Size-assortative mating and non-reciprocal copulation in a hermaphroditic intertidal limpet: test of the mate availability hypothesis

Mating behaviour and mating patterns are affected to a large extent by body size in both hermaphrodites and gonochorists. Detailed research on mating patterns, mate choice, pre- and post-copulatory sexual selection in marine pulmonates is wanting, thus warranting more attention as a study system in the future. The simultaneous hermaphroditic limpet Siphonaria capensis (Pulmonata: Basommatophora) shows size-dependent fecundity, and acts as a suitable organism to test the effects of body size on mating patterns, mating success, gender expression and reciprocity in hermaphroditic marine gastropods. We mainly used bootstrap resampling techniques to estimate the effects of different factors on mating patterns. In the populations studied, a strong size-assortative mating pattern was observed, where small-scale spatial distribution of potential mating partners (the mate availability hypothesis) could explain 65% of this pattern, while mate choice and mating constraints explaining the rest. No significant difference in mating success between limpets with different body size was found, even though in one population, the sperm recipients were larger than the non-copulating limpets. Interestingly, we found that intromission was non-reciprocal during copulations. This may mean that this species does not conform to the common rule of reciprocity predicted for hermaphrodites, unless there is sex-role alternation between individuals in a mating pair. The mating partners consisted of similar sized, acting males and females, thus without any indication of the body size determining the gender expression. The matings took place in early mornings only at spring tides and the animals were observed laying egg masses only during neap tides. Since siphonariid limpets possess both a spermatheca and a seminal vesicle, which may have either a sperm storing and/or digestive function, post-copulatory sexual selection (e.g., sperm competition) cannot be dismissed.     

Strategic mating effort in a simultaneous hermaphrodite

Sexual selection theory for simultaneously hermaphroditic animals predicts an overall preference for inseminating partners that have a relatively higher female fecundity. Previous work on the link between male mating decisions and female fecundity has primarily focused on the effect of the partners’ body size using existing variation in this trait within a study population. On the assumption that the body size is positively correlated with female fecundity, sperm donors should preferentially inseminate relatively larger individuals to obtain a higher fitness gain through their male sex function. However, empirical evidence for such size-dependent mate choice in simultaneous hermaphrodites is equivocal, possibly because of confounding variables. We studied the mating behavior of the simultaneously hermaphroditic flatworm Macrostomum lignano and tested for a strategic mating effort in response to the feeding status of the partner. We experimentally manipulated the feeding status of potential mating partners in order to generate variation in female fecundity among them and tested whether this affected the copulation number and the number of sperm that the focal worm managed to store in the partner’s sperm storage organ. We found that the manipulation of the feeding status had a strong effect on the body size of the potential mating partners and that focal worms copulated more frequently with, and stored more sperm in well-fed partners compared to unfed partners. Our results suggest that M. lignano adjusts its mating effort in response to the feeding status of the mating partner.     

Simultaneous hermaphroditism in the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae): an undescribed sexual system in the decapod Crustacea

Simultaneous hermaphroditism with outcrossing, a previously unconfirmed sexual system in decapod crustaceans, is documented in the shrimp Lysmata wurdemanni (Gibbes), using time-lapse video observations on mating in pairs of “female-phase” (FP) individuals. Copulations between FPs resulted in successful spawning and development of embryos. However, female-phase hermaphrodites maintained in isolation were unable to self-fertilize spawned eggs. All smaller individuals possessed characters typical of caridean males, including male gonopores, appendices masculinae, ejaculatory ducts, and cincinnuli on the first pleopods. However, the gonad of these male-phase (MP) individuals was an ovotestis with an undeveloped ovarian portion. FPs, which spawn eggs and incubate embryos, also had male gonopores and an ovotestis terminating in ejaculatory ducts containing sperm. In FPs, male pleopod characters were absent or reduced, and a female incubatory character, expanded pleopod flanges, showed a greater relative size. Smaller size classes of the population were composed only of MPs while larger size classes consisted of both MPs and FPs. “Transitionals,” individuals with MP characters but an ovotestis containing vitellogenic oocytes, were rare and overlapped completely in size with FP and larger MP individuals. It is suggested that not all MPs transform into FP hermaphrodites. Social interactions may mediate MP change into FP hermaphrodites in L. wurdemanni. The social system of L. wurdemanni and other Lysmata spp. may determine the exact form of the sexual system in these species. Received: 26 October 1997 / Accepted: 21 April 1998     

Sex ratios,mating behavior and sexual size dimorphism of the northern water snake,Nerodia sipedon

Competition among males to mate is generally associated with male-biased size dimorphism. In this study we examine mating behavior in the northern water snake (Nerodia sipedon), a species in which males are much smaller than females despite substantial competition among males to mate. Competition among males was a consequence of a male-biased operational sex ratio due to slightly higher female mortality from a birth sex ratio of 1 : 1, and, in 1 year, more synchronous and longer mating activity by males. Approximately one-third of both males and females appeared not to mate in a given year. Larger males were generally more likely to attempt mating, but size did not explain the variance in the number of aggregations in which individual males participated. Within aggregations, males that were successful at achieving intromission were larger than unsuccessful males in 1 of 2 years. Variation in condition (mass relative to length) and relative tail length were not generally useful predictors of either mating effort or success in males. Because large size was often advantageous to males, sexual size dimorphism appeared not to be a consequence of sexual selection favoring smaller males. Because sexual dimorphism was evident at birth, and both males and females matured sexually at about 4 years, sexual dimorphism was not simply a consequence of one sex growing at the maximum rate for longer. Female fecundity increased with size, and sex differences in size-fecundity relations may underly the pattern of sexual size dimorphism. However, because multiple mating by females is common, sperm competition is likely to be important in determining male reproductive success. Therefore, allocation of energy to sperm rather than growth may also prove to be an important influence on male growth rates and sexual size dimorphism.     

The role of body size in early mating behavior in a simultaneous hermaphrodite, <Emphasis Type="Italic">Chelidonura sandrana</Emphasis>

Intraspecific variation in mating behavior is widespread among simultaneous hermaphrodites but its underlying sources remain largely unexplored. In the sea slug Chelidonura sandrana, most matings are reciprocal. However, despite non-conditional sperm exchange and potential polygamy-mediated benefits, 30% of matings end after unilateral insemination. To resolve this apparent inconsistency, we here investigated the effect of body size on the frequency of reciprocal matings by testing the following two hypotheses. First, sex-allocation theory predicts that the likelihood of reciprocity depends on the size difference between mating partners. Second, if both sex functions temporally differ in reaching maturity, reciprocal matings should be more frequent with increasing absolute body size of the smaller partner. The likelihood of reciprocity increased with body size of the smaller partner. Moreover, smaller individuals acted more often as males among unilateral matings. These findings suggest that the ability to donate sperm develops prior to female functionality in C. sandrana.     

Hermaphrodite sex role preferences: the role of partner body size, mating history and female fitness in the sea slug Chelidonura sandrana

Costs and benefits associated with matings and the effects of mating frequency on fitness commonly differ between the sexes. As a result, outcrossing simultaneous hermaphrodites may prefer to copulate in the more rewarding sex role, generating conflicts over sperm donation and sperm receipt between mates. Because recent sex role preference models remain controversial, we contrast here some of their assumptions and predictions in the sea slug Chelidonura sandrana. For this hermaphrodite with sperm storage and internal fertilisation, risk-averse models assume that fitness pay-offs are constantly higher in the female than in the male function in any single mating. Moreover, excluding mutual partner assessment, these models predict male mating behaviour to be independent of receiver traits. The competing gender ratio hypothesis assumes that relative fitness pay-offs, and thus the preferred mating roles, vary and may reverse between matings and predicts that ejaculation strategies co-vary with receiver quality. We found that field mating rates of C. sandrana substantially exceeded what is required to maintain female fertility and fecundity, indicating large variation in direct female benefits between matings. We further demonstrate that male copulation duration adaptively increased with partner body size (i.e. fecundity) but decreased with recent partner promiscuity. These findings are compatible with the gender ratio hypothesis but contradict risk-averse models.     

Mating system of the hermaphroditic coral-reef fish,Serranus baldwini

Summary The lantern bass, Serranus baldwini, is a small hermaphroditic serranid found adjacent to coral reefs throughout the Caribbean. Data from gonad inspection, spawning behavior, and gamete release from individuals all confirm that populations consist of simultaneous hermaphrodites and males. This gender pattern appears to be sequential, with larger males derived from smaller hermaphrodites. The social system is haremic, with the male defending an area containing 1–7 hermaphrodites. The social system and gender pattern are similar to those of the eastern Pacific serranid, Serranus fasciatus. Males obtain disproportionately high mating success by being nearly the sole mates of hermaphrodites within their harems. Hermaphrodites obtain very low levels of mating success through male function. This pattern may result from female choice by hermaphrodites, mate sequestering tactics by males, or both. The serranids that change gender from hermaphrodite to male appear to have a higher environmental potential for polygyny than other simultaneous hermaphrodites in this family. Factors that may maintain male function in hermaphroditic S. baldwini are outlined, but none currently provides clear evidence for why this species has not evolved to protogyny.     

Gender-role alternation in the simultaneously hermaphroditic freshwater snail <Emphasis Type="Italic">Physa acuta</Emphasis>: not with the same partner

In simultaneous hermaphrodites, gender conflicts that arise from two potential mates sharing the same gender preference may be solved through conditional reciprocity (or gamete trading). Conditional reciprocity had initially been considered widespread, but recent studies suggest that its real occurrence may have been overestimated, possibly because most mating observations have been performed on isolated pairs of individuals. Some resulting patterns (e.g., non-random alternation of sexual roles) were indeed compatible with conditional reciprocity but could also have stemmed from the two partners independently executing their own mating strategy and being experimentally enforced to do so with the same partner. Non-random alternation of gender roles was recently documented in the simultaneously hermaphroditic freshwater snail Physa acuta. To distinguish between conditional and unconditional gender alternations, we observed copulations of individually marked snails reared at three contrasted densities. We showed that density affected the overall frequency of copulations during the first 2 days of the experiment with high-density boxes showing more copulations than low density boxes, but it did not affect gender alternation patterns. A change in gender role was observed more often than expected by chance over two successive copulations by the same individual, confirming previous studies. However, gender switches did not preferentially occur with the same partner. We conclude that gender alternation is not due to conditional reciprocity in P. acuta. It may rather stem from each individual having a preference for gender alternation. We finally discuss the mechanisms and the potential extent of this unconditional reciprocity.     

Allocation in reproduction is not tailored to the probable number of matings in common toad (<Emphasis Type="Italic">Bufo bufo</Emphasis>) males

The theory of life history evolution assumes trade-offs between competing fitness traits such as reproduction, somatic growth, and maintenance. One prediction of this theory is that if large individuals have a higher reproductive success, small/young individuals should invest less in reproduction and allocate more resources in growth than large/old individuals. We tested this prediction using the common toad (Bufo bufo), a species where mating success of males is positively related to their body size. We measured testes mass, soma mass, and sperm stock size in males of varying sizes that were either (1) re-hibernated at the start of the breeding season, (2) kept without females throughout the breeding season, or (3) repeatedly provided with gravid females. In the latter group, we also estimated fertilization success and readiness to re-mate. Contrary to our predictions, the relationship between testes mass and soma mass was isometric, sperm stock size relative to testes mass was unrelated to male size, fertilization success was not higher in matings with larger males, and smaller males were not less likely to engage in repeated matings than larger males. These results consistently suggest that smaller males did not invest less in reproduction to be able to allocate more in growth than larger males. Causes for this unexpected result may include relatively low year-to-year survival, unpredictable between-year variation in the strength of sexual selection and low return rates of lowered reproductive investment.     

Sex adjustments are not functionally costly in simultaneous hermaphrodites

Because of their double sex functions, hermaphrodites are selected to optimize their investment in the two sex functions. Sex allocation (SA) theory predicts that, in promiscuous mating conditions, simultaneous hermaphrodites should adjust their reproductive investment so as to invest an amount of resources into the male relatively larger than that invested into the female function. In contrast, in monogamy, individuals should invest relatively larger amount of resources into the female function at the expenses of the male function. In the study of SA patterns of simultaneous hermaphrodites little attention has been paid to allocate adjustments costs, which may play an important role in determining variations in SA pattern among species. Indeed, the costs paid for such adjustments may constrain sex investment resulting in suboptimal allocation. We evaluated the costs of SA adjustments on individual fitness in each sexual function in the simultaneous, outcrossing hermaphrodite Ophryotrocha diadema. Following a crossover design, we compared the reproductive success in paternal and maternal offspring of focal hermaphrodites, which were put in replicated monogamous and promiscuous regimes. We document that those hermaphrodites that switched mating regimes and altered their sex investment accordingly did not entail large short-term fitness costs in any sexual function compared to those that were in stable mating regimes. Indeed, individuals changed their sex investment quickly and appropriately to current mating conditions. Hermaphrodites, which had to adjust their SA, did not decrease their maternal or paternal reproductive output with respect to those which did not change their SA. Time needed to shift resources from one to the other sex function is 5 days (the time interval between successive egg layings is of 3 days) indicating that selective pressures for SA adjustments may favour great plasticity and quick adjustments of sex investments in simultaneous hermaphrodites.     

Sperm traits in the quacking frog (<Emphasis Type="Italic">Crinia georgiana</Emphasis>), a species with plastic alternative mating tactics

In species where males use alternative reproductive tactics and male phenotypes are confronted with different risks of sperm competition, theory predicts that between-male-type differences in sperm expenditure may evolve. In the frog Crinia georgiana big males can monopolize females, whereas small males often engage in polyandrous matings. Consequently, big males may experience a lower risk of sperm competition than do small males. We tested if the predictions from theoretical models can be applied to the mating system of C. georgiana. Our results showed that small males do not have larger testes relative to their body size compared to their larger counterparts and that the efficiency with which sperm number, size, motility, and longevity are produced by the testes does not differ between small and large males in the predicted way. These results are not in alignment with predictions from a loaded raffle model of sperm competition on sperm expenditure in males with alternative phenotypes. The plasticity in mating tactics used by C. georgiana males and a high intraseasonal variation in male densities may have prevented the evolution of enhanced sperm performance in smaller males. A fair raffle in the sperm competition game played by C. georgiana males could also explain the observed patterns in sperm traits. Future investigations determining the parameters responsible for the deviation from theoretical predictions in this system will test the degree to which current theoretical models can indeed be applied to species with plastic reproductive tactics.     

Body size preferences in the pot-bellied seahorse <Emphasis Type="Italic">Hippocampus abdominalis:</Emphasis> choosy males and indiscriminate females

Male seahorses (genus Hippocampus) provide all post-fertilization parental care, yet despite high levels of paternal investment, these species have long been thought to have conventional sex roles, with female mate choice and male–male competition. Recent studies of the pot-bellied seahorse (Hippocampus abdominalis) have shown that sex-role reversal occurs in high-density female-biased populations, indicating that male mating preferences may lead to sexual selection on females in this species. Egg size, egg number, and offspring size all correlate positively with female body size in Hippocampus, and by choosing large mating partners, male seahorses may increase their reproductive success. While male brood size is also positively correlated with body size, small H. abdominalis males can carry exceptionally large broods, suggesting that the fecundity benefits of female preference for large partners may be limited. We investigated the importance of body size in reproductive decisions of H. abdominalis, presenting focal individuals of both sexes with potential mating partners of different sizes. Mating preferences were quantified in terms of time spent courting each potential partner. Male seahorses were highly active throughout the mate-choice trials and showed a clear behavioral preference for large partners, while females showed significantly lower levels of activity and equivocal mating preferences. The strong male preferences for large females demonstrated here suggest that sexual selection may act strongly on female body size in wild populations of H. abdominalis, consistent with predictions on the importance of female body size for reproductive output in this species. An erratum to this article can be found at     

Population density and the intensity of sexual selection on body length in spatially or temporally restricted natural populations of a seed bug

Summary Population density affects the dynamics of mate acquisition and the opportunity for sexual selection in natural populations of the seed bug, Neacoryphus bicrucis Say (Hemiptera : Lygaeidae). The opportunity for sexual selection and the intensity of directional sexual selection on body length increased as the population density declined within a season for a population in a small, disjunct patch of host plant, Senecio anonymus. In a larger, dispersed population, both measures of selection were greater in host plant patches of low rather than high adult density when the population was sampled at peak density. Under conditions of higher density, males were more likely to share plants, larger males were less likely to monopolize patches of host plant to which females were attracted for mating, and smaller males were more likely to mate in the presence of large males. Thus, resource defense polygyny collapsed under high density, obviating the advantage of size in territory control, and resulted in scramble competition among males for mates. The population exhibited significant additive genetic variation for body length. This suggests that natural selection acting on other components of fitness favors smaller size or that the direction of sexual selection on size fluctuates between generations in response to the between-year variation in population density. Thus, strong sexual selection appears to impose a significant genetic load.     

Mate with the young, kill the old: reversed sexual cannibalism and male mate choice in the spider Micaria sociabilis (Araneae: Gnaphosidae)

Female mate choice is regarded as a strong selective force that significantly affects male mating success. In extreme cases, mate rejection can result in sexual cannibalism. However, males may choose between their partners as well. The killing of potential female mates, i.e. reversed form of sexual cannibalism, may be related to male mate choice. We examined male mate choice in the spider Micaria sociabilis, focusing on the roles of female mating status (virgin/mated), size and age. Reversed cannibalism reached its highest frequency in the period of generation overlap, i.e. when young males from the summer generation met old(er) females from the spring generation. These results suggest discrimination against old(er) females. The frequency of cannibalism was not affected by female mating status or female size. However, larger males from the summer generation were more cannibalistic than smaller males from the spring generation. We conclude that reversed sexual cannibalism might be an adaptive mate choice mechanism and can be explained in the context of the aggressive spillover hypothesis.     

Sexual selection and the function of a melanin-based plumage ornament in polygamous penduline tits <Emphasis Type="Italic">Remiz pendulinus</Emphasis>

Melanin-based ornaments are often involved in signaling aggression and dominance, and their role in sexual selection is increasingly recognized. We investigated the functions of a melanin-based plumage ornament (facial ‘mask’) in male Eurasian penduline tits Remiz pendulinus in the contexts of male–male aggression, mating success, and parental care. The penduline tit is a passerine bird with a unique mating system in which both sexes may mate with several mates in a breeding season, and one (or both) parent deserts the clutch. Our study revealed that mask size of males is more likely an honest signal used by females in their mate choice decisions than a trait involved in male–male competition. First, mask size increased with both age and body condition, indicating that the mask may signal male quality. Second, males with larger masks paired more quickly and had more mates over the breeding season than males with smaller masks. Third, we found no evidence that male mask size signals male–male aggression or dominance during competitive encounters. The increased mating success of large-masked males, however, did not translate into higher reproductive success, as nestling survival decreased with mask size. Therefore, we conclude that there is either no directional selection on male mask size or males with larger masks receive indirect, long-term benefits.     

The effects of mating system on male mate choice in a coral reef fish

Summary We show how mate limitation appears to be critical in determining whether or not males exercise mate choice among available females. Thalassoma bifasciatum is a Caribbean reef fish with two distinct mating patterns: group-spawning and pair-spawning. In both mating systems, female fecundity is variable and size dependent, and female availability is high. However, sperm competition among group-spawning males apparently limits the number of effective matings in which a male may engage, whereas territorial pair-spawning males have little or no such limitation. Group-spawning males should be discriminating in their choice of mates and our data confirm this: there is strong evidence for assortative mating in group-spawns, with more large males joining in mating groups around large females. In contrast, pair-spawning males show no indication of mate preferences, and spawn with all females who arrive at their territories.     

Effects of frequent mating on sex allocation in the simultaneously hermaphroditic great pond snail (Lymnaea stagnalis)

Simultaneous hermaphrodites have the opportunity to control the allocation of resources to the male and female function depending on the circumstances. Such flexibility also provides the possibility to influence sex allocation in the mating partner. To investigate this idea, we measured egg production (female investment) and sperm production as well as prostate gland size (both are part of male investment) under different mating regimes in the great pond snail Lymnaea stagnalis. We find no evidence for the prediction from sex allocation theory that sperm production increases with mating frequency. However, we do find that animals with more mating opporunities develop smaller prostate glands, in which seminal fluid is produced. Moreover, repeated mating increases egg production, thus shifting allocation towards the female function, and probably decreases growth. So, our data hint at a three-way trade-off between part of the male function (prostate gland), female function, and growth. Interestingly, sex allocation seems to be shifted in the opposite direction from the one predicted by theory. We discuss how this feminization is suggestive of a direct manipulation by the sperm donor, probably to stimulate immediate sperm use.     

Male mating opportunities affect sex allocation in a protrandric-simultaneous hermaphroditic shrimp

Sex allocation theory predicts phenotypic adjustments by individuals in their investments into the male and female reproductive function in response to environmental conditions. I tested for phenotypically plastic shifts in sex allocation in a protandric simultaneous hermaphrodite, in which individuals mature and reproduce as males first, and later in life, as simultaneous hermaphrodites. I predicted that initially maturing males should adjust the timing of maturation as hermaphrodites according to male mating opportunities mediated by population size of hermaphrodites. In a first experiment, males maintained with only one hermaphrodite reduced the time they spent as males in comparison to males maintained with no conspecifics, presumably because total reproductive output is maximized by two individuals being simultaneous hermaphrodites when the mating system is a pair. Conversely, males maintained in groups with two or more hermaphrodites increased the time they spent as males in comparison to single males. This delay in maturation was not an effect of resource depletion with increasing shrimp density because the growth rate of males did not differ among most of the experimental treatments. One hypothesis to explain this social mediation of sex allocation is that the smaller males are more successful in mating as males than are the larger hermaphrodites: it will pay reproductively for males to delay maturation as hermaphrodites in large but not in small groups. In agreement with this notion, a second experiment demonstrated that smaller males were four times more successful than were larger hermaphrodites in inseminating shrimps reproducing as females. The informative cue that males may use to perceive different group sizes deserves further attention.     

Male dimorphism, sperm traits and immunology in the corkwing wrasse (Symphodus melops L.)

The evolution of alternative male mating phenotypes inevitably involves variation in risk or intensity of sperm competition. Males that typically mate in disfavoured roles (i.e. sneakers/parasitic males) are predicted to experience higher magnitudes of sperm competition than males mating in favoured roles (preferred by females/exhibiting mate monopolisation). Here, we investigated whether two distinct male phenotypes in corkwing wrasse (Symphodus melops) differ with respect to adaptations for sperm competition in terms of sperm quantity, sperm motility and fertilising capacity. We found that males exhibiting female mimicry (disfavoured role) had both absolutely and relatively larger gonads than males with typical secondary sexual characters (favoured role). Moreover, a higher proportion of sperm from female mimics was motile 5 min after activation compared to sperm of territorial males. There were, however, no differences in sperm concentration or in in vitro fertilisation ability between the two male morphs. We also examined whether the male phenotypes differed in some immune parameters and if any such variation is associated with sperm traits. Current theories predict that ejaculate quality should be negatively correlated with the level of immunocompetence. Territorial males had relatively heavier spleens than female mimics, but whether this reflects differing immunocompetence is uncertain, since the spleen is also an important organ for erythrocyte storage. Furthermore, there were no differences in the densities of circulating lymphocytes or granulocytes, and the immune parameters did not covary with the sperm traits. Differences in immunocompetence are therefore unlikely to provide a major proximate explanation for variations in sperm traits in corkwing wrasse.     

Analysis of the causal components of assortative mating in water striders

Field studies demonstrate that natural populations of a group of water striders (Heteroptera: Gerridae) that share a common mating system are characterized by weak assortative mating by size and by large sizes of mating males and females relative to single individuals. This study presents an experimental assessment of the components of mating that may contribute to these mating patterns. The effects of male and female body size on each of three components of mating were studied in three water strider species in the laboratory. Large females of all three species mated more frequently, copulated for longer and were guarded longer than small females. Large males mated more frequently than small males in all three species, and also guarded females for longer in the two species where the average of mate guarding was long. However, we found an antagonistic effect of male size on copulation duration: small males copulated for longer than large males in all three species. We show that the combined effects of these size biases mimic the mating patterns found in the wild, e.g. weak and variable assortative mating, and stronger and less variable size ratios of mating versus non-mating females relative to males. We suggest that the antagonistic effects of male size on copulation and guarding duration may be a key source of interpopulational variation in assortative mating and sexual selection on male size. Further, neither spatial or temporal covariation in size, nor mechanical constraints, caused the assortative mating observed here in this group of water striders. Some combination of male and female choice (either active or passive forms) of large mates and male-male exploitation competition for mates play potentially important roles in producing population level assortative mating in water striders. Received: 17 March 1995/Accepted after revision: 28 October 1995