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.     

Mating frequency and resource allocation to male and female function in the simultaneous hermaphrodite land snail Arianta arbustorum

Sex allocation theory predicts that mating frequency and long‐term sperm storage affect the relative allocation to male and female function in simultaneous hermaphrodites. We examined the effect of mating frequency on male and female reproductive output (number of sperm delivered and eggs deposited) and on the resources allocated to the male and female function (dry mass, nitrogen and carbon contents of spermatophores and eggs) in individuals of the simultaneous hermaphrodite land snail Arianta arbustorum. Similar numbers of sperm were delivered in successive copulations. Consequently, the total number of sperm transferred increased with increasing number of copulations. In contrast, the total number of eggs produced was not influenced by the number of copulations. Energy allocation to gamete production expressed as dry mass, nitrogen or carbon content was highly female‐biased (>95% in all estimates). With increasing number of copulations the relative nitrogen allocation to the male function increased from 1.7% (one copulation) to 4.7% (three copulations), but the overall reproductive allocation remained highly female‐biased. At the individual level, we did not find any trade‐off between male and female reproductive function. In contrast, there was a significant positive correlation between the resources allocated to the male and female function. Snails that delivered many sperm also produced a large number of eggs. This finding contradicts current theory of sex allocation in simultaneous hermaphrodites.     

Accessory male investment can undermine the evolutionary stability of simultaneous hermaphroditism

Sex allocation (SA) models are traditionally based on the implicit assumption that hermaphroditism must meet criteria that make it stable against transition to dioecy. This, however, puts serious constraints on the adaptive values that SA can attain. A transition to gonochorism may, however, be impossible in many systems and therefore realized SA in hermaphrodites may not be limited by conditions that guarantee stability against dioecy. We here relax these conditions and explore how sexual selection on male accessory investments (e.g. a penis) that offer a paternity benefit affects the evolutionary stable strategy SA in outcrossing, simultaneous hermaphrodites. Across much of the parameter space, our model predicts male allocations well above 50 per cent. These predictions can help to explain apparently ‘maladaptive’ hermaphrodite systems.     

Multivariate quantitative genetics and the lek paradox: genetic variance in male sexually selected traits of Drosophila serrata under field conditions

Single male sexually selected traits have been found to exhibit substantial genetic variance, even though natural and sexual selection are predicted to deplete genetic variance in these traits. We tested whether genetic variance in multiple male display traits of Drosophila serrata was maintained under field conditions. A breeding design involving 300 field-reared males and their laboratory-reared offspring allowed the estimation of the genetic variance-covariance matrix for six male cuticular hydrocarbons (CHCs) under field conditions. Despite individual CHCs displaying substantial genetic variance under field conditions, the vast majority of genetic variance in CHCs was not closely associated with the direction of sexual selection measured on field phenotypes. Relative concentrations of three CHCs correlated positively with body size in the field, but not under laboratory conditions, suggesting condition-dependent expression of CHCs under field conditions. Therefore condition dependence may not maintain genetic variance in preferred combinations of male CHCs under field conditions, suggesting that the large mutational target supplied by the evolution of condition dependence may not provide a solution to the lek paradox in this species. Sustained sexual selection may be adequate to deplete genetic variance in the direction of selection, perhaps as a consequence of the low rate of favorable mutations expected in multiple trait systems.     

Determinants of mating and sperm‐transfer success in a simultaneous hermaphrodite

The number of mating partners an individual has within a population is a crucial parameter in sex allocation theory for simultaneous hermaphrodites because it is predicted to be one of the main parameters influencing sex allocation. However, little is known about the factors that determine the number of mates in simultaneous hermaphrodites. Furthermore, in order to understand the benefits obtained by resource allocation into the male function it is important to identify the factors that predict sperm‐transfer success, i.e. the number of sperm a donor manages to store in a mate. In this study we experimentally tested how social group size (i.e. the number of all potential mates within a population) and density affect the number of mates and sperm‐transfer success in the outcrossing hermaphroditic flatworm Macrostomum lignano. In addition, we assessed whether these parameters covary with morphological traits, such as body size, testis size and genital morphology. For this we used a method, which allows tracking sperm of a labelled donor in an unlabelled mate. We found considerable variation in the number of mates and sperm‐transfer success between individuals. The number of mates increased with social group size, and was higher in worms with larger testes, but there was no effect of density. Similarly, sperm‐transfer success was affected by social group size and testis size, but in addition this parameter was influenced by genital morphology. Our study demonstrates for the first time that the social context and the morphology of sperm donors are important predictors of the number of mates and sperm‐transfer success in a simultaneous hermaphrodite. Based on these findings, we hypothesize that sex allocation influences the mating behaviour and outcome of sperm competition.     

Experimental evolution under varying sex ratio and nutrient availability modulates male mating success in Drosophila melanogaster

Biased population sex ratios can alter optimal male mating strategies, and allocation to reproductive traits depends on nutrient availability. However, there is little information on how nutrition interacts with sex ratio to influence the evolution of pre-copulatory and post-copulatory traits separately. To address this omission, we test how male mating success and reproductive investment evolve under varying sex ratios and adult diet in Drosophila melanogaster, using experimental evolution. We found that sex ratio and nutrient availability interacted to determine male pre-copulatory performance. Males from female-biased populations were slow to mate when they evolved under protein restriction. By contrast, we found direct and non-interacting effects of sex ratio and nutrient availability on post-copulatory success. Males that evolved under protein restriction were relatively poor at suppressing female remating. Males that evolved under equal sex ratios fathered more offspring and were better at supressing female remating, relative to males from male-biased or female-biased populations. These results support the idea that sex ratios and nutrition interact to determine the evolution of pre-copulatory mating traits, but independently influence the evolution of post-copulatory traits.     

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.     

Sexual selection without sexual dimorphism: Bateman gradients in a simultaneous hermaphrodite

One of the most general patterns in sexual selection is stronger selection on mating activity in males than in females. This asymmetry is thought to result from the higher energetic cost of producing one female compared to one male gamete (anisogamy). However, most studies focused on gonochoric species with strong sexual dimorphism, in which males and females are necessarily under different selection regimes. The question remains whether anisogamy alone would suffice to produce such differences. In simultaneous hermaphrodites one can compare sexual selection on the male and female functions in the absence of sexual dimorphism. Here we quantify sexual selection in the hermaphroditic freshwater snail Physa acuta under laboratory conditions. We combine exhaustive behavioral records of mating activity in mating groups and molecular paternity assignment to measure the mating success and reproductive success of 120 individuals. Our results validate the prediction of stronger selection to gain mating partners in the male than in the female function. Moreover, we did not detect cross‐sex effects on fitness, or correlations between male and female production of offspring over the course of our experiment. We conclude that with respect to sexual selection P. acuta is comparable to gonochorists, confirming that anisogamy is a sufficient explanation for the differences in sexual selection regimes between sexes.     

Opposing selection on a sexually dimorphic trait through female choice and male competition in a water boatman

Female choice and male-male competition are traditionally considered to act in concert, with male competition facilitating female choice. This situation would enforce the strength of directional selection, which could reduce genetic variation and thus the benefits of choice. Here I show that in a water boatman, Sigara falleni, the direction of selection through female choice and male competition vary among traits under laboratory conditions. The two forces were mutually enforcive in acting on body size but exerted opposing selection on a sexually selected trait, male foreleg pala size. Female choice favored large palae, whereas male competition favored smaller palae, suggesting that large palae are costly in competition. This conflicting selection through female choice and male competition could be one of the forces that contribute to the maintenance of genetic variation in sexually selected traits.     

Social situation,sperm competition and sex allocation in a simultaneous hermaphrodite parasite,the cestode Schistocephalus solidus

Evolutionary theory predicts an influence of mating group size on sex allocation in simultaneous hermaphrodites. We experimentally manipulated the social situation during reproduction in a simultaneous hermaphrodite parasite, the tapeworm Schistocephalus solidus, by placing worms as singles, pairs or triplets into an in vitro system that replaces the final host. We then determined the reproductive allocation patterns after 24 h (i.e. before the start of egg release) and after 72 h (i.e. around the peak of egg release rate) using stereology. After 24 h, sex allocation strongly depended on worm volume (which is determined in the second intermediate host), but was not significantly affected by the social situation experienced during reproduction. After 72 h, worms in groups had less vesicular sperm (i.e. sperm to be used in future inseminations) than singles. They also stored significantly more received sperm in their seminal receptacles than singles, suggesting that more sperm had been transferred in groups. Moreover, worms in triplets stored significantly more received sperm than worms in pairs, suggesting that they either mated more often and/or transferred more sperm per mating. This suggests a behavioural response to the increased risk of sperm competition in triplets. We further discuss the relative importance of sex allocation decisions at different life‐history stages.     

Environmental and demographic drivers of male mating success vary across sequential reproductive episodes in a polygynous breeder

Ecological and social factors underpinning the inequality of male mating success in animal societies can be related to sex ratio, sexual conflict between breeders, effects of nonbreeders, resource dispersion, climatic conditions, and the various sequential stages of mating competition that constitute the sexual selection process. Here, we conducted an individual‐based study to investigate how local resource availability and demography interact with annual climate conditions to determine the degree of male mating inequality, and thus opportunity for sexual selection across two sequential reproductive episodes (harem and subsequent mate acquisition) in a naturally regulated (feral) horse population in Sable Island National Park Preserve, Canada. Using a 5‐year, spatially explicit, mark‐resight dataset and hierarchical mixed‐effects linear modeling, we evaluated the influence of adult sex ratio (ASR) on mating success and then tested for effects of freshwater availability, density, unpaired male abundance, and precipitation during each breeding season. Unpaired male abundance, freshwater availability, and ASR differed in their effects on male mating success according to year and selection episode. Opportunity for sexual selection in males associated with harem acquisition increased with ASR, and unpaired male abundance further explained weather‐related interannual variation after accounting for ASR. In contrast, once a harem was secured, ASR had little effect on male mating inequality in regard to acquiring additional females, while interannual variation in mating inequality increased with decreasing freshwater availability. Our findings show that local demography, resource availability, and weather effect opportunity for sexual selection in males differently depending on selection episode, and can attenuate or accentuate effects of ASR.     

Direct detection of male quality can facilitate the evolution of female choosiness and indicators of good genes: Evolution across a continuum of indicator mechanisms

The evolution of mating displays as indicators of male quality has been the subject of extensive theoretical and empirical research for over four decades. Research has also addressed the evolution of female mate choice favoring such indicators. Yet, much debate still exists about whether displays can evolve through the indirect benefits of female mate choice. Here, we use a population genetic model to investigate how the extent to which females can directly detect male quality influences the evolution of female choosiness and male displays. We use a continuum framework that incorporates indicator mechanisms that are traditionally modeled separately. Counter to intuition, we find that intermediate levels of direct detection of male quality can facilitate, rather than impede, the evolution of female choosiness and male displays in broad regions of this continuum. We examine how this evolution is driven by selective forces on genetic quality and on the display, and find that direct detection of male quality results in stronger indirect selection favoring female choosiness. Our results imply that displays maybe more likely to evolve when female choosiness has already evolved to discriminate perceptible forms of male quality. They also highlight the importance of considering general female choosiness, as well as preference, in studies of “good genes.”     

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.     

Differential effects of genetic vs. environmental quality in Drosophila melanogaster suggest multiple forms of condition dependence

Condition is a central concept in evolutionary ecology, but the roles of genetic and environmental quality in condition‐dependent trait expression remain poorly understood. Theory suggests that condition integrates genetic, epigenetic and somatic factors, and therefore predicts alignment between the phenotypic effects of genetic and environmental quality. To test this key prediction, we manipulated both genetic (mutational) and environmental (dietary) quality in Drosophila melanogaster and examined responses in morphological and chemical (cuticular hydrocarbon, CHC) traits in both sexes. While the phenotypic effects of diet were consistent among genotypes, effects of mutation load varied in magnitude and direction. Average effects of diet and mutation were aligned for most morphological traits, but non‐aligned for the male sexcombs and CHCs in both sexes. Our results suggest the existence of distinct forms of condition dependence, one integrating both genetic and environmental effects and the other purely environmental. We propose a model to account for these observations.     

Lifetime reproductive output in a hermaphrodite cestode when reproducing alone or in pairs: a time cost of pairing

The cestode Schistocephalus solidus is a facultatively self-fertilising simultaneous hermaphrodite. Here we test for differences in the starting point, the rate, and the magnitude of egg production between individuals allowed to reproduce alone (only self-fertilisation possible) or in pairs (both self- and cross-fertilisation possible). Specifically, we want to distinguish between alternative processes responsible for the lower egg production in paired individuals observed in an earlier study (Wedekind et al., 1998). We designed an improved in vitro system, replacing the bird final host that allows us to measure, with high temporal resolution, the timing and magnitude of lifetime egg production of worms in these two social situations. We found that the experimental groups did not differ significantly in the starting point of egg production. However, the temporal pattern in egg production differed between them, in that paired individuals had a lower rate of egg production. This, however, did not lead to a significant reduction in lifetime egg production, as pairs compensated for the lower rate by producing eggs longer than single individuals. We argue that the lower rate of egg production may nevertheless lead to a time cost of pairing in the study species, and that this cost is likely to represent a cost of outcrossing due to sexual selection. This revised version was published online in July 2006 with corrections to the Cover Date.     

Immune system activation affects male sexual signal and reproductive potential in crickets

Parasite-mediated sexual selection theory posits that individuals(usually females) choose mates by assessing the expression ofcostly secondary sexual signals, which provide reliable indicationsof parasite resistance. If these signals are indeed reliable,then immune-compromised males are predicted to exhibit changesin the sexual signal that are discernable by the female. Moreover,the mating pair is predicted to exhibit some reduction in reproductivefitness if the male is immune compromised. Here, we addressedthese predictions in the ground cricket, Allonemobius socius,by injecting juvenile males with lipopolysaccarides, which allowedus to activate the immune system without the introduction ofa metabolically active pathogen. As a consequence, we were ableto disentangle the cost of immune system activation from thecost of infection. We found that immune activation had a long-termeffect on male calling song and the males' ability to providepaternal resources, which can constrain male and female reproductivepotential. We also found that song interpulse interval variedsignificantly with the male's immune treatment and may thereforeprovide choosy females with a way to avoid mating with immune-compromisedmales. In short, our data support the parasite-mediated theoryof sexual selection, suggesting that female's gain direct benefitsby mating with males who are immune competent.     

Resource availability,mating opportunity and sexual selection intensity influence the expression of male alternative reproductive tactics

The expression of alternative reproductive tactics can be plastic and occur simultaneously depending on cues that vary spatially or temporally. For example, variation in resources and sexual selection intensity is expected to influence the pay‐off of each tactic and shape the decision of which tactic to employ. Males of the nuptial gift‐giving spider Pisaura mirabilis can adopt three tactics: offering a genuine prey gift, a ‘worthless’ non‐nutritious gift or no gift. We hypothesized that resources and/or male body condition, and mating opportunity and sexual selection intensity, vary over the course of the mating season to shape the co‐existence of alternative traits. We measured these variables in the field over two seasons, to investigate the predictions that as the mating season progresses, (i) males become more likely to employ a gift‐giving tactic, and (ii) the likelihood of switching from worthless to genuine gifts increases. Prey availability increased over the season and co‐varied with the propensity of males to employ the gift‐giving tactic, but we found no support for condition‐dependent gift giving. Males responded to an increase in female availability by increasing their mating effort (gift production). Furthermore, the frequency of genuine gift use increased with sexual selection intensity, consistent with the assumption that sperm competition intensity increases with time. Our results suggest that the frequency of alternative tactics is shaped by seasonal changes in ecological factors and sexual selection. This leads to relaxed selection for the gift‐giving tactic early in the season when females are less choosy and resources more scarce, and increased selection for genuine gifts later in the season driven by mating opportunity and risk of sperm competition.     

Bigger testes increase paternity in a simultaneous hermaphrodite,independently of the sperm competition level

Hermaphroditic animals face the fundamental evolutionary optimization problem of allocating their resources to their male vs. female reproductive function (e.g. testes and sperm vs. ovaries and eggs), and this optimal sex allocation can be affected by both pre‐ and post‐copulatory sexual selection. For example, local sperm competition (LSC) – the competition between related sperm for the fertilization of a partner's ova – occurs in small mating groups and can favour a female‐biased sex allocation, because, under LSC, investment into sperm production is predicted to show diminishing fitness returns. Here, we test whether higher testis investment increases an individual's paternity success under sperm competition, and whether the strength of this effect diminishes when LSC is stronger, as predicted by sex allocation theory. We created two subsets of individuals of the simultaneously hermaphroditic flatworm Macrostomum lignano – by sampling worms from either the highest or lowest quartile of the testis investment distribution – and estimated their paternity success in group sizes of either three (strong LSC) or eight individuals (weak LSC). Specifically, using transgenic focal individuals expressing a dominant green‐fluorescent protein marker, we showed that worms with high testis investment sired 22% more offspring relative to those with low investment, corroborating previous findings in M. lignano and other species. However, the strength of this effect was not significantly modulated by the experienced group size, contrasting theoretical expectations of more strongly diminishing fitness returns under strong LSC. We discuss the possible implications for the evolutionary maintenance of hermaphroditism in M. lignano.