Constrained sex allocation in a parasitoid due to variation in male quality

The theory of constrained sex allocation posits that when a fraction of females in a haplodiploid population go unmated and thus produce only male offspring, mated females will evolve to lay a female-biased sex ratio. I examined evidence for constrained sex ratio evolution in the parasitic hymenopteran Uscana semifumipennis. Mated females in the laboratory produced more female-biased sex ratios than the sex ratio of adults hatching from field-collected eggs, consistent with constrained sex allocation theory. However, the male with whom a female mated affected her offspring sex ratio, even when sperm was successfully transferred, suggesting that constrained sex ratios can occur even in populations where all females succeed in mating. A positive relationship between sex ratio and fecundity indicates that females may become sperm-limited. Variation among males occurred even at low fecundity, however, suggesting that other factors may also be involved. Further, a quantitative genetic experiment found significant additive genetic variance in the population for the sex ratio of offspring produced by females. This has only rarely been demonstrated in a natural population of parasitoids, but is a necessary condition for sex ratio evolution. Finally, matings with larger males produced more female-biased offspring sex-ratios, suggesting positive selection on male size. Because the great majority of parasitic hymenoptera are monandrous, the finding of natural variation among males in their capacity to fertilize offspring, even after mating successfully, suggests that females may often be constrained in the sex allocation by inadequate number or quality of sperm transferred.     

How multiple mating by females affects sexual selection

Multiple mating by females is widely thought to encourage post-mating sexual selection and enhance female fitness. We show that whether polyandrous mating has these effects depends on two conditions. Condition 1 is the pattern of sperm utilization by females; specifically, whether, among females, male mating number, m (i.e. the number of times a male mates with one or more females) covaries with male offspring number, o. Polyandrous mating enhances sexual selection only when males who are successful at multiple mating also sire most or all of each of their mates'' offspring, i.e. only when Cov_♂(m,o), is positive. Condition 2 is the pattern of female reproductive life-history; specifically, whether female mating number, m, covaries with female offspring number, o. Only semelparity does not erode sexual selection, whereas iteroparity (i.e. when Cov_♀(m,o), is positive) always increases the variance in offspring numbers among females, which always decreases the intensity of sexual selection on males. To document the covariance between mating number and offspring number for each sex, it is necessary to assign progeny to all parents, as well as identify mating and non-mating individuals. To document significant fitness gains by females through iteroparity, it is necessary to determine the relative magnitudes of male as well as female contributions to the total variance in relative fitness. We show how such data can be collected, how often they are collected, and we explain the circumstances in which selection favouring multiple mating by females can be strong or weak.     

Sexual size dimorphism in parasitoid wasps

Sexual dimorphism in body length and proportion of overlap between the ranges of body length for males and females were estimated for 361 species of parasitoid wasps from 21 families. In most species, females are generally larger than males, though the range of male and female sizes overlap. Species in the family Ichneumonidae differ significantly from species in other families in three ways: (1) ichneumonids on average are larger, (2) in most species, females are generally smaller than males, and (3) on average, proportion overlap between the ranges of body length for males and females is greater. At present, there is a paucity of life history data on parasitoid wasp species for which size dimorphism is known. Thus it is not clear why ichneumonids differ from species in other families. Possible evolutionary explanations for variation in dimorphism among parasitoid wasp species are discussed.     

Sex allocation and investment into pre- and post-copulatory traits in simultaneous hermaphrodites: the role of polyandry and local sperm competition

Sex allocation theory predicts the optimal allocation to male and female reproduction in sexual organisms. In animals, most work on sex allocation has focused on species with separate sexes and our understanding of simultaneous hermaphrodites is patchier. Recent theory predicts that sex allocation in simultaneous hermaphrodites should strongly be affected by post-copulatory sexual selection, while the role of pre-copulatory sexual selection is much less clear. Here, we review sex allocation and sexual selection theory for simultaneous hermaphrodites, and identify several strong and potentially unwarranted assumptions. We then present a model that treats allocation to sexually selected traits as components of sex allocation and explore patterns of allocation when some of these assumptions are relaxed. For example, when investment into a male sexually selected trait leads to skews in sperm competition, causing local sperm competition, this is expected to lead to a reduced allocation to sperm production. We conclude that understanding the evolution of sex allocation in simultaneous hermaphrodites requires detailed knowledge of the different sexual selection processes and their relative importance. However, little is currently known quantitatively about sexual selection in simultaneous hermaphrodites, about what the underlying traits are, and about what drives and constrains their evolution. Future work should therefore aim at quantifying sexual selection and identifying the underlying traits along the pre- to post-copulatory axis.     

A sex allocation cost to polyandry in a parasitoid wasp

The costs and benefits of polyandry are central to understanding the near-ubiquity of female multiple mating. Here, we present evidence of a novel cost of polyandry: disrupted sex allocation. In Nasonia vitripennis, a species that is monandrous in the wild but engages in polyandry under laboratory culture conditions, sexual harassment during oviposition results in increased production of sons under conditions that favour female-biased sex ratios. In addition, females more likely to re-mate under harassment produce the least female-biased sex ratios, and these females are unable to mitigate this cost by increasing offspring production. Our results therefore argue that polyandry does not serve to mitigate the costs of harassment (convenience polyandry) in Nasonia. Furthermore, because males benefit from female-biased offspring sex ratios, harassment of ovipositing females also creates a novel cost of that harassment for males.     

Parental investment, sexual selection and sex ratios

Conventional sex roles imply caring females and competitive males. The evolution of sex role divergence is widely attributed to anisogamy initiating a self‐reinforcing process. The initial asymmetry in pre‐mating parental investment (eggs vs. sperm) is assumed to promote even greater divergence in post‐mating parental investment (parental care). But do we really understand the process? Trivers [Sexual Selection and the Descent of Man 1871–1971 (1972), Aldine Press, Chicago] introduced two arguments with a female and male perspective on whether to care for offspring that try to link pre‐mating and post‐mating investment. Here we review their merits and subsequent theoretical developments. The first argument is that females are more committed than males to providing care because they stand to lose a greater initial investment. This, however, commits the ‘Concorde Fallacy’ as optimal decisions should depend on future pay‐offs not past costs. Although the argument can be rephrased in terms of residual reproductive value when past investment affects future pay‐offs, it remains weak. The factors likely to change future pay‐offs seem to work against females providing more care than males. The second argument takes the reasonable premise that anisogamy produces a male‐biased operational sex ratio (OSR) leading to males competing for mates. Male care is then predicted to be less likely to evolve as it consumes resources that could otherwise be used to increase competitiveness. However, given each offspring has precisely two genetic parents (the Fisher condition), a biased OSR generates frequency‐dependent selection, analogous to Fisherian sex ratio selection, that favours increased parental investment by whichever sex faces more intense competition. Sex role divergence is therefore still an evolutionary conundrum. Here we review some possible solutions. Factors that promote conventional sex roles are sexual selection on males (but non‐random variance in male mating success must be high to override the Fisher condition), loss of paternity because of female multiple mating or group spawning and patterns of mortality that generate female‐biased adult sex ratios (ASR). We present an integrative model that shows how these factors interact to generate sex roles. We emphasize the need to distinguish between the ASR and the operational sex ratio (OSR). If mortality is higher when caring than competing this diminishes the likelihood of sex role divergence because this strongly limits the mating success of the earlier deserting sex. We illustrate this in a model where a change in relative mortality rates while caring and competing generates a shift from a mammalian type breeding system (female‐only care, male‐biased OSR and female‐biased ASR) to an avian type system (biparental care and a male‐biased OSR and ASR).     

The causes and implications of sex role diversity in shorebird breeding systems

Males and females often exhibit different behaviours during mate acquisition, pair-bonding and parenting, and a convenient label to characterize these behaviours is sex role. The diverse roles that male and female shorebirds (plovers, sandpipers and allies) exhibit in mating and parenting have played a key role in advancing mainstream theories in avian ecology and behavioural biology including sexual selection, sexual conflict and parental cooperation. Recent advances in shorebird research have also highlighted the significance of the social environment in driving sex role behaviours by linking the adult sex ratio with breeding behaviour and population demography. Here we review the key advances in sex role research using shorebirds as an ecological model system. We identify knowledge gaps and argue that shorebirds have untapped potential to accelerate diverse research fields including evolutionary genomics, movement ecology, social networks and environmental changes. Future studies of sex roles will benefit from individual-based monitoring using advanced tracking technologies, and from multi-team collaborations that are facilitated by standardized data collection methodologies across different species in the field. These advances will not only contribute to our understanding of reproductive strategies, but they will also have knock-on effects on predicting population resilience to environmental changes and on prioritizing species for conservation.     

A measure of sexual selection for interspecific comparisons of species with diversified mating systems and different mortality schedules

Based on variances in components of lifetime reproductive success (LRS), a new index of the intensity of sexual selection was proposed mainly useful for interspecific comparisons. The index was defined as the male to female ratio of the standardized variance in mating efficiency during mating period. The index can to a large extent exclude the effect from natural selection which commonly act on both sexes in mating period and also from mortality in pre-reproductive period. This empirical measure has some defects in the strict sense (i.e., dichotomy of natural and sexual selection), however, it enables interspecific comparisons of the intensity of sexual selection among different taxonomic groups of animals with various mating systems and mortality schedules.     

Exposure to the neonicotinoid imidacloprid disrupts sex allocation cue use during superparasitism in the parasitoid wasp Nasonia vitripennis

1. Neonicotinoid insecticides are potent neurotoxins of significant economic importance. However, it is clear that their use can adversely impact beneficial insects in the environment, even at low, sub‐lethal doses. 2. It has recently been shown that the neonicotinoid imidacloprid disrupts adaptive sex allocation in the parasitoid wasp Nasonia vitripennis (Walker) by limiting their ability to respond to the presence of other females on oviposition patches. In the present study, that work was extended to explore whether sex allocation when superparasitising – laying eggs on a host that has already been parasitised – is also disrupted by imidacloprid. 3. Under superparasitism, sex allocation theory predicts that females should vary their offspring sex ratio in relation to their relative clutch size. It was found that sex allocation under superparasitism in Nasonia is disrupted in a dose‐dependent manner, with exposed females producing more daughters. 4. Importantly, imidacloprid does not appear to influence the ability of females to estimate the number of eggs already present on a host, suggesting a disassociation between the sex ratio and clutch size cues. 5. The present work highlights the fitness costs to beneficial insects of exposure to neonicotinoids, but also provides clues as to how female Nasonia use information when allocating sex.     

Sex allocation and sexual conflict in simultaneously hermaphroditic animals

Links between sex allocation (SA) and sexual conflict in simultaneous hermaphrodites have been evident since Charnov''s landmark paper published 30 years ago. We discuss two links, namely the potential for sexual conflict over SA between sperm donor and recipient, and the importance of post-copulatory sexual selection and the resulting sexual conflict for the evolution of SA. We cover the little empirical and theoretical work exploring these links, and present an experimental test of one theoretical prediction. The link between SA and sexual conflict is an interesting field for future empirical and theoretical research.     

Different effects of mating group size as male and as female on sex allocation in a simultaneous hermaphrodite

Sex allocation theory predicts that the optimal sexual resource allocation of simultaneous hermaphrodites is affected by mating group size (MGS). Although the original concept assumes that the MGS does not differ between male and female functions, the MGS in the male function (MGSm; i.e., the number of sperm recipients the focal individual can deliver its sperm to plus one) and that in the female function (MGSf; the number of sperm donors plus one) do not always coincide and may differently affect the optimal sex allocation. Moreover, reproductive costs can be split into “variable” (e.g., sperm and eggs) and “fixed” (e.g., genitalia) costs, but these have been seldom distinguished in empirical studies. We examined the effects of MGSm and MGSf on the fixed and variable reproductive investments in the sessilian barnacle Balanus rostratus. The results showed that MGSm had a positive effect on sex allocation, whereas MGSf had a nearly significant negative effect. Moreover, the “fixed” cost varied with body size and both aspects of MGS. We argue that the two aspects of MGS should be distinguished for organisms with unilateral mating.     

Does time until mating affect progeny sex ratio? A manipulative experiment with the parasitoid wasp Aphelinus asychis

In haplodiploid organisms, unmated or sperm depleted females are “constrained” to produce only male progeny. If such constrained females reproduce, the population sex ratio will shift toward males and unconstrained females will be selected to produce more females. Assuming that a female's own time spent constrained is an index of the population-wide level of constrained oviposition, and that constrained and unconstrained females reproduce at the same rate, the proportion of sons that females produce when unconstrained should decrease with increasing time spent constrained. Alternatively, if females cannot measure time spent constrained or if time spent constrained is not an index to the level of constrained oviposition in the population, the proportion of sons among progeny produced when unconstrained should not depend upon time spent constrained and should be female biased to an extent depending upon the average time spent constrained over evolutionary time. To test these predictions, we manipulated the amount of time spent virgin in the parasitoid wasp Aphelinus asychis Walker (Hymenoptera: Aphelinidae) and measured the number of males and females among progeny produced before and after mating. First, we found no interaction between age and age at mating in their effect on fecundity, which suggests that mating does not change fecundity. Second, we found that females mated at 8 days and 15 days produced equal sex ratios after mating but these were slightly more female biased than the sex ratios of females mated at 1 day. This observed “step response” suggests that females may perceive time from emergence to mating as a discrete rather than a continuous variable (i.e., short versus long), or that females do not perceive time per se but assess their age class (i.e., young versus old) at the time of mating.     

Sperm limitation affects sex allocation in a parasitoid wasp Nasonia vitripennis

Insect reproduction is influenced by various external factors including temperature, a well-studied constraint. We investigated to what extent different levels of sperm limitation of males exposed to different heat stresses (34 and 36℃) afFect fem ales' offspring production and sex allocation in Nasonia vitripennis. In this haplodiploid parasitoid wasp attacking different species of pest flies, we investigated the effect of the quantity of sperm females received and stored in their spermatheca on their sperm use decisions, hence sex allocation, over successive ovipositions. In particular, we compared the sex allocation of females presenting three levels of sperm limitation (i.e.,mated with control, 34 ℃ heat-stressed or 36℃heat-stressed males) on each host they parasitized. To disentangle the potential reduction of sperm quality after a heat stress exposure from that of sperm quantity, we also explored the clutch size and sex ratio produced by fem ales that were partially sperm limited after copulating with multiply mated males. Independently of their sperm numbers, all types of fem ales produced a similar total number of offspring, but the more limited ones had fewer daughters. Sperm limitation further affected the distribution of daughters' production across time.In addition to constraints acting on female physiology, male fertility should therefore be considered in studies measuring reproductive outputs of insects submitted to heat stresses.     

Differential sperm expenditure reveals a possible role for post‐copulatory sexual selection in a lekking moth

Male reproductive success in the lesser wax moth Achroia grisella is strongly determined by pre‐copulatory mate choice, during which females choose among males aggregated in small leks based on the attractiveness of ultrasonic songs. Nothing is known about the potential of post‐copulatory mechanisms to affect male reproductive success. However, there is evidence that females at least occasionally remate with a second male and that males are unable to produce ejaculates quickly after a previous copulation. Here we investigated the effects of mating history on ejaculate size and demonstrate that the number of transferred sperm significantly decreased from first (i.e., virgin) to second (i.e., nonvirgin) copulation within individual males. For males of identical age, the number of sperm transferred was higher in virgin than in nonvirgin copulations, too, demonstrating that mating history, is responsible for the decrease in sperm numbers transferred and not the concomitant age difference. Furthermore, the number of transferred sperm was significantly repeatable within males. The demonstrated variation in ejaculate size both between subsequent copulations as well as among individuals suggests that there is allocation of a possibly limited amount of sperm. Because female fecundity is not limited by sperm availability in this system, post‐copulatory mechanisms, in particular sperm competition, may play a previously underappreciated role in the lesser wax moth mating system.     

The mismeasurement of sexual selection

Sexual selection can explain major micro‐ and macro‐evolutionary patterns. Much of current theory predicts that the strength of sexual selection (i) is driven by the relative abundance of males and females prepared to mate (i.e. the operational sex ratio, OSR) and (ii) can be generally estimated by calculating intra‐sexual variation in mating success (e.g. the opportunity for sexual selection, I_s). Here, we demonstrate the problematic nature of these predictions. The OSR and I_s only accurately predict sexual selection under a limited set of circumstances, and more specifically, only when mate monopolization is extremely strong. If mate monopolization is not strong, using OSR or I_s as proxies or measures of sexual selection is expected to produce spurious results that lead to the false conclusion that sexual selection is strong when it is actually weak. These findings call into question the validity of empirical conclusions based on these measures of sexual selection.     

Operational sex ratio influences the opportunity for sexual selection in guppies

The opportunity for sexual selection was greater when the operational sex ratio (OSR) in guppies Poecilia reticulata was biased towards males. This could be due to an increase in both male-male competition and female mate choice under male-biased OSR.     

Within‐season variation in sexual selection in a fish with dynamic sex roles

The strength of sexual selection may vary between species, among populations and within populations over time. While there is growing evidence that sexual selection may vary between years, less is known about variation in sexual selection within a season. Here, we investigate within‐season variation in sexual selection in male two‐spotted gobies (Gobiusculus flavescens). This marine fish experiences a seasonal change in the operational sex ratio from male‐ to female‐biased, resulting in a dramatic decrease in male mating competition over the breeding season. We therefore expected stronger sexual selection on males early in the season. We sampled nests and nest‐holding males early and late in the breeding season and used microsatellite markers to determine male mating and reproductive success. We first analysed sexual selection associated with the acquisition of nests by comparing nest‐holding males to population samples. Among nest‐holders, we calculated the potential strength of sexual selection and selection on phenotypic traits. We found remarkable within‐season variation in sexual selection. Selection on male body size related to nest acquisition changed from positive to negative over the season. The opportunity for sexual selection among nest‐holders was significantly greater early in the season rather than late in the season, partly due to more unmated males. Overall, our study documents a within‐season change in sexual selection that corresponds with a predictable change in the operational sex ratio. We suggest that many species may experience within‐season changes in sexual selection and that such dynamics are important for understanding how sexual selection operates in the wild.     

Anisogamy,sexual selection,and the evolution and maintenance of sex

Summary In the present paper we distinguish between two aspects of sexual reproduction. Genetic recombination is a universal features of the sexual process. It is a primitive condition found in simple, single-celled organisms, as well as in higher plants and animals. Its function is primarily to repair genetic damage and eliminate deleterious mutations. Recombination also produces new variation, however, and this can provide the basis for adaptive evolutionary change in spatially and temporally variable environments.The other feature usually associated with sexual reproduction, differentiated male and female roles, is a derived condition, largely restricted to complex, diploid, multicellular organisms. The evolution of anisogamous gametes (small, mobile male gametes containing only genetic material, and large, relatively immobile female gametes containing both genetic material and resources for the developing offspring) not only established the fundamental basis for maleness and femaleness, it also led to an asymmetry between the sexes in the allocation of resources to mating and offspring. Whereas females allocate their resources primarily to offspring, the existence of many male gametes for each female one results in sexual selection on males to allocate their resources to traits that enhance success in competition for fertilizations. A consequence of this reproductive competition, higher variance in male than female reproductive success, results in more intense selection on males.The greater response of males to both stabilizing and directional selection constitutes an evolutionary advantage of males that partially compensates for the cost of producing them. The increased fitness contributed by sexual selection on males will complement the advantages of genetic recombination for DNA repair and elimination of deleterious mutations in any outcrossing breeding system in which males contribute only genetic material to their offspring. Higher plants and animals tend to maintain sexual reproduction in part because of the enhanced fitness of offspring resulting from sexual selection at the level of individual organisms, and in part because of the superiority of sexual populations in competition with asexual clones.