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The Cost of Mating: Influences of Life History Traits and Mating Strategies on Lifespan in Two Closely Related Yponomeuta Species

The Cost of Mating: Influences of Life History Traits and Mating Strategies on Lifespan in Two... Hindawi Publishing Corporation International Journal of Zoology Volume 2011, Article ID 658908, 8 pages doi:10.1155/2011/658908 Research Article The Cost of Mating: Influences of Life History Traits and Mating Strategies on Lifespan in Two Closely Related Yponomeuta Species A. C. Bakker,J.CamposLouc ¸a, ˜ P. Roessingh, and S. B. J. Menken Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE Amsterdam, The Netherlands Correspondence should be addressed to P. Roessingh, roessingh@uva.nl Received 23 December 2010; Revised 21 February 2011; Accepted 18 May 2011 Academic Editor: Marie Herberstein Copyright © 2011 A. C. Bakker et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Theory predicts that in monandrous butterfly species males should not invest in a long lifespan because receptive females quickly disappear from the mating population. In polyandrous species, however, it pays for males to invest in longevity, which increases the number of mating opportunities and thus reproductive fitness. We tested an extension of this idea and compared male and female lifespan of two closely related Yponomeuta species with different degree of polyandry. Our results confirmed the theoretical prediction that male lifespan is fine-tuned to female receptive lifespan; once-mated males and females of both polyandrous species had an equal lifespan. However, the degree of polyandry was not reflected in male relative to female lifespan. The observed similar female and male lifespan could largely be attributed to a dramatic reduction of female lifespan after mating. 1. Introduction negative effects, it may seem surprising that multiple mating is the rule in insects at rates that are often much higher Multiple mating can have both positive and negative effects than required for fertilizing the total egg content of a female on female fitness [1–5]. Together these benefits and costs [7]. Therefore, there must also be positive effects associated determine the optimal mating rate of a female. Knowledge with polyandry. These positive effects include compensation of the species-specific advantages and disadvantages of for mating with a genetically incompatible, inferior, or monandry (females mate only once) and polyandry (females infertile male and an increase in genetic variability among mate more than once) is important for understanding the the offspring ([16, 17], and references therein). Moreover, substances in the male ejaculate (nuptial gifts) can increase adaptive significance of mating systems. Negative effects of multiple mating include an increase of energy and time spent female lifespan [18, 19], female fecundity (see [20]for an on mating, as well as the concomitant increased vulnerability overview), and offspring fitness [21, 22]. Positive effects of the ejaculate act either directly, by providing extra resources to predation, sexual diseases, parasites, and pathogens [6]. Furthermore, an excess of sperm can have a negative effect for somatic maintenance of females ([18] and references on both egg production rate (and thus female fecundity) therein [19, 23]), or indirectly, by protecting the female and fertility ([7], and references therein). In addition, in against predators (e.g., the pyrrolizidine alkaloids transferred polyandrous species, mating may reduce female lifespan as by male Utetheisa ornatrix [24]). a consequence of male manipulation [6–9]. Manipulation The mating strategy of a species and multiple mating in comprises both the transfer of toxic compounds, such as particular may influence certain life history traits such as those found in Drosophila fruitflies[10], the bruchid Acan- lifespan. Wiklund et al. [25] suggested that in Lepidoptera different mating systems may select for different sex-specific thoscelides obtectus [11], or the nematode Caenorhabditis elegans [12], and physical damage, such as that brought about mortality rates. In species where females mate multiple by bed bugs [13], the bruchid Callosobruchus maculatus times, receptive females are continuously available, and [14], or the dung fly Sepsis cynipsea [15]. Considering these males that allocate resources to increase their lifespan may 2 International Journal of Zoology directly increase their number of opportunities to mate very much alike in many of their life history traits and and consequently their reproductive fitness. Wiklund et al. behaviour. They do however differ in lifespan, and although [25] showed that males of a polyandrous species indeed both are able to mate more than once, they display significant lived as long as their conspecific females while males of differences in female mating frequencies [39]. The average a monandrous species did not. Males of a monandrous mating frequency of Y. cagnagellus females are 3.0 ± 0.3 times species (under the condition of high synchrony in receptivity (mean ± standard error). In the laboratory, they can mate patterns among individual females) are expected to allocate up to 9 times. The average mating frequency of Y. padellus resources to other traits that improve reproductive success, females is 2.0 ± 0.2, and a majority of females is mating such as development rate, pheromone production, and only once [39]. We can therefore conclude that Y. cagnagellus flight muscles. Fast development leading to males emerging females are highly polyandrous and Y. padellus females have before females (protandry) is advantageous in precopulatory a low degree of polyandry. male competition, whereas male sex pheromones facilitate We ask four questions in this paper: (1) are male and efficient signalling of partners (e.g., in species that form female lifespans equal in polyandrous species as Wiklund male leks [26]) flight muscles improve flight ability and et al. [25] predicts? (2) Can Wiklund’s hypothesis be thus the capability of pursuing and catching females (e.g., in extended to cover sex-specific adjustment of lifespan related Papilionidae: [27] and in Nymphalidae [28]). to the degree of polyandry of the species? (3) Does mating Here we extend the hypothesis of Wiklund et al. [25]and affect lifespan? (4) Is there a significant effect of pupal weight hypothesize that the overall chances of males of encountering on lifespan? a receptive female should affect to which extent resources would be allocated to prolong male reproductive lifespan. 2. Materials and Methods If in a species many females mate only once and few more than once, it is expected that males invest in traits other than In the summer of 2004, fifth instars of the monophagous lifespan (assuming females are receptive around the same Y. cagnagellus were collected in the Netherlands in Cas- ◦  ◦  ◦  ◦ time). We therefore predict that the degree of polyandry will tricum (52 32 N, 4 38 E), Amsterdam (52 8 N, 4 29 E), be reflected in the lifespan of males relative to females. ◦  ◦ andOverveen(52 23 N, 4 34 E) from Euonymus europaeus When testing this hypothesis, certain other life history (Celastraceae). Fifth instars of the oligophagous Y. padellus traits and effects of mating need to be considered. First, in ◦  ◦ were collectedinLeiden(52 21 N, 4 56 E) from Crataegus Lepidoptera, positive [19, 29–33], negative [9, 34], or no monogyna (Rosaceae). They were reared as described below effects [35, 36] of mating on lifespan have been observed in on leaves of their host plant. After eclosion, adult moths either sex or in both sexes. Therefore, the effect of mating were placed under a net on their host plant and allowed itself needs to be considered when investigating sex-specific to mate and lay eggs. Egg batches with first instars were longevity and relating it to male investment in lifespan. A sec- kept outdoors under natural conditions. In the next spring, ond aspect that needs to be taken into account is the possible egg batches were opened and the first stadium larvae fed effect of body size. In many species, larger individuals tend in Petri dishes (10 cm ∅) with a maximum of 15 L5 to live longer than smaller ones, and females tend to be larger larvae per dish on freshly picked leaves of Prunus spinosa than males ([37] and references therein). Therefore, it may be (Rosaceae) for Y. padellus and E. europaeus for Y. cagnagellus, expected that individuals that have developed from heavier at 22 C, 60% R.H., and L17:D7 photoperiod until pupation. pupae live longer, as they may allocate more resources to the Pupae were weighed individually on an OHAUS Analytical prolongation of adult life. If indeed females are larger than Standard Scale (d = 0.0001 g) microbalance (OHAUS, males, this might cause (all else being equal) lifespan to be Viroflay, France) after their pupal skin had hardened. They sex specific. The influence of mating itself and possible effects were subsequently placed in individual glass vials (8 cm high of body size on sex-specific lifespan were unfortunately not and 2 cm ∅) that were closed with a cotton wool plug and investigated by Wiklund et al. [25]. stored in climate boxes at 20 C during the photophase and In this study we reevaluate the hypothesis proposed by 18 C during the scothophase, 70–80% R.H, and L17:D7 Wiklund et al. [25] and specifically investigate if it holds photoperiod. for species with different degrees of polyandry. We used two closely related species from the genus Yponomeuta We used pupal weight as a proxy for body size to test for (Lepidoptera: Yponomeutidae). Yponomeuta cagnagellus a correlation with longevity. For all individuals the number (Hubner) ¨ and Y. padellus (L.) have synchronized female of days between weighing and eclosion was recorded. Pupae eclosion in the field and can remate until the end of their were weighed between 3 and 13 days prior to eclosion, with life (A. C. Bakker, unpublished data). Females of both species an average of 6.8 ± 0.1 days for Y. padellus and 8.0 ± 0.2 days mate maximally once per day. Yponomeuta padellus females for Y. cagnagellus. The weight of pupae diminishes every day show synchronized sexual maturity (as indicated by female until eclosion (weight loss amounts to 1.18 ± 0.07% per day ‘calling’ behaviour) and have similar age at first mating for Y. cagnagellus and 1.15 ± 0.04% per day for Y. padellus). in the laboratory [38, 39]. Yponomeuta cagnagellus females To correct for this confounding factor, we estimated the also show synchronized sexual maturity [38] but the age of rate of weight loss in the controls of the two species using females mating for the first time can vary widely, and this a regression of pupal weight against time to eclosion for may indicate that Y. cagnagellus females are choosy [39]. males and females of both species and used these results to The two species are closely related [40, 41] and therefore predict pupal weight of all insects at the time of eclosion. International Journal of Zoology 3 Table 1: ANOVA table of a GLM model to estimate the effects of sex, species, mating status, and the interaction of sex and species on pupal weight at the time of adult eclosion. Model terms Degree of freedom Deviance Residual degree of freedom Residual deviance FP Null model 502 26345.9 ∗∗∗ Sex 1 6037.5 501 20308.4 207.6 0.0000 ∗∗∗ Species 1 5806.3 500 14502.1 199.7 0.0000 Sex∗species 1 16.5 498 14479.8 0.567 0.4517 Mating status 1 5.8 499 14496.3 0.199 0.6555 ∗∗∗ P< 0.05, P< 0.01, P < 0.001. These estimated weights were subsequently used as a covari- loss since weighing as described above). To test for sex- ate in the GLM analyses to evaluate the effect of pupal specific lifespan, a sex species interaction term was included. weight (as proxy for adult size) on lifespan. To minimize To test the differential effects of mating, a sex mating status uncontrolled differences in weight loss due to variations in and a species∗mating status terms were also included. All humidity, all experiments were conducted in the same room, statistical tests were performed in R (version 2.9.1 [42]). and all treatments were run simultaneously. Throughout the study, average values are presented together After eclosion, moths were sexed and supplied once with their standard errors. a week with a cube of 10% honey-containing 1% agar (w/v; type 1-D LEEO: Sphaero-Q, Leiden, The Netherlands). 3. Results When the moths were sexually mature, that is, at 14–18 days after eclosion for Y. cagnagellus and 8–14 days for Y. 3.1. Pupal Weight. Pupal weights of Y. padellus ranged from padellus, individuals were randomly assigned to either the 17.6 to 48.5 mg for females and from 17.8 to 39.2 mg for mated or the virgin (control) group. One female and one males. In the heavier Y. cagnagellus, pupal weights ranged male were placed together in a Petri dish in the climate room from 28.7 to 57.4 mg for females and for males from 21.1 to at 20-21 C, 60–85% R.H., with a L17 : D7 cycle (of which 46.7 mg. A generalized linear model (Table 1) with estimated the photophase contained 1 h twilight at dawn, provided pupal weight at the day of eclosion as the dependent variable by a 40 W screened lamp). A red darkroom lamp (Philips showed significant main effects of both sex and species, PF712E, 15 W) allowed us to observe the moths during but no interaction effect between them, and no effect of the scothophase without disturbing them. The mated group treatment (mated or control). The correlations showed that was allowed to mate once. The females and males of the Y. cagnagellus is significantly heavier than Y. padellus and that control group were treated similarly, except that they were females of both species are heavier than males. The lack of placed individually in Petri dishes. Data were collected from amaineffect of treatment (mating status) showed that our 43 Y. cagnagellus mating pairs, and 49 unmated males and experimental groups did not systematically differ in weight 51 unmated females served as controls. For Y. padellus, 54 (Figure 1). mating pairs were analysed, and 55 unmated males and 59 unmated females were controls. After mating had ended, 3.2. Lifespan. The individual lifespan of Y. padellus ranged male and female moths were placed individually in glass vials from 15 to 94 days for females (n = 113) and from 19 and were provided with a piece of polystyrene which served to 74 days for males (n = 109). In Y. cagnagellus female as an oviposition substrate. They were kept in a climate lifespan ranged from 17 to 146 days (n = 90) and for males box under the same conditions as when they were maturing from 22 to 115 days (n = 92). We used a generalized linear andwerecontinued to be fedonceaweek.Survivaland model to evaluate the influence of species, sex, mating status, oviposition were checked daily, with the exception of a few and the covariate pupal weight on lifespan (Table 2). The weekends where checks were made only once in 2 days. model showed significant effects for all the factors as well as strong interaction effects (Figure 2, Table 2). Inspection of 2.1. Statistical Analysis. The effects of sex and species on the coefficients for the main effects showed that Y. cagnagellus pupal weight and a possible difference in pupal weight lived significantly longer than Y. padellus, that females lived between treatment groups were investigated using a GLM longer than males, that mating reduced lifespan significantly, model that included these factors and a gausian variance and that a higher pupal weight at eclosion increased lifespan. function. The presence of a significant interaction of sex and mating To investigate the effects of species, sex, and mating status status revealed however that the effects of mating differed on lifespan, we used a GLM model with a quasipoisson strongly between the sexes. Mating reduced lifespan in both variance function (appropriate for lifespan data that showed sexes but significantly more in females than in males. a clear poisson distribution with a tail towards long lifespan). The interaction between sex and species on the other Main effects for species, sex, and mating status were included, hand was not significant. While overall the lifespan of Y. as well as the covariate pupal weight (corrected for weight cagnagellus was longer than that of Y. padellus and females 4 International Journal of Zoology Table 2: ANOVA table of a GLM model to estimate the effects of sex, species, mating status, the covariate pupal weight, and specific planned contrasts. Model term Degree of freedom Deviance Residual degree of freedom Residual deviance FP Null model 502 5055.8 ∗∗∗ Species 1 1381.3 500 3674.5 241.63 0.0000 ∗∗∗ Sex 1 274.0 501 3400.5 47.94 0.0000 ∗∗∗ Mating status 1 273.3 499 3127.2 47.81 0.0000 Pupal weight 1 31.9 498 3095.3 5.58 0.0185 n.s. Sex∗species 1 20.1 497 3075.2 3.52 0.0612 ∗∗∗ Sex∗mating status 1 123.2 496 2952.0 21.55 0.0000 n.s. Species∗mating status 1 6.8 495 2945.2 1.19 0.2765 ∗∗ Sex∗Pupal weight 1 46.7 494 2829.5 8.16 0.0046 ∗ ∗∗ ∗∗∗ P < 0.05, P < 0.01, P < 0.001. 40 80 30 60 20 40 10 20 0 0 Y. cagnagellus Y. padellus Y. cagnagellus Y. padellus Female, control Male, control Female, control Male, control Female, mated Male, mated Female, mated Male, mated Figure 1: Estimated pupal weights (in mg) at the day of eclosion Figure 2: Lifespan (in days) as a function of species (Yponomeuta as a function of species (Yponomeuta padellus or Yponomeuta padellus or Yponomeuta cagnagellus), sex, and mating status (virgin cagnagellus), sex, and mating status (virgin control or once mated). control or once mated). lived longer than males, there was no significant sex-specific 4. Discussion lifespan difference between Y. padellus (the less polyandrous species) and Y. cagnagellus (the longer living and more 4.1. EffectofDegreeofPolyandry on Male Investment polyandrous species). in Lifespan. We investigated sex-specific lifespan of two Apositivemaineffect of pupal weight on lifespan was Yponomeuta species that differ in some life history traits found, but this correlation was also dependent on sex, and and in degree of polyandry. We tested the hypothesis of close examination of the coefficients showed that lifespan was Wiklund et al. [25] that males of polyandrous species invest significantly more positively influenced by pupal weight in in lifespan because this will lead to more matings and thus males than in females. more offspring and higher fitness. We chose species with All the interaction effects described above are also evident adifferent level of polyandry to test if Wiklund’s original in the survival curves presented in Figure 3. The significant suggestion would hold even when the degree of polyandry is negative effect of mating on lifespan in the two species considered. Our results confirmed the theoretical prediction is clearly visible, resulting in equal lifespan for males and of polyandrous species having male lifespan close to female females. The interaction effect of mating status with species lifespan: once-mated males and once-mated females had is represented by the relative large reduction of lifespan in an equal lifespan. The hypothesis of Wiklund et al. [25] Y. cagnagellus females after mating. implies that males of polyandrous species continue to live Estimated pupal weight at data of eclosion (mg) Lifespan (days) International Journal of Zoology 5 0.8 0.8 0.6 0.6 0.4 0.4 0.2 0.2 0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 140 Time (days) Time (days) Y. padellus females Y. padellus females Y. cagnagellus females Y. cagnagellus females Y. padellus males Y. padellus males Y. cagnagellus males Y. cagnagellus males (a) (b) Figure 3: (a) Survival curves of virgin adult Yponomeuta padellus and Yponomeuta cagnagellus males and females. Day 0 is the day of eclosion. (b) Survival curves of mated adult Yponomeuta padellus and Yponomeuta cagnagellus males and females. Day 0 is the day of eclosion. after the peak of female receptivity (at least under the higher oviposition rate or to prevent females from remating condition that females receptivity is synchronous, as is the (as is formulated in the adaptive harm hypothesis: [6, 44]). case in Yponomeuta) and thus live past the moment that There are few studies on Lepidoptera in which lifespan of most females have mated once. Indeed, our results showed mated females is compared with virgin female lifespan; in that in both species males live long after the peak of female many studies only lifespan of single-mated females has been receptivity: males of both species live on average more than compared with that of multiple-mated ones. A comparable 45 days after eclosion, but Y. cagnagellus females are receptive negative effect of mating on lifespan was found in Ostrinia at 14.6 ± 1.2 (mean ± SE) days and Y. padellus females at 4.9 nubilalis (Crambidae) [34] and in Colias eurytheme (Pieri- ± 0.6 days after eclosion [39]. dae) [9]. We extended Wiklund’s hypothesis to sex-specific lifes- While the above explanations picture the reduction in pan differences between high and low polyandrous species lifespan after mating as a cost of mating, other explanations and expected a larger investment in lifespan in Y. cagnagellus cannot be excluded. The reduction in lifespan could in prin- males; that is, we predicted a significant sex by species ciple also be caused by a higher activity of females that were interaction on lifespan. This effect was not found (Table 2) paired up (i.e., activity of females before mating, extensive and while both sex and species influence lifespan, the effects walking or flying behaviour in search of a suitable oviposition are similar in both species, and we were unable to find site after mating). However, in our experimental setup, the evidence for an increase in male investment in lifespan in the moths are placed in Petri dishes and glass vials where they more polyandrous species. cannot easily spend resources on locomotion behaviour. Although we have not formally recorded behaviour, our daily 4.2. Effects of Mating on Lifespan. In Lepidoptera mating can observations showed that moths in all treatments stayed have both positive and negative effects on male and female largely in one place (females call while being motionless and lifespan (e.g., [9, 19, 29–34, 43]). One of our objectives only move around if they do not want to mate), and we have was therefore to investigate if, and how, mating influenced no reason to believe that paired females were more active lifespan in Y. padellus and Y. cagnagellus.Inour experiment, thanvirginfemales. a single mating event reduced lifespan of both species, but Another explanation for the reduction of lifespan after in particular that of females. Apparently, any advantageous mating could be a change in physiology (i.e., allocation of energy to eggs after fertilisation). Although this would still effects of mating on female lifespan were outweighed by disadvantageous ones. This net negative effect on female represent a cost of reproduction,itwould notbeatrue lifespan might be a side effect (i.e., pleiotropic) of male cost of mating. The design of our experiment is however not suitable to address the difference between reproduction traits that are beneficial in sperm competition; alternatively, males might deliberately harm females in order to stimulate a and mating. We used an artificial oviposition substrate, Proportion alive Proportion alive 6 International Journal of Zoology on which only 13 out of 90 Y. cagnagellus and 15 out of 113 in this study, are also expected to influence sex-specific Y. padellus females laid eggs (several unmated females also lifespan. Adult feeding can have important effects on sex- oviposited). But even in experiments in which oviposition is specific mortality rates and sexual behaviour (see also [55]). better facilitated and monitored, it is not easy to discriminate For example, Pararge aegeria (Satyridae) adults lived longer between hypotheses based on physiological changes and when fed [56] and in Pseudoplusia includens (Noctuidae), hypotheses based on harm or male manipulation. Regardless a shortage of food and water led to sex-specific lifespan of the underlying cause for the effect of mating, we found a in a population in which males normally live as long as significant sex∗mating status interaction. A single mating in females [57]. Furthermore, Gotthard et al. [56] found in Yponomeuta did reduce male lifespan significantly less than the monandrous P. aegeria adifference in lifespan between female lifespan even though males of both species transferred males and females when females eclosed synchronously, an ejaculate comprising some 15% of their body weight but no difference when eclosion of females was continuous during a single mating [45]. Mating also had no effect on throughout the year (causing virgin females to be available male lifespan in Danaus plexippus (Nymphalidae), which over a longer period of time). Sex ratios in the field also play transfers an ejaculate that amounts up to 10% of its body an important role because in a population of a monandrous mass [46, 47], nor in Callophrys xami (Lycaenidae), with species with more females than males, it is advantageous for an ejaculate of some 3% of its body mass [48]. However, a male to invest in lifespan as some virgin females will still under resource limitation (achieved by starving the larvae), be available after males have mated once. In monogamous multiple-mated males of C. xami lived shorter than virgin species (in which male lifespan is expected to be shorter than males [48]. We did not test whether resource limitation female lifespan) with protandry (i.e., males eclose or become influences the effect of mating on lifespan. In our study, as sexually active before females [58]), the earlier eclosion of in that of Oberhauser [47], and in the non-resource limiting males can reduce the difference in sex-specific lifespan. This experiment of Cordero [48], adult males were provided with is because male lifespan will tend to be increased to bridge a sugar or honey solution, and this may have enabled them the period between male and female eclosion. To test for to replenish some of their resources. On the other hand, as male investment in lifespan in species with protandry, it is species differ in the allocation of larval and adult resources therefore better to determine if males continue to live after to reproduction and lifespan [49], it is conceivable that in the peak of female receptivity, as we did in this study. Yponomeuta, resources for male lifespan cannot be allocated Our results supported the hypothesis of Wiklund et to reproduction. Another important difference with the al. [25] that polyandrous males should invest in lifespan studies of Oberhauser [47]and Cordero[48] is that males and therefore live about as long as females. The differ- were mated multiple times, while in this study males were ence in polyandry between the species was however not mated just once. This difference is important because the reflected in male investment in lifespan. The data instead relationship between lifespan and number of matings could strongly suggest a large reduction of female lifespan by be nonlinear. (as yet unknown) negative effects of mating. It would be interesting to elucidate the actual causes, that is, investigate 4.3. Influence of Pupal Weight on Lifespan. Most Lepidoptera the effects of multiple mating on male and female lifespan acquire most, if not all, of their resources during larval and discriminate between true costs of mating due to male life (so-called capital breeders [50]). These resources can manipulation and male-inflicted damage, and changes due in principle be allocated to prolong lifespan, enhance mate to altered resource allocation after mating. finding, or increase the number and quality of eggs or ejaculate, all of which might increase reproductive output. Acknowledgments By measuring pupal weight, we have indirectly investigated the correlation between resources acquired during the larval The authors thank Louis Lie and Wil van Ginkel for their help stage and adult lifespan, and we expected to find a positive with rearing of the Yponomeuta moths and collecting data, correlation between pupal weight and adult lifespan, a and Emiel van Loon for statistical advice. They are grateful to mechanism found across many species ([37] and references Christer Wiklund and two anonymous reviewers for highly therein). 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The Cost of Mating: Influences of Life History Traits and Mating Strategies on Lifespan in Two Closely Related Yponomeuta Species

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Hindawi Publishing Corporation International Journal of Zoology Volume 2011, Article ID 658908, 8 pages doi:10.1155/2011/658908 Research Article The Cost of Mating: Influences of Life History Traits and Mating Strategies on Lifespan in Two Closely Related Yponomeuta Species A. C. Bakker,J.CamposLouc ¸a, ˜ P. Roessingh, and S. B. J. Menken Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE Amsterdam, The Netherlands Correspondence should be addressed to P. Roessingh, roessingh@uva.nl Received 23 December 2010; Revised 21 February 2011; Accepted 18 May 2011 Academic Editor: Marie Herberstein Copyright © 2011 A. C. Bakker et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Theory predicts that in monandrous butterfly species males should not invest in a long lifespan because receptive females quickly disappear from the mating population. In polyandrous species, however, it pays for males to invest in longevity, which increases the number of mating opportunities and thus reproductive fitness. We tested an extension of this idea and compared male and female lifespan of two closely related Yponomeuta species with different degree of polyandry. Our results confirmed the theoretical prediction that male lifespan is fine-tuned to female receptive lifespan; once-mated males and females of both polyandrous species had an equal lifespan. However, the degree of polyandry was not reflected in male relative to female lifespan. The observed similar female and male lifespan could largely be attributed to a dramatic reduction of female lifespan after mating. 1. Introduction negative effects, it may seem surprising that multiple mating is the rule in insects at rates that are often much higher Multiple mating can have both positive and negative effects than required for fertilizing the total egg content of a female on female fitness [1–5]. Together these benefits and costs [7]. Therefore, there must also be positive effects associated determine the optimal mating rate of a female. Knowledge with polyandry. These positive effects include compensation of the species-specific advantages and disadvantages of for mating with a genetically incompatible, inferior, or monandry (females mate only once) and polyandry (females infertile male and an increase in genetic variability among mate more than once) is important for understanding the the offspring ([16, 17], and references therein). Moreover, substances in the male ejaculate (nuptial gifts) can increase adaptive significance of mating systems. Negative effects of multiple mating include an increase of energy and time spent female lifespan [18, 19], female fecundity (see [20]for an on mating, as well as the concomitant increased vulnerability overview), and offspring fitness [21, 22]. Positive effects of the ejaculate act either directly, by providing extra resources to predation, sexual diseases, parasites, and pathogens [6]. Furthermore, an excess of sperm can have a negative effect for somatic maintenance of females ([18] and references on both egg production rate (and thus female fecundity) therein [19, 23]), or indirectly, by protecting the female and fertility ([7], and references therein). In addition, in against predators (e.g., the pyrrolizidine alkaloids transferred polyandrous species, mating may reduce female lifespan as by male Utetheisa ornatrix [24]). a consequence of male manipulation [6–9]. Manipulation The mating strategy of a species and multiple mating in comprises both the transfer of toxic compounds, such as particular may influence certain life history traits such as those found in Drosophila fruitflies[10], the bruchid Acan- lifespan. Wiklund et al. [25] suggested that in Lepidoptera different mating systems may select for different sex-specific thoscelides obtectus [11], or the nematode Caenorhabditis elegans [12], and physical damage, such as that brought about mortality rates. In species where females mate multiple by bed bugs [13], the bruchid Callosobruchus maculatus times, receptive females are continuously available, and [14], or the dung fly Sepsis cynipsea [15]. Considering these males that allocate resources to increase their lifespan may 2 International Journal of Zoology directly increase their number of opportunities to mate very much alike in many of their life history traits and and consequently their reproductive fitness. Wiklund et al. behaviour. They do however differ in lifespan, and although [25] showed that males of a polyandrous species indeed both are able to mate more than once, they display significant lived as long as their conspecific females while males of differences in female mating frequencies [39]. The average a monandrous species did not. Males of a monandrous mating frequency of Y. cagnagellus females are 3.0 ± 0.3 times species (under the condition of high synchrony in receptivity (mean ± standard error). In the laboratory, they can mate patterns among individual females) are expected to allocate up to 9 times. The average mating frequency of Y. padellus resources to other traits that improve reproductive success, females is 2.0 ± 0.2, and a majority of females is mating such as development rate, pheromone production, and only once [39]. We can therefore conclude that Y. cagnagellus flight muscles. Fast development leading to males emerging females are highly polyandrous and Y. padellus females have before females (protandry) is advantageous in precopulatory a low degree of polyandry. male competition, whereas male sex pheromones facilitate We ask four questions in this paper: (1) are male and efficient signalling of partners (e.g., in species that form female lifespans equal in polyandrous species as Wiklund male leks [26]) flight muscles improve flight ability and et al. [25] predicts? (2) Can Wiklund’s hypothesis be thus the capability of pursuing and catching females (e.g., in extended to cover sex-specific adjustment of lifespan related Papilionidae: [27] and in Nymphalidae [28]). to the degree of polyandry of the species? (3) Does mating Here we extend the hypothesis of Wiklund et al. [25]and affect lifespan? (4) Is there a significant effect of pupal weight hypothesize that the overall chances of males of encountering on lifespan? a receptive female should affect to which extent resources would be allocated to prolong male reproductive lifespan. 2. Materials and Methods If in a species many females mate only once and few more than once, it is expected that males invest in traits other than In the summer of 2004, fifth instars of the monophagous lifespan (assuming females are receptive around the same Y. cagnagellus were collected in the Netherlands in Cas- ◦  ◦  ◦  ◦ time). We therefore predict that the degree of polyandry will tricum (52 32 N, 4 38 E), Amsterdam (52 8 N, 4 29 E), be reflected in the lifespan of males relative to females. ◦  ◦ andOverveen(52 23 N, 4 34 E) from Euonymus europaeus When testing this hypothesis, certain other life history (Celastraceae). Fifth instars of the oligophagous Y. padellus traits and effects of mating need to be considered. First, in ◦  ◦ were collectedinLeiden(52 21 N, 4 56 E) from Crataegus Lepidoptera, positive [19, 29–33], negative [9, 34], or no monogyna (Rosaceae). They were reared as described below effects [35, 36] of mating on lifespan have been observed in on leaves of their host plant. After eclosion, adult moths either sex or in both sexes. Therefore, the effect of mating were placed under a net on their host plant and allowed itself needs to be considered when investigating sex-specific to mate and lay eggs. Egg batches with first instars were longevity and relating it to male investment in lifespan. A sec- kept outdoors under natural conditions. In the next spring, ond aspect that needs to be taken into account is the possible egg batches were opened and the first stadium larvae fed effect of body size. In many species, larger individuals tend in Petri dishes (10 cm ∅) with a maximum of 15 L5 to live longer than smaller ones, and females tend to be larger larvae per dish on freshly picked leaves of Prunus spinosa than males ([37] and references therein). Therefore, it may be (Rosaceae) for Y. padellus and E. europaeus for Y. cagnagellus, expected that individuals that have developed from heavier at 22 C, 60% R.H., and L17:D7 photoperiod until pupation. pupae live longer, as they may allocate more resources to the Pupae were weighed individually on an OHAUS Analytical prolongation of adult life. If indeed females are larger than Standard Scale (d = 0.0001 g) microbalance (OHAUS, males, this might cause (all else being equal) lifespan to be Viroflay, France) after their pupal skin had hardened. They sex specific. The influence of mating itself and possible effects were subsequently placed in individual glass vials (8 cm high of body size on sex-specific lifespan were unfortunately not and 2 cm ∅) that were closed with a cotton wool plug and investigated by Wiklund et al. [25]. stored in climate boxes at 20 C during the photophase and In this study we reevaluate the hypothesis proposed by 18 C during the scothophase, 70–80% R.H, and L17:D7 Wiklund et al. [25] and specifically investigate if it holds photoperiod. for species with different degrees of polyandry. We used two closely related species from the genus Yponomeuta We used pupal weight as a proxy for body size to test for (Lepidoptera: Yponomeutidae). Yponomeuta cagnagellus a correlation with longevity. For all individuals the number (Hubner) ¨ and Y. padellus (L.) have synchronized female of days between weighing and eclosion was recorded. Pupae eclosion in the field and can remate until the end of their were weighed between 3 and 13 days prior to eclosion, with life (A. C. Bakker, unpublished data). Females of both species an average of 6.8 ± 0.1 days for Y. padellus and 8.0 ± 0.2 days mate maximally once per day. Yponomeuta padellus females for Y. cagnagellus. The weight of pupae diminishes every day show synchronized sexual maturity (as indicated by female until eclosion (weight loss amounts to 1.18 ± 0.07% per day ‘calling’ behaviour) and have similar age at first mating for Y. cagnagellus and 1.15 ± 0.04% per day for Y. padellus). in the laboratory [38, 39]. Yponomeuta cagnagellus females To correct for this confounding factor, we estimated the also show synchronized sexual maturity [38] but the age of rate of weight loss in the controls of the two species using females mating for the first time can vary widely, and this a regression of pupal weight against time to eclosion for may indicate that Y. cagnagellus females are choosy [39]. males and females of both species and used these results to The two species are closely related [40, 41] and therefore predict pupal weight of all insects at the time of eclosion. International Journal of Zoology 3 Table 1: ANOVA table of a GLM model to estimate the effects of sex, species, mating status, and the interaction of sex and species on pupal weight at the time of adult eclosion. Model terms Degree of freedom Deviance Residual degree of freedom Residual deviance FP Null model 502 26345.9 ∗∗∗ Sex 1 6037.5 501 20308.4 207.6 0.0000 ∗∗∗ Species 1 5806.3 500 14502.1 199.7 0.0000 Sex∗species 1 16.5 498 14479.8 0.567 0.4517 Mating status 1 5.8 499 14496.3 0.199 0.6555 ∗∗∗ P< 0.05, P< 0.01, P < 0.001. These estimated weights were subsequently used as a covari- loss since weighing as described above). To test for sex- ate in the GLM analyses to evaluate the effect of pupal specific lifespan, a sex species interaction term was included. weight (as proxy for adult size) on lifespan. To minimize To test the differential effects of mating, a sex mating status uncontrolled differences in weight loss due to variations in and a species∗mating status terms were also included. All humidity, all experiments were conducted in the same room, statistical tests were performed in R (version 2.9.1 [42]). and all treatments were run simultaneously. Throughout the study, average values are presented together After eclosion, moths were sexed and supplied once with their standard errors. a week with a cube of 10% honey-containing 1% agar (w/v; type 1-D LEEO: Sphaero-Q, Leiden, The Netherlands). 3. Results When the moths were sexually mature, that is, at 14–18 days after eclosion for Y. cagnagellus and 8–14 days for Y. 3.1. Pupal Weight. Pupal weights of Y. padellus ranged from padellus, individuals were randomly assigned to either the 17.6 to 48.5 mg for females and from 17.8 to 39.2 mg for mated or the virgin (control) group. One female and one males. In the heavier Y. cagnagellus, pupal weights ranged male were placed together in a Petri dish in the climate room from 28.7 to 57.4 mg for females and for males from 21.1 to at 20-21 C, 60–85% R.H., with a L17 : D7 cycle (of which 46.7 mg. A generalized linear model (Table 1) with estimated the photophase contained 1 h twilight at dawn, provided pupal weight at the day of eclosion as the dependent variable by a 40 W screened lamp). A red darkroom lamp (Philips showed significant main effects of both sex and species, PF712E, 15 W) allowed us to observe the moths during but no interaction effect between them, and no effect of the scothophase without disturbing them. The mated group treatment (mated or control). The correlations showed that was allowed to mate once. The females and males of the Y. cagnagellus is significantly heavier than Y. padellus and that control group were treated similarly, except that they were females of both species are heavier than males. The lack of placed individually in Petri dishes. Data were collected from amaineffect of treatment (mating status) showed that our 43 Y. cagnagellus mating pairs, and 49 unmated males and experimental groups did not systematically differ in weight 51 unmated females served as controls. For Y. padellus, 54 (Figure 1). mating pairs were analysed, and 55 unmated males and 59 unmated females were controls. After mating had ended, 3.2. Lifespan. The individual lifespan of Y. padellus ranged male and female moths were placed individually in glass vials from 15 to 94 days for females (n = 113) and from 19 and were provided with a piece of polystyrene which served to 74 days for males (n = 109). In Y. cagnagellus female as an oviposition substrate. They were kept in a climate lifespan ranged from 17 to 146 days (n = 90) and for males box under the same conditions as when they were maturing from 22 to 115 days (n = 92). We used a generalized linear andwerecontinued to be fedonceaweek.Survivaland model to evaluate the influence of species, sex, mating status, oviposition were checked daily, with the exception of a few and the covariate pupal weight on lifespan (Table 2). The weekends where checks were made only once in 2 days. model showed significant effects for all the factors as well as strong interaction effects (Figure 2, Table 2). Inspection of 2.1. Statistical Analysis. The effects of sex and species on the coefficients for the main effects showed that Y. cagnagellus pupal weight and a possible difference in pupal weight lived significantly longer than Y. padellus, that females lived between treatment groups were investigated using a GLM longer than males, that mating reduced lifespan significantly, model that included these factors and a gausian variance and that a higher pupal weight at eclosion increased lifespan. function. The presence of a significant interaction of sex and mating To investigate the effects of species, sex, and mating status status revealed however that the effects of mating differed on lifespan, we used a GLM model with a quasipoisson strongly between the sexes. Mating reduced lifespan in both variance function (appropriate for lifespan data that showed sexes but significantly more in females than in males. a clear poisson distribution with a tail towards long lifespan). The interaction between sex and species on the other Main effects for species, sex, and mating status were included, hand was not significant. While overall the lifespan of Y. as well as the covariate pupal weight (corrected for weight cagnagellus was longer than that of Y. padellus and females 4 International Journal of Zoology Table 2: ANOVA table of a GLM model to estimate the effects of sex, species, mating status, the covariate pupal weight, and specific planned contrasts. Model term Degree of freedom Deviance Residual degree of freedom Residual deviance FP Null model 502 5055.8 ∗∗∗ Species 1 1381.3 500 3674.5 241.63 0.0000 ∗∗∗ Sex 1 274.0 501 3400.5 47.94 0.0000 ∗∗∗ Mating status 1 273.3 499 3127.2 47.81 0.0000 Pupal weight 1 31.9 498 3095.3 5.58 0.0185 n.s. Sex∗species 1 20.1 497 3075.2 3.52 0.0612 ∗∗∗ Sex∗mating status 1 123.2 496 2952.0 21.55 0.0000 n.s. Species∗mating status 1 6.8 495 2945.2 1.19 0.2765 ∗∗ Sex∗Pupal weight 1 46.7 494 2829.5 8.16 0.0046 ∗ ∗∗ ∗∗∗ P < 0.05, P < 0.01, P < 0.001. 40 80 30 60 20 40 10 20 0 0 Y. cagnagellus Y. padellus Y. cagnagellus Y. padellus Female, control Male, control Female, control Male, control Female, mated Male, mated Female, mated Male, mated Figure 1: Estimated pupal weights (in mg) at the day of eclosion Figure 2: Lifespan (in days) as a function of species (Yponomeuta as a function of species (Yponomeuta padellus or Yponomeuta padellus or Yponomeuta cagnagellus), sex, and mating status (virgin cagnagellus), sex, and mating status (virgin control or once mated). control or once mated). lived longer than males, there was no significant sex-specific 4. Discussion lifespan difference between Y. padellus (the less polyandrous species) and Y. cagnagellus (the longer living and more 4.1. EffectofDegreeofPolyandry on Male Investment polyandrous species). in Lifespan. We investigated sex-specific lifespan of two Apositivemaineffect of pupal weight on lifespan was Yponomeuta species that differ in some life history traits found, but this correlation was also dependent on sex, and and in degree of polyandry. We tested the hypothesis of close examination of the coefficients showed that lifespan was Wiklund et al. [25] that males of polyandrous species invest significantly more positively influenced by pupal weight in in lifespan because this will lead to more matings and thus males than in females. more offspring and higher fitness. We chose species with All the interaction effects described above are also evident adifferent level of polyandry to test if Wiklund’s original in the survival curves presented in Figure 3. The significant suggestion would hold even when the degree of polyandry is negative effect of mating on lifespan in the two species considered. Our results confirmed the theoretical prediction is clearly visible, resulting in equal lifespan for males and of polyandrous species having male lifespan close to female females. The interaction effect of mating status with species lifespan: once-mated males and once-mated females had is represented by the relative large reduction of lifespan in an equal lifespan. The hypothesis of Wiklund et al. [25] Y. cagnagellus females after mating. implies that males of polyandrous species continue to live Estimated pupal weight at data of eclosion (mg) Lifespan (days) International Journal of Zoology 5 0.8 0.8 0.6 0.6 0.4 0.4 0.2 0.2 0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 140 Time (days) Time (days) Y. padellus females Y. padellus females Y. cagnagellus females Y. cagnagellus females Y. padellus males Y. padellus males Y. cagnagellus males Y. cagnagellus males (a) (b) Figure 3: (a) Survival curves of virgin adult Yponomeuta padellus and Yponomeuta cagnagellus males and females. Day 0 is the day of eclosion. (b) Survival curves of mated adult Yponomeuta padellus and Yponomeuta cagnagellus males and females. Day 0 is the day of eclosion. after the peak of female receptivity (at least under the higher oviposition rate or to prevent females from remating condition that females receptivity is synchronous, as is the (as is formulated in the adaptive harm hypothesis: [6, 44]). case in Yponomeuta) and thus live past the moment that There are few studies on Lepidoptera in which lifespan of most females have mated once. Indeed, our results showed mated females is compared with virgin female lifespan; in that in both species males live long after the peak of female many studies only lifespan of single-mated females has been receptivity: males of both species live on average more than compared with that of multiple-mated ones. A comparable 45 days after eclosion, but Y. cagnagellus females are receptive negative effect of mating on lifespan was found in Ostrinia at 14.6 ± 1.2 (mean ± SE) days and Y. padellus females at 4.9 nubilalis (Crambidae) [34] and in Colias eurytheme (Pieri- ± 0.6 days after eclosion [39]. dae) [9]. We extended Wiklund’s hypothesis to sex-specific lifes- While the above explanations picture the reduction in pan differences between high and low polyandrous species lifespan after mating as a cost of mating, other explanations and expected a larger investment in lifespan in Y. cagnagellus cannot be excluded. The reduction in lifespan could in prin- males; that is, we predicted a significant sex by species ciple also be caused by a higher activity of females that were interaction on lifespan. This effect was not found (Table 2) paired up (i.e., activity of females before mating, extensive and while both sex and species influence lifespan, the effects walking or flying behaviour in search of a suitable oviposition are similar in both species, and we were unable to find site after mating). However, in our experimental setup, the evidence for an increase in male investment in lifespan in the moths are placed in Petri dishes and glass vials where they more polyandrous species. cannot easily spend resources on locomotion behaviour. Although we have not formally recorded behaviour, our daily 4.2. Effects of Mating on Lifespan. In Lepidoptera mating can observations showed that moths in all treatments stayed have both positive and negative effects on male and female largely in one place (females call while being motionless and lifespan (e.g., [9, 19, 29–34, 43]). One of our objectives only move around if they do not want to mate), and we have was therefore to investigate if, and how, mating influenced no reason to believe that paired females were more active lifespan in Y. padellus and Y. cagnagellus.Inour experiment, thanvirginfemales. a single mating event reduced lifespan of both species, but Another explanation for the reduction of lifespan after in particular that of females. Apparently, any advantageous mating could be a change in physiology (i.e., allocation of energy to eggs after fertilisation). Although this would still effects of mating on female lifespan were outweighed by disadvantageous ones. This net negative effect on female represent a cost of reproduction,itwould notbeatrue lifespan might be a side effect (i.e., pleiotropic) of male cost of mating. The design of our experiment is however not suitable to address the difference between reproduction traits that are beneficial in sperm competition; alternatively, males might deliberately harm females in order to stimulate a and mating. We used an artificial oviposition substrate, Proportion alive Proportion alive 6 International Journal of Zoology on which only 13 out of 90 Y. cagnagellus and 15 out of 113 in this study, are also expected to influence sex-specific Y. padellus females laid eggs (several unmated females also lifespan. Adult feeding can have important effects on sex- oviposited). But even in experiments in which oviposition is specific mortality rates and sexual behaviour (see also [55]). better facilitated and monitored, it is not easy to discriminate For example, Pararge aegeria (Satyridae) adults lived longer between hypotheses based on physiological changes and when fed [56] and in Pseudoplusia includens (Noctuidae), hypotheses based on harm or male manipulation. Regardless a shortage of food and water led to sex-specific lifespan of the underlying cause for the effect of mating, we found a in a population in which males normally live as long as significant sex∗mating status interaction. A single mating in females [57]. Furthermore, Gotthard et al. [56] found in Yponomeuta did reduce male lifespan significantly less than the monandrous P. aegeria adifference in lifespan between female lifespan even though males of both species transferred males and females when females eclosed synchronously, an ejaculate comprising some 15% of their body weight but no difference when eclosion of females was continuous during a single mating [45]. Mating also had no effect on throughout the year (causing virgin females to be available male lifespan in Danaus plexippus (Nymphalidae), which over a longer period of time). Sex ratios in the field also play transfers an ejaculate that amounts up to 10% of its body an important role because in a population of a monandrous mass [46, 47], nor in Callophrys xami (Lycaenidae), with species with more females than males, it is advantageous for an ejaculate of some 3% of its body mass [48]. However, a male to invest in lifespan as some virgin females will still under resource limitation (achieved by starving the larvae), be available after males have mated once. In monogamous multiple-mated males of C. xami lived shorter than virgin species (in which male lifespan is expected to be shorter than males [48]. We did not test whether resource limitation female lifespan) with protandry (i.e., males eclose or become influences the effect of mating on lifespan. In our study, as sexually active before females [58]), the earlier eclosion of in that of Oberhauser [47], and in the non-resource limiting males can reduce the difference in sex-specific lifespan. This experiment of Cordero [48], adult males were provided with is because male lifespan will tend to be increased to bridge a sugar or honey solution, and this may have enabled them the period between male and female eclosion. To test for to replenish some of their resources. On the other hand, as male investment in lifespan in species with protandry, it is species differ in the allocation of larval and adult resources therefore better to determine if males continue to live after to reproduction and lifespan [49], it is conceivable that in the peak of female receptivity, as we did in this study. Yponomeuta, resources for male lifespan cannot be allocated Our results supported the hypothesis of Wiklund et to reproduction. Another important difference with the al. [25] that polyandrous males should invest in lifespan studies of Oberhauser [47]and Cordero[48] is that males and therefore live about as long as females. The differ- were mated multiple times, while in this study males were ence in polyandry between the species was however not mated just once. This difference is important because the reflected in male investment in lifespan. The data instead relationship between lifespan and number of matings could strongly suggest a large reduction of female lifespan by be nonlinear. (as yet unknown) negative effects of mating. It would be interesting to elucidate the actual causes, that is, investigate 4.3. Influence of Pupal Weight on Lifespan. Most Lepidoptera the effects of multiple mating on male and female lifespan acquire most, if not all, of their resources during larval and discriminate between true costs of mating due to male life (so-called capital breeders [50]). These resources can manipulation and male-inflicted damage, and changes due in principle be allocated to prolong lifespan, enhance mate to altered resource allocation after mating. finding, or increase the number and quality of eggs or ejaculate, all of which might increase reproductive output. Acknowledgments By measuring pupal weight, we have indirectly investigated the correlation between resources acquired during the larval The authors thank Louis Lie and Wil van Ginkel for their help stage and adult lifespan, and we expected to find a positive with rearing of the Yponomeuta moths and collecting data, correlation between pupal weight and adult lifespan, a and Emiel van Loon for statistical advice. They are grateful to mechanism found across many species ([37] and references Christer Wiklund and two anonymous reviewers for highly therein). 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