Trade-Offs Between Flight and Fecundity in the Soybean Aphid - BioOne

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ABSTRACT The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is native to eastern Asia and was accidentally introduced into North America ...


Trade-Offs Between Flight and Fecundity in the Soybean Aphid (Hemiptera: Aphididae) YING ZHANG,1 KONGMING WU,1,2 KRIS A.G. WYCKHUYS,3



J. Econ. Entomol. 102(1): 133Ð138 (2009)

ABSTRACT The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is native to eastern Asia and was accidentally introduced into North America in 2000. Within a few years, it was found throughout the U.S. and Canadian soybean-growing regions. The spread of A. glycines in North America is partly ascribed to its great ßight capacity. We conducted direct measurements of ßight performance of winged A. glycines adults and correlated this to their subsequent longevity and fecundity to determine whether there are trade-offs between ßight and fecundity. We also estimated fecundity and development time of the offspring of females that had ßown varying distances to examine potential maternal effects linked to ßight. The experiment was conducted using a speciÞcally designed aphid ßight mill system in which winged aphids were tethered by their abdomens and ßight duration, distance and speed were quantiÞed. Fecundity, longevity and reproductive periods of 12-h-old A. glycines alates that had engaged in ⬎0.5 km long ßights were signiÞcantly lower than those of ⬍0.5-km individuals. The offspring of alates with ßight experiences of ⬎1.5 km also had lower fecundity than those produced by individuals that had engaged in ßights ⬍1.5 km. Our results are therefore consistent both with direct trade-offs between ßight and fecundity and a trade-off between ßight and fecundity via maternal effects. KEY WORDS Aphis glycines, ßight, development, fecundity, maternal effects

The ability to ßy allows many insects to exploit habitats and resources that would otherwise be inaccessible and has clearly been an important component of their ecological and evolutionary success (Rankin and Burchsted 1992, Dingle 1996). However, life history theory predicts that certain traits trade off with one another, especially when each trait is energetically costly (Zera and Harshman 2001). In insects, a potential trade-off of this kind is the one between ßight and reproduction (Rankin and Burchsted 1992, Gatehouse 1994, Dingle 1996, Roff 2002, Baguette and Schtickzelle 2006, Guerra and Pollack 2007). Support for a trade-off between reproduction and ßight is widespread in wing-dimorphic species (Zera and Denno 1997) and this includes aphids (Dixon and Wratten 1971, Dixon 1972, Wratten 1977, Dixon and Howard 1986, Dixon and Kindlmann 1999, Dixon et al. 1993). A few studies have also shown that winged morphs produce smaller eggs or nymphs than nonwinged morphs do (Dixon and Wratten 1971, Solbreck 1986), indicating that maternal effects can be incorporated into the trade-off. 1 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant protection, Chinese Academy of Agricultural Sciences, Beijing 100094, PeopleÕs Republic of China. 2 Corresponding author, e-mail: [email protected] 3 Horticulture Research Center (CIAA), Universidad Jorge Tadeo Lozano, Chia (Cundinamarca), Colombia. 4 Department of Entomology, University of Minnesota, 219 Hodson Hall, 1980 Folwell Ave., St. Paul, MN 55108.

Studies on the relationship between the degree of ßight and reproduction for dispersive morphs are rare, however, and evidence for a trade-off between ßight and reproduction in this context has been mixed. In butterßies, for example, results of studies for some species are consistent with a trade-off (Hughes et al. 2003, Baguette and Schtickzelle 2006), whereas the Glanville fritillary, Melitaea cinxia (L.) exhibits no such trade-off (Saastamoinen 2007). And in aphids, Cockbain (1961a,b,c) tethered winged morphs (alatae) of the black bean aphid, Aphis fabae Scopoli, onto pinheads and measured longevity and reproduction of individuals that had been ßown to exhaustion. Although ßight-exhausted A. fabae had depleted their glycogen and fat reserves in these experiments (Cockbain 1961a), ßight to exhaustion (3Ð9 h) did not decrease longevity or fecundity of individuals that were placed directly onto plants postßight compared with controls that had been ßown for 15 min (Cockbain 1961b). In nontethered ßight chamber studies, Kennedy and Booth (1963) found that longer ßight duration in A. fabae led to an increased propensity to larviposit, showing that a period of ßight is needed in this species before the bulk of reproduction begins (Kennedy and Booth 1964). Here, we investigate the effect of ßight duration on longevity, fecundity, and offspring reproduction of the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae). The soybean aphid is heteroecious (use of primary and secondary host plants during winter and summer,

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respectively) and holocyclic (sexual morphs produce over-wintering eggs on the primary host), with parthenogenic reproduction during spring and summer (Wu et al. 2004). In spring, A. glycines maintain several generations on Rhamnus spp. before winged aphids (alates) depart and colonize soybean. R. cathartica is the principal overwintering host of soybean aphid in North America (Voegtlin et al. 2005). Soybean aphids develop winged morphs throughout the soybean growing season (i.e., summer migrants) and in early fall (i.e., fall migrants) (Ragsdale et al. 2004, Hodgson et al. 2005). Production of winged soybean aphids is likely triggered by photoperiod, although factors such as temperature, host plant quality, crowding, and presence of natural enemies could also play a role (Hodgson et al. 2005). The soybean aphid is native to eastern Asia and was accidentally introduced to North America in 2000. Within ⬍2 yr of its initial discovery in the United States, A. glycines successfully established and compromised soybean production in ⬎20 U.S. states and three Canadian provinces (Ragsdale et al. 2004, 2007; Venette and Ragsdale 2004). The impressive geographical spread of A. glycines has been ascribed to a combination of passive (wind-aided) and active ßight (Venette and Ragsdale 2004, Zhu et al. 2006, Zhang et al. 2008). Given the status of A. glycines as a successful invasive pest in North America, it would be expected to be adapted both for long-distance ßight and high fecundity (Rankin and Burchsted 1992). We showed recently that 12Ð24-h-old A. glycines exhibited fairly strong ßight capacity (Zhang et al. 2008). Alate individuals ßew actively on ßight mills for a maximum of 11.2 continuous hours (mean ⫾ SEM, 4.3 ⫾ 0.5), which corresponded to a maximum of 18.5 km (5.1 ⫾ 0.7 km). This work also showed that ßight activity peaked when aphids were 12Ð24 h old and declined thereafter. Because reproduction by alates of A. glycines typically begins between 24 and 48 h of attaining the adult stage (see results), this observation is consistent with the “oogenesis-ßight syndrome,” in which reproduction principally occurs after ßight (Johnson 1969, Walters and Dixon 1983, Dixon and Howard 1986, Dingle 1996). Materials and Methods Study Insects. We initiated a laboratory colony of A. glycines with individuals collected in July 2006 from a soybean Þeld in Beijing, China. The laboratory colony was maintained on soybean plants kept under controlled climatic conditions (25⬚C, 75% RH, and a photoperiod of 16:8 [L:D] h). Soybeans (Zhonghuang 13) were sown in regular potting soil and transplanted at the seedling stage into 100-ml glass bottles Þlled with a hydroponic nutrient solution (Wu and Liu 1994). Each soybean plant was infested with several A. glycines adults, and colonies were renewed every 3 d. We collected alatoid nymphs (i.e., older aphid instars with wing pads) from these colonies daily, placed these individually on a clean plant and checked for molting into the winged adult stage (alates) every 8 h. Upon

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Fig. 1. Schematic of a ßight mill apparatus. a,U-shaped steel stand; b, paired magnets; c, copper thread cantilever; d, axial needle; e, plastic bracket; f, photosensor; g, light shade; h, electrical cable; and i, alate aphid glued to the end of the cantilever for ßight.

molting, we kept track of the age of alates that were used in further ßight mill experiments. We selected 12-h-old A. glycines alates and allowed them to engage in ßights of ⬍0.5, 0.5Ð1.5, 1.5Ð2.5, and ⬎2.5 km, with each ßight distance category considered a separate experimental treatment. Next, aphids were removed from the ßight mill apparatus by dipping their abdomen into water at ambient temperature to dissolve the glue (Feng et al. 2004). Live aphids without visible injury were placed individually into 5-cm-diameter petri dishes in which a soybean leaßet was placed on 1% agar (Liu et al. 2003), and kept at 25⬚C, 75% RH, and a photoperiod of 16:8 (L:D) h. Soybean leaßets were renewed every 3 d, and aphids were checked daily for longevity and nymphal production. Nymphs were removed from petri dishes to be used in the life table analyses described below. Each treatment consisted of ⬎24 individuals. Aphids that died within the Þrst 24 h after removal from the ßight mill apparatus were not included in data analysis as this mortality may have been related to the apparatus. Flight Mill Experiment. We developed a computermonitored ßight mill for the purposes of this study. Details of the ßight mill are described in Zhang et al. (2008), but brießy, the ßight mill was composed of a 10-cm copper thread placed between two miniature magnets (Fig. 1). Individual aphids were glued to the top surface of one edge of the copper thread with a droplet of 502 Glue (Yuyao Kexing Adhesive Co., Zhejiang, China), applied to the ventral side of their abdomen. This design ensured that aphids maintained a horizontal ßight orientation and, as aphids are glued only on their ventral side, the tethering process does not interfere with wings or the dorsal thoracic cavity where the ßight muscles are housed (Feng et al. 2004, Zhang et al. 2008). In total, 32 ßight mills were placed within a climate-controlled chamber at the Institute of Plant Protection (Chinese Academy of Agricultural Sciences, Beijing, China) and individually connected to a single computer. Data recorded included the time of ßight initiation and cessation and the number of mill revolutions that occurred in consecutive 5-s intervals. Flights interrupted by a 1-min or greater interval with zero counts were considered separate ßights. The number of ßight mill revolutions over a given period of time was recorded and ßight distance, speed, and duration for each tested aphid were computed by a custom-made software package (Cheng et al. 1997,

February 2009 Table 1.



Effect of different flight treatments on the subsequent development and reproductive success of winged A. glycines

Flight distance (km)

Fecundity (n)

Longevity (d)

Reproductive period (d)

Postreproductive period (d)

⬍0.5 0.5Ð1.5 1.5Ð2.5 ⬎2.5

31.63 ⫾ 1.86a 25.41 ⫾ 2.19b 21.67 ⫾ 1.52b 16.07 ⫾ 2.24c

15.92 ⫾ 0.49a 13.00 ⫾ 0.70b 11.50 ⫾ 0.54bc 10.00 ⫾ 0.55c

13.71 ⫾ 0.64a 11.74 ⫾ 0.77b 9.88 ⫾ 0.64b 6.74 ⫾ 0.89c

2.00 ⫾ 0.52ab 1.26 ⫾ 0.35b 1.54 ⫾ 0.78b 3.18 ⫾ 0.56a

Data are presented as mean ⫾ SE. Means in the same column followed by different letters are signiÞcantly different (nonparametric KruskalÐWallis method of ANOVA by ranks was used to test differences between means of fecundity, P ⬍0.05. DuncanÕs multiple range test was used to identify differences between means of longevity, reproductive period and postreproductive period, P ⬍0.05).

Zhang et al. 2008). All ßight mill experiments were carried out at 25⬚C and 75% RH. Effects of Flight on A. glycines Offspring. First instar nymphs produced by alate A. glycines from each of the different treatments (⬍0.5, 0.5Ð1.5, 1.5Ð2.5, and ⬎2.5 km) were placed individually within 5-cm-diameter petri dishes with a soybean leaf on 1% agar (see above). Nymphs were maintained at 25⬚C, 75% RH, and a photoperiod of 16:8 (L:D) h and checked daily for development, longevity, reproduction, and mortality. Nymphal development was recorded by checking nymphal instar and eventual evidence of molting (i.e., presence of exuviae). Observations were continued over the entire life span of the aphid. Data were used to calculate the following life table parameters: net reproductive rate (Ro ⫽ 冱mxlx), time interval between subsequent generations (T ⫽ 冱mxlxx/ 冱mxlx), intrinsic rate of population increase (rm ⫽ In Ro/T), and Þnite rate of increase (␭ ⫽ erm), with (x) the age intervals, (mx) the age-speciÞc fecundity, and (lx) the age-speciÞc survivorship. Data Analysis. We used analysis of variance (ANOVA) to test for differences between treatment means. The KolmogorovÐSmirnov test was used to ensure that data satisÞed the assumptions of ANOVA. Where data failed to meet ANOVA assumptions, we used the nonparametric KruskalÐWallis method of ANOVA by ranks (Zar 1999) to test differences between means (SPSS Inc. 1997). The Duncan multiple range test was used to compare speciÞc treatments (SAS Institute 1988).

Results Effect of Flight on Fecundity. Alates that had engaged in longer ßights (⬎0.5 km) had signiÞcantly lower fecundity (KruskalÐWallis statistic ⫽ 14.12, P ⬍ 0.05), lower longevity (F3, 104 ⫽ 26.17; P ⬍ 0.05) and a shorter reproductive period (F3, 104 ⫽ 16.80; P ⬍ 0.05) than those that had ßown for shorter distances (⬍0.5 km) (Table 1; Fig. 2). There were not signiÞcant differences in temporal patterns of nymphal reproduction between alates that had engaged in short ßights and those that had engaged in long-distance ßights (Fig. 3). Effect of Flight on Offspring Fecundity. Nymphs produced by winged A. glycines in the different treatments reached adulthood by the age of 5 d and commenced reproduction at the age of 6 d, reaching an early peak in fecundity (Fig. 4). We observed no differences in longevity (KruskalÐWallis statistic ⫽ 5.79, P ⬎ 0.05), age of Þrst reproduction (KruskalÐ Wallis statistic ⫽ 3.28, P ⬎ 0.05) among treatments. However, signiÞcant differences were found among treatments in fecundity (KruskalÐWallis statistic ⫽ 8.25, P ⬍ 0.05), with fecundity of the offspring of alates that had engaged in long-distance ßights lower than that of individuals that only undertook short ßights. Aphids produced by alates that had undertaken ßights ⬍0.5 km had higher net reproductive rate (R0) (F3, 12 ⫽ 6.83; P ⬍ 0.05) than those produced by individuals that ßew for ⬎1.5 km (Table 2). The reproductive capacity of aphids that were the offspring of females ßown for

Fig. 2. Survivorship curves for winged A. glycines adults with different ßight treatments. Treatments included ßights of differing distance (⬍0.5, 0.5Ð1.5, 1.5Ð2.5, and ⬎2.5 km). The day of adult molt was considered as day 0 for the purposes of the experiment, and the number of days past this day was used to indicate alate age.



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Fig. 3. Fertility schedule for winged A. glycines with different ßight treatments. Treatments included ßights of differing distances (⬍0.5, 0.5Ð1.5, 1.5Ð2.5, and ⬎2.5 km). The day of adult molt was considered as day 0 for the purposes of the experiment, and the number of days past this day was used to indicate alate age. Number of alatoid nymphs was recorded on a daily basis.

short distances was similar to other studies of A. glycines reproduction under optimal conditions, including Þeld studies (McCornack et al. 2004, Rutledge and OÕNeil 2006). Discussion We have uncovered trade-offs between ßight and fecundity in the soybean aphid, A. glycines. Our work shows that long-distance ßight leads to decreased lifetime fecundity and longevity of A. glycines alates and also results in lowered fecundity of alate offspring. Various insect species undertake long-distance migratory ßights while reproductively immature and only engage in active reproductive behavior upon termination of ßight (Rankin et al. 1986, Wheeler 1996). This phenomenon reßects a trade-off between ßight and fecundity, and is termed the “oogenesisßight syndrome” This term seems to be applicable to A. glycines because 1) ßight tends to precede reproduction and 2) alates increased their reproductive rate immediately after ßights. After this initial burst of postßight fecundity, however, fecundity dropped and total reproductive output was greatly diminished by long-distance ßight. For example, A. glycines alates

that had engaged in ⬎2.5 km ßight lived almost 6 d fewer and produced ⬇15 fewer nymphs than did alates that had engaged in short (⬍0.5-km) ßights. The pattern of reproduction postßight, with the bulk of reproduction occurring immediately after ßight, would be expected to attenuate the magnitude of the tradeoff between ßight and reproduction, in particular because of the value of early over late reproduction in growing populations (Cole 1954). We had shown previously that 12-h-old A. glycines ßy at a rate of ⬇1.5 km/h (Zhang et al. 2008). In a study by Cockbain (1961a), A. fabae used up most of their glycogen reserves during the Þrst 1Ð2 h of tethered ßight and began using lipid reserves during the second hour of ßight. To the extent that the use of ßight fuel in A. glycines resembles that of A. fabae, this would suggest that physiological trade-offs between long-distance ßight and fecundity are mediated by lipid reserves because the strongest effects on fecundity were seen in the group of alates that had been ßown for ⬎2.5 km. Trade-offs between dispersal and fecundity are mediated by lipid reserves in the wing-polymorphic cricket Gryllus firmus (Scudder) as well (Zera and Zhao 2006).

Fig. 4. Fertility schedule for offspring produced by winged A. glycines adults with different ßight treatments. Treatments included ßights of differing distances (⬍0.5, 0.5Ð1.5, 1.5Ð2.5, and ⬎2.5 km). Number of nymphs produced was recorded on a daily basis.


February 2009

Table 2. Life table parameters for offspring produced by winged A. glycines adults with different flight treatments Flight distance (km)




⬍0.5 0.5Ð1.5 1.5Ð2.5 ⬎2.5

34.931a 30.968a 21.130b 17.736b

13.087a 11.817a 12.780a 12.132a

0.272a 0.291a 0.239a 0.237a

␭ 1.312a 1.337a 1.270a 1.267a

Means in the same column followed by different letters are significantly different (P ⬍0.05; DuncanÕs multiple range test).

Flight experience of winged A. glycines adults also affected fecundity and development of subsequent aphid offspring, suggesting the presence of a maternal effect. Nymphs produced by alates that had engaged in long-distance ßight had lower fecundity than those produced by alates that only undertook short-distance ßights. Given our experimental design, such an affect cannot be explained by genetic differences or by differences in the environment of the nymphs and so must be due to the behavior of the mothers, i.e., a maternal effect (Mousseau and Fox 1998). Zehnder and Hunter (2007) have recently echoed Dixon (1998) in arguing that maternal effects are particularly likely in aphids because of their telescoping generations, in which nymphs contain embryos (and these embryos themselves contain embryos) at birth. Despite this, Zehnder and Hunter (2007) found only weak maternal effects for development time of apterous aphids associated with crowding in the oleander aphid, Aphis nerii Boyer de Fonscolombe, and no maternal effects at all associated with developing on low-quality host plant species. In our experiment, reduced fecundity was found only in nymphs that had ßown for 1.5 km or more. As noted above, ßights longer than this take more than one hour after which time lipid reserves are expected to decline (Cockbain 1961a). Thus, the depletion of lipid reserves during ßight may have led not only to be reduced provisioning of offspring but also to be reduced provisioning of oocytes or embryos within these offspring. We also may be able to explain why the A. nerii in the study by Zehnder and Hunter (2007) showed no maternal effect for fecundity with respect to host plant used and crowding: if these stressors were not strong enough to deplete lipid reserves, reproductive trade-offs may not be expected. Despite the trade-offs identiÞed in this study however, the distribution of A. glycines has expanded to cover almost the entire North American soybean growing region within a few years of its arrival (Venette and Ragsdale 2004). This is likely explained by passive, wind-aided ßight, which presumably incurs less physiological cost than does active ßight (Isard and Gage 2001, Zhu et al. 2006). An alternative explanation of multiple colonization events by A. glycines in various sites because the initial invasion in 2000 seems unlikely given the initial distributional pattern (Venette and Ragsdale 2004). Because we only studied A. glycines produced on soybean, Glycine max (L.)


Merr., our Þndings exclusively explain the effects of aphid ßight on fecundity during summer conditions (with aphids dispersing between patches of soybean). To capture trade-offs between ßight and fecundity during, e.g., spring migration, A. glycines would have to be reared on its winter hosts, Rhamnus spp., because life-history trade-offs may vary with the host plant (Coll and Yuva 2004). Acknowledgments We thank Dengfa Cheng (Institute of Plant protection, Chinese Academy of Agricultural Sciences, Beijing) for providing the 32-channel, computer-monitored ßight-mill system; Mark Asplen (University of Minnesota) for fruitful discussion; and two anonymous reviewers for helpful comments on the manuscript. This research was supported by Þnancial assistance from National Natural Science Foundation of China (30625028), Chinese Ministry of Science and Technology (2006 CB102007), and NCSRPC and USDA RAMP funding.

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