Evolution of sex-biased maternal effects in birds. IV. Intra-ovarian growth dynamics can link sex determination and sex-specific acquisition of resources

The evolutionary importance of maternal effects is determined by the interplay of maternal adaptations and strategies, offspring susceptibility to these strategies, and the similarity of selection pressures between the two generations. Interaction among these components, especially in species where males and females differ in the costs and requirements of growth, limits inference about the evolution of maternal strategies from their expression in the offspring phenotype alone. As an alternative approach, we examine divergence in the proximate mechanisms underlying maternal effects across three house finch populations with contrasting patterns of sex allocation: an ancestral population that shows no sex-biased ovulation, and two recently established populations at the northern and southern boundaries of the species range that have opposite sequences of ovulation of male and female eggs. For each population, we examined how oocyte acquisition of hormones, carotenoids and vitamins was affected by oocyte growth and overlap with the same and opposite sexes. Our results suggest that sex-specific acquisition of maternal resources and sex determination of oocytes are linked in this system. We report that acquisition of testosterone by oocytes that become males was not related to growth duration, but instead covaried with temporal exposure to steroids and overlap with other male oocytes. In female oocytes, testosterone acquisition increased with the duration of growth and overlap with male oocytes, but decreased with overlap with female oocytes. By contrast, acquisition of carotenoids and vitamins was mostly determined by organism-wide partitioning among oocytes and oocyte-specific patterns of testosterone accumulation, and these effects did not differ between the sexes. These results provide important insights into three unresolved phenomena in the evolution of maternal effects - (i) the evolution of sex-specific maternal allocation in species with simultaneously developing neonates of both sexes; (ii) the link between sex determination and sex-specific acquisition of maternal products; and (iii) the evolution of context-dependent modulation of maternal effects.     

Evolution of sex-biased maternal effects in birds: II. Contrasting sex-specific oocyte clustering in native and recently established populations

In species that produce broods of multiple offspring, parents need to partition resources among simultaneously growing neonates that often differ in growth requirements. In birds, multiple ovarian follicles develop inside the female at the same time, resulting in a trade-off of resources among them and potentially limiting maternal ability for sex-specific allocation. We compared resource acquisition among oocytes in relation to their future sex and ovulation order in two populations of house finches with contrasting sex-biased maternal strategies. In a native Arizona population, where mothers do not bias offspring sex in relation to ovulation order, the male and female oocytes did not show sex-specific trade-offs of resources during growth and there was no evidence for spatial or temporal segregation of male and female oocytes in the ovary. In contrast, in a recently established Montana population where mothers strongly bias offspring sex in relation to ovulation order, we found evidence for both intra-sexual trade-offs among male and female oocytes and sex-specific clustering of oocytes in the ovary. We discuss the importance of sex-specific resource competition among offspring for the evolution of sex-ratio adjustment and sex-specific maternal resource allocation.     

Evolution of sex-biased maternal effects in birds: I. Sex-specific resource allocation among simultaneously growing oocytes

Females in species that produce broods of multiple offspring need to partition resources among simultaneously growing ova, embryos or neonates. In birds, the duration of growth of a single egg exceeds the ovulation interval, and when maternal resources are limited, a temporal overlap among several developing follicles in the ovary might result in a trade-off of resources among them. We studied growth of oocytes in relation to their future ovulation order, sex, and overlap with other oocytes in a population of house finches (Carpodacus mexicanus) where strongly sex-biased maternal effects are favoured by natural selection. We found pronounced differences in growth patterns between oocytes that produced males and females. Male oocytes grew up to five times faster and reached their ovulation size earlier than female oocytes. Early onset and early termination of male oocytes' growth in relation to their ovulation resulted in their lesser temporal overlap with other growing ova compared with female oocytes. Consequently, ovulation mass of female but not male oocytes was strongly negatively affected by temporal overlap with other oocytes. In turn, mass of male oocytes was mostly affected by the order of ovulation and by maternal incubation strategy. These results provide a mechanism for sex-biased allocation of maternal resources during egg formation and provide insights into the timing of the sex-determining meiotic division in relation to ovulation in this species.     

Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird

Maternal modification of offspring sex in birds has strong fitness consequences, however the mechanisms by which female birds can bias sex of their progeny in close concordance with the environment of breeding are not known. In recently established populations of house finches (Carpodacus mexicanus), breeding females lay a sex-biased sequence of eggs when ambient temperature causes early onset of incubation. We studied the mechanisms behind close association of incubation and sex-determination strategies in this species and discovered that pre-ovulation oocytes that produce males and females differed strongly in the temporal patterns of proliferation and growth. In turn, sex-specific exposure of oocytes to maternal secretion of prolactin and androgens produced distinct accumulation of maternal steroids in oocyte yolks in relation to oocyte proliferation order. These findings suggest that sex difference in oocyte growth and egg-laying sequence is an adaptive outcome of hormonal constraints imposed by the overlap of early incubation and oogenesis in this population, and that the close integration of maternal incubation, oocytes' sex-determination and growth might be under control of the same hormonal mechanism. We further document that population establishment and the evolution of these maternal strategies is facilitated by their strong effects on female and offspring fitness in a recently established part of the species range.     

Maternal effects mediated by egg quality in the Yellow-legged Gull Larus michahellis in relation to laying order and embryo sex

Background

Maternal effects mediated by egg size and quality may profoundly affect offspring development and performance, and mothers may adjust egg traits according to environmental or social influences. In avian species, context-dependency of maternal effects may result in variation in egg composition, as well as in differential patterns of covariation among selected egg components, according to, for example, position in the laying sequence or offspring sex. We investigated variation in major classes of egg yolk components (carotenoids, vitamins and steroid hormones) in relation to egg size, position in the laying sequence and embryo sex in clutches of the Yellow-legged Gull (Larus michahellis). We also investigated their covariation, to highlight mutual adjustments, maternal constraints or trade-offs in egg allocation.

Results

Laying sequence-specific patterns of allocation emerged: concentration of carotenoids and vitamin E decreased, while concentrations of androgens increased. Vitamin A, estradiol and corticosterone did not show any change. There was no evidence of sex-specific allocation or covariation of yolk components. Concentrations of carotenoids and vitamins were positively correlated. Egg mass decreased along the laying sequence, and this decrease was negatively correlated with the mean concentrations of carotenoids in clutches, suggesting that nutritionally constrained females lay low quality clutches in terms of carotenoid content. Finally, clutches with smaller decline in antioxidants between first- and last-laid eggs had a larger increase in yolk corticosterone, suggesting that a smaller antioxidant depletion along the laying sequence may entail a cost for laying females in terms of increased stress levels.

Conclusions

Since some of the analyzed yolk components (e.g. testosterone and lutein) are known to exert sex-specific phenotypic effects on the progeny in this species, the lack of sex-specific egg allocation by mothers may either result from trade-offs between contrasting effects of different egg components on male and female offspring, or indicate that sex-specific traits are controlled primarily by mechanisms of sexual differentiation, including endogenous hormone production or metabolism of exogenous antioxidants, during embryonic development.     

Maternal allocation strategies and differential effects of yolk carotenoids on the phenotype and viability of yellow-legged gull (Larus michahellis) chicks in relation to sex and laying order

Egg quality may mediate maternal allocation strategies according to progeny sex. In vertebrates, carotenoids have important physiological roles during embryonic and post-natal life, but the consequences of variation in yolk carotenoids for offspring phenotype in oviparous species are largely unknown. In yellow-legged gulls, yolk carotenoids did not vary with embryo sex in combination with egg laying date, order and mass. Yolk lutein supplementation enhanced the growth of sons from first eggs but depressed that of sons from last eggs, enhanced survival of daughters late in the season, and promoted immunity of male chicks and chicks from small eggs. Lack of variation in egg carotenoids in relation to sex and egg features, and the contrasting effects of lutein on sons and daughters, do not support the hypothesis of optimal sex-related egg carotenoid allocation. Carotenoids transferred to the eggs may rather result from a trade-off between opposing effects on sons or daughters.     

Maternal dietary carotenoids mitigate detrimental effects of maternal GnRH on offspring immune function in Japanese quail Coturnix japonica

Maternal resources deposited in eggs can affect the development of several offspring phenotypic traits and result in trade‐offs among them. For example, maternal androgens in eggs may be beneficial to offspring growth and competitive ability, but detrimental to immunocompetence and oxidative stress. In contrast, maternal antioxidants in eggs may be beneficial if they mitigate oxidative stress and immunosuppressive effects of androgens. We investigated possible interactive effects of maternal steroids and carotenoids on aspects of offspring physiology and phenotype, by simultaneously manipulating levels of androgens (via gonadotropin‐releasing hormone, GnRH‐challenges) and carotenoids (via diet supplementation) in captive female Japanese quail Coturnix japonica during egg laying. Carotenoid supplementation of hens, which elevates yolk concentrations of carotenoid and vitamins A and E, enhanced egg hatching success, offspring survival to age 15 d, and size of the bursa of Fabricius in offspring. In contrast, repeated maternal GnRH challenges, which elevated yolk testosterone concentrations, enhanced offspring neonatal size, but negatively affected bursa size. However, interaction among the treatments suggests that the positive effect of maternal carotenoid supplementation on plasma bactericidal capacity was mediated by maternal GnRH challenges. Chicks originating from carotenoid‐supplemented hens were less immunosuppressed than those originating from carotenoid‐supplemented + GnRH‐challenged hens, which were less immunosuppressed than chicks from GnRH‐challenged females not supplemented with carotenoids. Females availability of carotenoid enriched diets allows them to enhance the development of offspring immune system via carotenoids and vitamins deposited in egg yolks and offset detrimental effects of androgens deposited by GnRH‐challenged females.     

The evolution of sexual size dimorphism in the house finch. V. Maternal effects

The phenotype of a mother and the environment that she provides might differentially affect the phenotypes of her sons and daughters, leading to change in sexual size dimorphism. Whereas these maternal effects should evolve to accommodate the adaptations of both the maternal and offspring generations, the mechanisms by which this is accomplished are rarely known. In birds, females adjust the onset of incubation (coincident with the first egg or after all eggs are laid) in response to the environment during breeding, and thus, indirectly, determine the duration of offspring growth. In the two house finch (Carpodacus mexicanus) populations that breed at the extremes of the species' distribution (Montana and Alabama), females experience highly distinct climatic conditions during nesting. We show that in close association with these conditions, females adjusted jointly the onset of incubation and the sequence in which they produced male and female eggs and consequently modified the growth of sons and daughters. The onset of incubation in newly breeding females closely tracked ambient temperature in a pattern consistent with the maintenance of egg viability. Because of the very different climates in Montana and Alabama, females in these populations showed the opposite patterns of seasonal change in incubation onset and the opposite sex bias in egg-laying order. In females with breeding experience, incubation onset and sex bias in laying order were closely linked regardless of the climatic variation. In nests in which incubation began with the onset of egg laying, the first-laid eggs were mostly females in Montana, but mostly males in Alabama. Because in both populations, male, but not female, embryos grew faster when exposed to longer incubation, the sex-bias produced highly divergent sizes of male and female juveniles between the populations. Overall, the compensatory interaction between the onset of incubation and the sex-biased laying order achieved a compromise between maternal and offspring adaptations and contributed to rapid morphological divergence in sexual dimorphism between populations of the house finch breeding at the climatic extremes of the species range.     

Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches

Yolk androgens affect offspring hatching, begging, growth and survival in many bird species. If these effects are sex-specific, yolk androgen deposition may constitute a mechanism for differential investment in male and female offspring. We tested this hypothesis in zebra finches. In this species, females increase yolk-testosterone levels and produce male-biased sex ratios when paired to more attractive males. We therefore predicted that especially sons benefit from elevated yolk androgens. Eggs were injected with testosterone or sesame oil (controls) after 2 days of incubation. Testosterone had no clear effect on sex-specific embryonic mortality and changed the pattern of early nestling mortality independent of offspring sex. Testosterone-treated eggs took longer to hatch than control eggs. Control males begged significantly longer than females during the first days after hatching and grew significantly faster. These sex differences were reduced in offspring from testosterone-treated eggs due to prolonged begging durations of daughters, enhanced growth of daughters and reduced growth of sons. The results show that variation in maternal testosterone can play an important role in avian sex allocation due to its sex-specific effects on offspring begging and growth.     

Stress hormones: a link between maternal condition and sex-biased reproductive investment

In species where offspring fitness is sex-specifically influenced by maternal reproductive condition, sex allocation theory predicts that poor-quality mothers should invest in the evolutionarily less expensive sex. Despite an accumulation of evidence that mothers can sex-specifically modulate investment in offspring in relation to maternal quality, few mechanisms have been proposed as to how this is achieved. We explored a hormonal mechanism for sex-biased maternal investment by measuring and experimentally manipulating baseline levels of the stress hormone corticosterone in laying wild female European starlings (Sturnus vulgaris) and examining effects on sex ratio and sex-specific offspring phenotype adjustment. Here we show that baseline plasma corticosterone is negatively correlated with energetic body condition in laying starlings, and subsequent experimental elevation of maternal baseline plasma corticosterone increased yolk corticosterone without altering maternal condition or egg quality per se. Hormonal elevation resulted in the following: female-biased hatching sex ratios (caused by elevated male embryonic mortality), lighter male offspring at hatching (which subsequently grew more slowly during postnatal development), and lower cell-mediated immune (phytohemagglutinin) responses in males compared with control-born males; female offspring were unaffected by the manipulation in both years of the study. Elevated maternal corticosterone therefore resulted in a sex-biased adjustment of offspring quality favorable to female offspring via both a sex ratio bias and a modulation of male phenotype at hatching. In birds, deposition of yolk corticosterone may benefit mothers by acting as a bet-hedging strategy in stochastic environments where the correlation between environmental cues at laying (and therefore potentially maternal condition) and conditions during chick-rearing might be low and unpredictable. Together with recent studies in other vertebrate taxa, these results suggest that maternal stress hormones provide a mechanistic link between maternal quality and sex-biased maternal investment in offspring.     

Sex ratio evolution when fitness and dispersal vary

In a heterogeneous environment, when the fitness of males and females are differently influenced by habitat quality, habitat-dependent sex ratios may evolve to favor the production of the sex that benefits more (or loses less) from the local habitat. Similarly, sex-biased dispersal favors the evolution of habitat-dependent sex ratios. The present study documents the convergence stable sex ratios expected in the presence of sex-specific fitness gains when dispersal is partial, sex-biased or costly, using a simple model with patches of two qualities. Results show that partial dispersal reduces the sex ratio bias expected with sex-specific fitness gains. The direction of the sex ratio bias can be reversed by sex-biased dispersal or the existence of sex-specific dispersal costs, provided that fitness gains for the two sexes are not too different. The reversal of the sex ratio bias is more readily observed when sex-specific dispersal rates are opposite and extreme. Both dispersal and fitness gains, especially when they are sex-specific, should thus be considered when making predictions about sex ratio evolution in a heterogeneous environment.     

Sex allocation in yellow-legged gulls (Larus michahellis) depends on nutritional constraints on production of large last eggs

Male and female offspring can differ in their susceptibility to pre-natal (e.g. egg quality) and post-natal (e.g. sib–sib competition) conditions, and parents can therefore increase their individual fitness by adjusting these maternal effects according to offspring sex. In birds, egg mass and laying/hatching order are the main determinants of offspring viability, but these effects can act differently on each sex. In a previous study, relatively large last-laid (c-)eggs of yellow-legged gulls (Larus michahellis) were more likely to carry a female embryo. This suggests compensatory allocation of maternal resources to daughters from c-eggs, which suffer reduced viability. In the present study, we supplemented yellow-legged gulls with food during the laying period to experimentally test whether their nutritional conditions were responsible for the observed covariation between c-egg sex and mass. As predicted, food supplementation enhanced female c-eggs'' mass more than that of male c-eggs. Thus, this experiment indicates that mothers strategically allocated their resources to c-eggs, possibly in order to compensate for the larger susceptibility of daughters to hatching (and laying) order. The results also suggested that mothers decided on resource allocation depending on the sex of already ovulated c-eggs, rather than ovulating ova of either sex depending on food availability.     

Sex-related effects of maternal egg investment on offspring in relation to carotenoid availability in the great tit

1. Maternal carotenoids in the egg yolk have been hypothesized to promote maturation of the immune system and protect against free radical damages. Depending on availability, mothers may thus influence offspring quality by depositing variable amounts of carotenoids into the eggs. Sex allocation theory predicts that in good quality environments, females should invest into offspring of the sex that will provide larger fitness return, generally males. 2. In a field experiment we tested whether female great tits bias their investment towards males when carotenoid availability is increased, and whether male offspring of carotenoid-supplemented mothers show higher body condition. We partially cross-fostered hatchlings to disentangle maternal effects from post-hatching effects, and manipulated hen flea Ceratophyllus gallinae infestation to investigate the relationship between carotenoid availability and resistance to ectoparasites. 3. As predicted, we found that carotenoid-supplemented mothers produced males that were heavier than their sisters at hatching, while the reverse was true for control mothers. This suggests that carotenoid availability during egg production affects male and female hatchlings differentially, possibly via a differential allocation to male and female eggs. 4. A main effect of maternal supplementation became visible 14 days after hatching when nestlings hatched from eggs laid by carotenoid-supplemented mothers had gained significantly more mass than control nestlings. Independently of the carotenoid treatment, fleas impaired mass gain of nestlings during the first 9 days in large broods only and reduced tarsus length of male nestlings at an age of 14 days, suggesting a cost to mount a defence against parasites. 5. Overall, our results suggest that pre-laying availability of carotenoids affects nestling condition in a sex-specific way with potentially longer-lasting effects on offspring fitness.     

Euploid chicken embryos from eggs containing one, two or several yolks

A high incidence of haploid/diploid chimerism in chick embryos from strains of chickens selected for large size was postulated to be caused by the propensity of such hens to ovulate erratically. To test the hypothesis karyological analysis was made of embryos in eggs containing 1 or greater than 1 yolk. The eggs were from a line selected for multiple ovulation for 20 generations. Double and multiple-yolk eggs are a manifestation of an irregular ovulatory pattern. Ova in multiple yolk eggs were significantly less fertile and significantly fewer embryos survived to 18 h of incubation than single ovulated ova. In the sample of 342 embryos analysed, only 2 forms of heteroploidy occurred in frequencies of greater than 1.2%; 2n/4n mosaicism (5.8%) and 3n (5.0%). Only triploidy occurred significantly more frequently in eggs containing greater than 1 yolk (7.0%) than in single yolk eggs (none). The overwhelming majority of 3n embryos had a digynic origin (i.e from ova with 2 maternal pronuclei), as inferred from the sex chromosome complement. Erratic ovulation therefore resulted in suppression of second polar body extrusion leading to digynic triploidy. Multiple yolks had no effect on dispermy, the primary cause of 1n/2n chimaeric embryos, in single-yolked chicken eggs.     

Potential mechanisms of avian sex manipulation

The aim of this review is to consider the potential mechanisms birds may use to manipulate the sex of their progeny, and the possible role played by maternal hormones. Over the past few years there has been a surge of reports documenting the ability of birds to overcome the rigid process of chromosomal sex determination. However, while many of these studies leave us in little doubt that mechanisms allowing birds to achieve this feat do exist, we are only left with tantalizing suggestions as to what the precise mechanism or mechanisms may be. The quest to elucidate them is made no easier by the fact that a variety of environmental conditions have been invoked in relation to sex manipulation, and there is no reason to assume that any particular mechanism is conserved among the vast diversity of species that can achieve it. In fact, a number of intriguing proposals have been put forward. We begin by briefly reviewing some of the most recent examples of this phenomenon before highlighting some of the more plausible mechanisms, drawing on recent work from a variety of taxa. In birds, females are the heterogametic sex and so non-Mendelian segregation of the sex chromosomes could conceivably be under maternal control. Another suggestion is that follicles that ultimately give rise to males and females grow at different rates. Alternatively, the female might selectively abort embryos or 'dump lay' eggs of a particular sex, deny certain ova a chance of ovulation, fertilization or zygote formation, or selectively provision eggs so that there is sex-specific embryonic mortality. The ideas outlined in this review provide good starting points for testing the hypotheses both experimentally (behaviourally and physiologically) and theoretically.     

The adaptive value of stress-induced phenotypes: effects of maternally derived corticosterone on sex-biased investment, cost of reproduction, and maternal fitness

The question of why maternal stress influences offspring phenotype is of significant interest to evolutionary physiologists. Although embryonic exposure to maternally derived glucocorticoids (i.e., corticosterone) generally reduces offspring quality, effects may adaptively match maternal quality with offspring demand. We present results from an interannual field experiment in European starlings (Sturnus vulgaris) designed explicitly to examine the fitness consequences of exposing offspring to maternally derived stress hormones. We combined a manipulation of yolk corticosterone (yolk injections) with a manipulation of maternal chick-rearing ability (feather clipping of mothers) to quantify the adaptive value of corticosterone-induced offspring phenotypes in relation to maternal quality. We then examined how corticosterone-induced "matching" within this current reproductive attempt affected future fecundity and maternal survival. First, our results provide support that low-quality mothers transferring elevated corticosterone to eggs invest in daughters as predicted by sex allocation theory. Second, corticosterone-mediated sex-biased investment resulted in rapid male-biased mortality resulting in brood reduction, which provided a better match between maternal quality and brood demand. Third, corticosterone-mediated matching reduced investment in current reproduction for low-quality mothers, resulting in fitness gains through increased survival and future fecundity. Results indicate that the transfer of stress hormones to eggs by low-quality mothers can be adaptive since corticosterone-mediated sex-biased investment matches the quality of a mother to offspring demand, ultimately increasing maternal fitness. Our results also indicate that the branding of the proximate effects of maternal glucocorticoids on offspring as negative ignores the possibility that short-term phenotypic changes may actually increase maternal fitness.     

Maternal effort and joey growth in koalas (Phascolarctos cinereus)

The extent to which sex-biased maternal investment characterizes mammals is controversial, with less information available for evaluating patterns of maternal effort in marsupials than in placentals. Koalas Phascolarctos cinereus are size-dimorphic animals with a lengthy period of dependency and they reside in mating systems that might favour sex-biased maternal investment. We examined 18 years of data recorded from koalas living at the San Diego Zoo in order to examine how joey development and maternal condition might be connected. Koalas are pregnant for only 1 month, but joey emergence from the pouch does not occur until 32 weeks of age. Neither maternal condition nor age affected sex ratio at joey emergence, and both sexes had the same survivorship prospects. Koala dams transport and nurse joeys for close to 1 year, at which time the two sexes are size dimorphic. Given the poor-quality diet of koalas, combined with maternal transport of infants who are at least 25% of maternal mass, we suggest that infant rearing poses high energetic costs on koala females. We suggest that ecological and energetic constraints have moulded koala maternal strategies such that females maximize allocation of resources to offspring, regardless of sex, in order to increase prospects for joey survivorship.     

Comparison of the penetrability of the egg vestments in follicular oocytes, unfertilized and fertilized ova of the rabbit

Mixed populations of rabbit ovulated eggs and follicular oocytes, one labelled with a fluorescent marker, were transferred to the same tubal ampulla of an inseminated recipient female and were then recovered 3 hr later. There was no significant difference in the number spermatozoa penetrating to the perivitelline space or within the substance of the zona pellucida of follicular oocytes (immature or atretic) and mature ovulated ova. In contrast to mature ovulated ova, however, none of the spermatozoa reaching the perivitelline space of vesicular (dictyate) oocytes had attached to or penetrated the vitelline surface to enter the ooplasm.The same approach involving transfer of nonpenetrated eggs together with eggs penetrated previously in a donor female, demonstrated that prior entry of spermatozoa does not reduce the penetrability or receptivity of the rabbit zona pellucida to subsequent spermatozoa.These experiments indicate: (a) that the penetrability of the granulosa cell investment and/or zona pellucida of the rabbit follicular oocyte does not change from the time of antrum formation until the point at which follicular atresia ensures; (b) that between the time of initial LH stimulation and ovulation important changes mediating the onset of the fertizability of the dictyate oocyte of the rabbit probably occur at the vitelline surface; and (c) that in neither a qualitative nor quantitative sense has the demonstrably greater resistance of the rabbit zona pellucida to proteolysis following fertilization any physiological significance for sperm penetration.     

Ovulation and fertilization in the vole, Pitymys subterraneus

The females of Pitymys subterraneus bred in laboratory conditions have an irregular sexual cycle and induced ovulation. The first freshly ovulated eggs, surrounded by dense cumulus cells, appear in oviducts 10 h after copulation. Administering exogenous gonadotropins: pregnant mare's serum (PMS), human chorionic gonadotropin (hCG) or luteinizing hormone releasing hormone (LHRH), also induces ovulation in mature females of Pitymys subterraneus. In these experimental conditions females ovulate a similar number of eggs as after copulation. Dual stimulation (PMS and hCG plus copulation) does not result in the ovulation of a large number of normal ova, however, it does cause a release of degenerated oocytes.     

Early-life food stress hits females harder than males in insects: A meta-analysis of sex differences in environmental sensitivity

Fitness consequences of early-life environmental conditions are often sex-specific, but corresponding evidence for invertebrates remains inconclusive. Here, we use meta-analysis to evaluate sex-specific sensitivity to larval nutritional conditions in insects. Using literature-derived data for 85 species with broad phylogenetic and ecological coverage, we show that females are generally more sensitive to food stress than males. Stressful nutritional conditions during larval development typically lead to female-biased mortality and thus increasingly male-biased sex ratios of emerging adults. We further demonstrate that the general trend of higher sensitivity to food stress in females can primarily be attributed to their typically larger body size in insects and hence higher energy needs during development. By contrast, there is no consistent evidence of sex-biased sensitivity in sexually size-monomorphic species. Drawing conclusions regarding sex-biased sensitivity in species with male-biased size dimorphism remains to wait for the accumulation of relevant data. Our results suggest that environmental conditions leading to elevated juvenile mortality may potentially affect the performance of insect populations further by reducing the proportion of females among individuals reaching reproductive age. Accounting for sex-biased mortality is therefore essential to understanding the dynamics and demography of insect populations, not least importantly in the context of ongoing insect declines.