.100); Fig. 1). This was not the case for paternal survival, that negatively and nonsignificantly predicted brood SR (F1,351 = 1.74, P = 0.189, binomial coefficient: 0.140 (0.107); Fig. 1). In a set of 24 pairs where both members survived and remated in consecutive years, brood SR was found to be significantly



based on 362 broods for fathers (1461 nestlings) and on 421 broods (1683 nestlings) for mothers. Offspring of surviving mothers were significantly more likely to be male.

repeatable between years, as indicated by a likelihood ratio test (χ2 1 = 6.54, P = 0.011). EXPERIMENTAL BROOD SEX RATIO AND SIZE MANIPULATION, AND PARENTAL SURVIVAL

In a sample of 182 broods whose size and SR were manipulated, we found no effect of change in brood SR on annual survival of mothers (F1,89 = 0.52, P = 0.474) and fathers (F1,89 = 0.24, P = 0.627) (Table S1; Fig. S1). Annual survival of parental males attending an enlarged brood was significantly lower (by ca. 18%) than that of males attending a reduced brood (F1,89 = 7.30, P = 0.008; Table S1; Fig. S2). The negative effect of brood enlargement on survival of females (13%) was smaller compared to that of males, and marginally statistically significant (F1,89 = 4.00, P = 0.049;



Lifespan of offspring in relation to lifespan of their mother. Lifespan (mean ± SEM) of male (n = 83) or female (n = 22) offspring in relation to lifespan of their mother. The squared sym-

Figure 2.

bols indicate offspring right-censored data. Symbols of increasing size represent 1, 2 or, respectively 4 overlaying data points. Lifespan of sons significantly increased with maternal lifespan.

Table S1; Fig. S2). The effect of brood size manipulation on parental survival did not depend on change in brood SR, as shown by the nonsignificant effect of the interaction between brood size treatment and change in SR (Table S1). LIFESPAN OF SONS AND DAUGHTERS IN RELATION TO MATERNAL LIFESPAN

In a shared frailty model with colony of origin as a random effect, the relationship between offspring and maternal lifespan differed according to offspring sex (Table 2; Fig. 2). Consistently with the expectation, the hazard of death of sons from one year to the next significantly declined with maternal lifespan, whereas the hazard of death of daughters nonsignificantly increased with maternal lifespan (Table 2; Fig. 2). In this model, the significant random effect of colony implies that lifespan varied among colonies of origin. In a model where we also included the effect of the offspring being recruited in their natal or in another colony, we found no significant effect of the three-way interaction with sex and maternal lifespan (χ2 1 = 0.58, P = 0.398). Hence, the relationship between maternal and offspring lifespan did not differ between offspring that were recruited in their natal or in another colony, implying that the inclusion in the sample of mostly philopatric individuals was unlikely to bias the results. Significant offspring sex by maternal lifespan effects on offspring lifespan were confirmed in alternative models where we included colony of recruitment (effect of the sex by maternal lifespan interaction: χ2 1 = 4.24, P = 0.037) or, respectively, maternal identity (effect of the sex by maternal lifespan interaction: χ2 1 = 3.94, P = 0.035) as random factors, instead of colony of origin.

The proportion of barn swallow offspring that were male and maternal survival were found to be positively associated. Because manipulation of brood SR did not affect parental survival, the positive covariation of brood SR and maternal survival is consistent with the hypothesis that better-surviving mothers produce more sons. Maternal lifespan, which integrates the information on individual annual survival, positively predicted lifespan of sons, but not of daughters. Hence, barn swallow mothers overproduce offspring of the sex that benefits the most from maternal quality as reflected by survival. In its widest proposition, sex allocation theory predicts that parents should adjust the SR of their progeny when the fitness of sons relative to daughters varies with extrinsic conditions or parental quality, and/or when the costs of rearing offspring of either sex differ. Evidence for adaptive SR adjustment has been provided in a number of instances (reviewed in Frank 1990 West and Sheldon 2002; ; West 2009; Komdeur 2012; Booksmythe et al. 2015). Yet, it is still equivocal, as a number of studies could identify no effects of candidate factors nor adaptive interpretations of the observed sex allocation patterns. Lack of evidence may potentially be due to broadly diverse circumstances, including temporal or geographical variation in sex allocation strategies (Budden and Beissinger 2004; Rubenstein 2007; Romano et al. 2015), peri-natal mortality blurring the patterns of offspring SR variation, and low power of statistical tests based on relatively small samples (Cassey et al. 2006). Patchiness of the evidence for facultative sex allocation may also arise because of failure in identifying the relevant factors that affect sex allocation decisions, including those parental quality traits that differentially affect the reproductive value of sons and daughters (Komdeur and Pen 2002; West and Sheldon 2002). In principle, sperm competition could also confound the analyses of sex allocation in relation to parental quality because sex allocation decisions may depend on the quality of the biological, extra-pair father of the offspring. In barn swallow colonies, a large proportion of nestlings is sired by a male different from the social mate of the parental mother (Saino et al. 1997b; Hubbard et al. 2015), whereas brood parasitism (i.e. egg laying in other females’ nests) is very rare (Saino et al. 1997b; Boncoraglio et al. 2008). We deem the possibility that extra-pair paternities confounded the analyses of survival in relation to brood SR unlikely. This is the case because mothers seem not to adjust their brood SR according to the phenotypic quality, in terms of sexual attractiveness, of their social as compared to their extra-pair mate (Saino et al. 1999b). Barn swallows are short-lived birds, with a very large fraction of the individuals having one-two breeding seasons in their life (Møller 1994; Saino et al. 1997b; Turner 2006). Breeding success per breeding event is high and relatively homogenous among individuals (Møller 1994; Turner 2006). Hence, lifespan strongly EVOLUTION 2016



Table 2.

Shared frailty model of the hazard of death of male (n = 83) or female (n = 22) offspring in relation to maternal lifespan.

Wald χ2 Colony of origin Sex Maternal lifespan Sex × maternal lifespan ∗

25.88 4.90 12.32 6.29

df 9.44 0.95 0.94 0.94

P 0.0028 0.0248 0.0004 0.0110

Parameter estimate (SE)

Sons: Daughters:

–0.601 (0.171) 0.688 (0.476)

P < 0.001.

Colony of origin was included as a frailty random effect.

positively predicts lifetime reproductive success, because it affects the number of reproductive events. In fact, in a previous study of the same population, a strong positive correlation was found between lifespan and lifetime realized reproductive success (r = 0.89, n = 45) (Saino et al. 2012). Offspring lifespan therefore qualifies as a major component of their fitness, and parents were thus expected to overproduce the sex that benefits the most in terms of longevity from parental viability. Here, we capitalized on information from a long-term study to gather unique information on maternal and offspring lifespan, and maternal sex allocation decisions, and showed that better-surviving mothers favor the production of sons, and this apparently reflects adaptive facultative sex allocation because sons benefit more than daughters from high maternal quality, as maternal lifespan predicts male (but not female) offspring lifespan. However, we note that the result on the nonsignificant association between the lifespan of mothers and daughters should be taken with caution because of the relatively small number of daughters included in the analysis, which is mainly due to female-biased natal dispersal (Turner 2006). Local recruits may not represent a random sample of the offspring, because natal dispersal may covary with specific offspring traits (e.g. Dingemanse et al. 2003; Saino et al. 2014). If mortality varies according to the individual dispersal status, the covariation between the lifespan of mothers and that of all their male offspring could be different from that observed using information on the recruits to their natal colony only (ca. 5% of all offspring produced). However, the three-way interaction between offspring sex, maternal lifespan, and offspring dispersal status was far from statistical significance. While the power of this analysis was probably low because of the small number of dispersing recruits, the three-way interaction effect was very weak and therefore suggests that dispersal status did not bias our analyses. A general link between offspring and maternal lifespan may arise via genetic variation in quality traits. Genetic variation in fitness traits is expected to be low because selection on heritable traits that confer fitness benefits is strong (Price and Schluter 1991). Yet, we observed a highly significant mother–son resemblance in lifespan, and this was the case despite mortality in



the barn swallow is likely largely dependent on environmental stochastic effects. In addition, maternal longevity may promote male offspring longevity because high quality mothers can set favorable early environmental conditions for their offspring (Lindstr¨om 1999; Ricklefs 2006), and sons may be more susceptible than daughters to such epigenetic effects, although we are not aware of any empirical evidence from birds supporting this speculation. Because of the high frequency of extra-pair paternity (Saino et al. 1997b; Hubbard et al. 2015), social father-offspring resemblance would not provide reliable estimates of heritability in lifespan. Unfortunately, we are not in the position of assessing paternity of individual recruits because this would require genotyping of all adult males present in the breeding colonies (i.e. more than 1500 individuals), and tissue samples dating back many years are no longer available. Through an experimental approach, we showed that a change in brood SR did not affect parental survival. This result was compatible with the hypothesis that better-surviving mothers decide in favor of larger allocation to males, but not with the idea that offspring sex determines maternal survival. However, the possibility that producing relatively more females had negative consequences on residual maternal reproductive value cannot be excluded at present. In barn swallow nestlings, sexual dimorphism is minimal (Saino et al. 2002b), but subtle physiological and behavioral differences between male and female offspring (Boncoraglio et al. 2008; Bonisoli-Alquati et al. 2008; Romano et al. 2011) may still cause the costs of parental care to vary according to brood sex composition. In addition, egg production may entail mothers with differential costs depending on offspring sex. This could be the case, for example, if eggs carrying either sex differ in size or biochemical composition and sex-related laying effort has consequences on maternal fecundity or quality of her future progeny. Differently from other passerine species (Magrath et al. 2003; Martyka et al. 2010), in the barn swallow egg size is not related to embryo sex (our unpublished data). Carotenoid and androgen concentrations in the yolk have also been shown not to covary with embryo sex (Saino et al. 2003, 2006). However, maternal antibodies are more concentrated in eggs carrying a female


(Saino et al. 2003). While larger allocation of humoral immune factors may represent a nonnegligible cost to laying females, the consequence of larger investment on this component of egg quality for maternal subsequent breeding performance is unknown. The negative effect of brood enlargement on paternal survival is not novel, as we previously documented (Saino et al. 1999a). Here, we also found that brood enlargement had a marginally significant, negative consequence for maternal survival. These effects likely mirror the cost of reproduction. Parents of experimentally enlarged broods had to attend a number of nestlings two units larger (corresponding to 44% of average brood size and to 2.3 standard deviations of natural broods size) than the number of nestlings attended by parents of reduced broods. Barn swallows respond to increased brood size by increasing their parental workload (Saino et al. 1997a, 1999a). Moreover, nest infestation by hematophagous mites is larger in enlarged broods (Saino et al. 2002c). Increased parental effort and parasitism could mediate the negative effect of brood size on parental survival. Annual maternal survival was nonsignificantly related to brood size in unmanipulated broods (Table 1), and the relationship between paternal survival and brood size was very close to 0. This suggests that barn swallow parents trade annual survival against brood size, obscuring the evidence of the survival cost of reproduction among parents of unmanipulated broods. Theoretical and empirical evolutionary studies of sex allocation date back almost one century. Yet, there is still great uncertainty on how common adaptive sex manipulation is and why observed deviations from random sex allocation are typically weak and inconsistent also within species (Frank 1990; West 2009; Komdeur 2012). Part of this uncertainty may well arise from the difficulties of studying sex allocation in the wild, on large samples, and focusing on major fitness traits, such as lifespan or realized reproductive success, rather than proxies of relative reproductive value of sons and daughters that may not accurately reflect offspring reproductive value. In addition, the mechanistic process of adaptive modulation of offspring SR still remains largely elusive (Komdeur and Pen 2002; West and Sheldon 2002). Irrespective of mechanistic interpretations, however, our results provide unprecedented strong evidence that mothers can bias the SR of their offspring in favor of the sex that will benefit the most in terms of lifetime reproductive success. Hence, our study lends strong empirical support to the large body of theory that predicts the evolution of the parental ability to bias allocation to either sex depending on the differential fitness rewards of producing sons or daughters.

ACKNOWLEDGMENTS We are grateful to all farm owners that allowed us to enter their private properties, and to a number of students who greatly helped during field works. We also thank Wolf Blanckenhorn and two anonymous reviewers

for constructive criticism and useful suggestions that improved a previous version of the manuscript.


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Associate Editor: W. Blanckenhorn Handling Editor: M. Servedio


Supporting Information Additional Supporting Information may be found in the online version of this article at the publisher’s website: Supplementary Information Table S1. Binomial linear mixed models of annual parental survival in relation to brood size manipulation and change in brood sex ratio following the experimental treatment. Pair of broods that were involved in the reciprocal exchange of hatchlings was included as random effect in the models. Figure S1. Annual survival of parents that attended a brood where the number of nestlings and the proportion of offspring of either sex was experimentally manipulated. Figure S2. Annual survival of parents in relation to brood size manipulation.