Influence of alternate reproductive tactics and pre- and postcopulatory sexual selection on paternity and offspring performance in a lizard

Sexual selection theory predicts different optima for multiple mating in males and females. We used mating experiments and genetic paternity testing to disentangle pre- and postcopulatory mechanisms of sexual selection and alternate reproductive tactics in the highly promiscuous lizard Eulamprus heatwolei. Both sexes mated multiply: 30–60 % of clutches were sired by two to four fathers, depending on the experiment. Larger males sired more offspring when we allowed male contest competition: 52 % of large males but only 14 % of small males sired at least one offspring. In the absence of male contest competition, females mated promiscuously and there was no large male advantage: 80 % of large males and 90 % of small males sired at least one offspring, and there was no evidence for last-male precedence. Multiple mating did not yield obvious direct or indirect benefits to females. E. heatwolei represents a complex system in which males attempt to improve their fertility success by limiting rivals from access to females and through adopting alternate reproductive tactics. Conversely, females exhibit no obvious precopulatory mate choice but may influence fitness through postcopulatory means by either promoting sperm competition or through cryptic female choice. Our results support the hypothesis that female multiple mating in nonavian reptiles is best explained by the combined effect of mate encounter frequency and high benefits to males but low costs to females.     

Factors affecting male and female reproductive success in a chipmunk (Tamias sibiricus) with a scramble competition mating system

While sexual selection in mammals with female defense systems has historically received considerable attention, much less is known about the factors affecting reproductive success in mammalian species with scramble competition mating systems. Using mark–recapture techniques and DNA microsatellite loci to assign parentage, we examined the mating system and factors affecting the variation of the annual reproductive success in an introduced population of the Siberian chipmunk, Tamias sibiricus, a small, monomorphic, solitary squirrel. Our analyses showed that breeding females were spatially dispersed, setting the stage for a scramble competition mating system. Male reproductive success was positively associated with the size of the home range. The strength of sexual selection on this behavioral trait was very strong, equaling previous estimates for morphological traits in female defense mating systems. These findings suggest that a behavioral trait, space use, strongly influences the annual reproductive success in males, which is consistent with expectations in a scramble competition mating system. In both sexes, reproductive success was influenced by habitat, with twice as many juveniles produced in semi-open than in closed habitat, possibly due to differences in food availability between the two habitats.     

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     

Natal dispersal in two mice species with contrasting social systems

We compared the natal dispersal behaviour of two mice species under laboratory conditions. Natal dispersal is a movement of an animal from its birthplace to its breeding area. This behaviour is known to be influenced by the mating system. In polygamous species, males are more likely to disperse, while in most of the monogamous species, both sexes disperse. Our subjects, the house mouse (Mus musculus) and the mound-building mouse (Mus spicilegus) are two sympatric species of the genus Mus. Both are native in Hungary, but they differ in their habitat type mating system and overwintering strategy. The house mouse is a polygynous species and adapted to human environment, known for mature and reproduce early. On the contrary, the mound-building mice are monogamous, and they inhabit extensively used agricultural fields, where they spend the unfavourable winter period in nest chambers under mounds, which they construct from soil and plant material. Successful overwintering for this species demands delayed maturity and reduced dispersion during the winter. Our results showed that the natal dispersal of these two species differ; both sexes of the mound-building mice dispersed later than the house mice, where a difference between sexes also occurs; house mice males dispersed earlier than females. The mound-building mice showed no sexual dimorphism in this behaviour.     

Intersexual dominance relationships and the influence of leverage on the outcome of conflicts in wild bonobos (Pan paniscus)

Dominance relationships between females and males are characteristic traits of species and are usually associated with sexual dimorphism. Exploring the social and contextual circumstances in which females win conflicts against males allows one to study the conditions triggering shifting power asymmetries between the sexes. This study investigates dominance relationships in bonobos (Pan paniscus), a species in which females are thought to display social dominance despite male-biased sexual dimorphism. To identify dominance relationships among females and males, we first explored how intrasexual dominance status affects the outcome of intersexual conflicts. Second, by incorporating social and behavioral information about the context of intersexual conflicts, we tested to which extent different components of power are relevant to the observed asymmetries in the relationships. Post-hoc analyses indicate a sex-independent dominance hierarchy with several females occupying the top ranks. Our results also reveal that two factors—female leverage and motivation to help offspring—had a significant influence on the outcome of intersexual conflicts. The results of our study do not indicate an overall reduction in male aggression against females but do show lower levels of male aggression in the mating context, and an absence of male aggression toward those females displaying visual signs of elevated fecundity. This indicates that both female sexuality and male mating strategies are involved in the shifting dominance relationships between the sexes.     

Rhythmic male reproductive behavior controls timing of courtship and mating in Laupala cerasina

In many organisms, mating behavior occurs at a particular time of day, which may be important for avoiding mate competition or interspecific mating. Crickets of the Hawaiian genus Laupala exhibit an unusually protracted courtship in which males produce a series of nuptial gifts prior to the species-typical time of mating. Mating time is one of several rhythmic behaviors that have diverged among closely related Laupala species, which exhibit an extremely high speciation rate. Mating rhythm may reflect direct selection on male and/or female sexual receptivity or the pleiotropic consequence of selection on other rhythmic behaviors. To examine the role of sexual rhythmicity in Laupala cerasina, we characterized the time boundaries or “circadian gate” of courtship and mating, as well as female phonotactic response to male song. We also examined which sex is responsible for mating rhythmicity by phase-shifting males relative to the female photophase. Our results demonstrate that mating behavior is gated by the end of the light phase. Time limits to female mating receptivity were not observed and thus male rhythm alone appears to be responsible for the timing of mating. Furthermore, when courtship is initiated later in the day, males produce fewer nuptial gifts and increase nuptial gift production rate while delaying mating, suggesting that the number of gifts a female receives is important to male reproductive success.     

Is sexual monomorphism a predictor of polygynandry? Evidence from a social mammal, the collared peccary

Sexual dimorphism is common in polygynous species, and there is clear evidence that both intra-sexual competition and female preferences can drive the evolution of large body size in males. In contrast, sexual monomorphism is often argued to reflect a relaxation of male mate competition or an intensification of resource competition among females. Alternatively, it might imply opportunities for females to circumvent or counteract male mate competition in a polygynandrous mating system. We test the prediction that sexual monorphism is associated with polygynandry in the collared peccary (Pecari tajacu, Tayassuidae), a social ungulate closely related to the old-world suids. The genetic mating system in the Tayassuidae is unknown, but its sexual monomorphism presents a striking contrast to the strong size dimorphism found in most Suidae, so that a departure from the polygynous system common in Suidae would be noteworthy. We characterized genetic relationships among adults within herds in three geographically distinct populations, assigned parents to 75 offspring, and tested for skew in individual reproductive success. Parentage assignment data indicated that multiple males sire offspring within a herd, and in the population for which genetic data were most complete, 19% of parentage assignments were potentially sired by extra-herd males. Some litters have multiple sires, and neither males nor females monopolized reproduction, even in small herds. This result supports our prediction and suggests that sexual monomorphism may either select for or be an evolutionary consequence of a promiscuous mating system.     

Male choice,fighting ability,assortative mating and the intensity of sexual selection in the milkweed longhorn beetle,Tetraopes tetraophthalmus (Coleoptera,Cerambycidae)

Summary Over five hundred adult longhorn milkweed beetles, Tetraopes tetraophthalmus, were individually marked and their copulatory success followed for one month in a pasture of Asclepias syriaca in northern Indiana, USA. Migration of beetles from the field site was greatest from areas of low population density. Dispersal was significantly greater for males experiencing low copulatory success; a similar but nonsignificant trend was observed for females. Large males, which displayed greater site tenacity than small males, copulated more frequently than small males because of their ability to displace small males from females. Both large and small males demonstrated a preference for large females in laboratory tests. Male preference in combination with aggressive displacement of small males results in size-assortative mating which was much stronger under conditions of high population density. It contributes to variance in male reproductive success since female size is known to be correlated with fecundity and offspring viability. Variance in copulatory success is similar for males and females, suggesting that both sexes experience similar intensities of sexual selection with respect to this component of reproductive success. Futhermore, comparison of this with other studies suggests that the intensity of sexual selection among males is positively correlated with the variance in body size which appears to be under both stabilizing and directional sexual selection in males but not in females.     

Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations

Spermatozoa vary greatly in size and shape among species across the animal kingdom. Postcopulatory sexual selection is thought to be the major evolutionary force driving this diversity. In contrast, less is known about how sperm size varies among populations of the same species. Here, we investigate geographic variation in sperm size in barn swallows Hirundo rustica, a socially monogamous passerine with a wide Holarctic breeding distribution. We included samples from seven populations and three subspecies: five populations of ssp. rustica in Europe (Czech, Italy, Norway, Spain, and Ukraine), one population of ssp. transitiva in Israel, and one population of ssp. erythrogaster in Canada. All sperm traits (head length, midpiece length, tail length, and total length) varied significantly among populations. The variation among the European rustica populations was much lower than the differences among subspecies, indicating that sperm traits reflect phylogenetic distance. We also performed a test of the relationship between the coefficient of between-male variation in total sperm length and extrapair paternity levels across different populations within a species. Recent studies have found a strong negative relationship between sperm size variation and extrapair paternity among species. Here, we show a similar negative relationship among six barn swallow populations, which suggests that the variance in male sperm length in a population is shaped by the strength of stabilizing postcopulatory sexual selection.     

Mate choice,fecundity and sexual dimorphism in two pipefish species (Syngnathidae)

Summary In order to understand the causes of sexual dimorphism, mate choice and size-related fecundity were studied in two pipefish species, Syngnathus typhle and Nerophis ophidion. Sexual dimorphism is more pronounced in N. ophidion; females are larger, have sexual colourings, and are more active during courtship. In S. typhle the sexes are alike in all these respects. Males brood their offspring in both species. In N. ophidion fecundity was positively correlated with both body size and the amount of sexual colouring in females. In males no correlation between body size and fecundity, or between body size and embryo size existed. Predictably, in mate choice experiments with equal-sized females, males chose females with more extensive sexual colourings. We explain sexual dimorphism in this species as a consequence of both natural selection (fecundity increases with size in females but not in males) and sexual selection (males prefer larger females). We argue that sexual size dimorphism did not evolve by selection minimizing overlap in food niches between the sexes, because food production is high in the Zostera beds where the fishes live, and no size dimorphism was found in the sympatrically occurring S. typhle. Furthermore, in N. ophidion dimorphism is not greater in a particular mouth character than in overall body size. In S. typhle egg size and the average number of eggs transferred per spawning were positively correlated with female body size. Apparently more energy per offspring was provided by larger males than by smaller males, and larger males also carried more offspring. As predicted, large mates were preferred by both sexes in mate choice experiments. This is explicable in terms of both natural selection (fecundity increases with size in both sexes) and sexual selection (both sexes prefer large mates). As a consequence of selection acting in the same direction in both sexes, sexual dimorphism is absent in S. typhle.     

Does promiscuous mating preclude female choice? Female sexual strategies in chimpanzees (Pan troglodytes verus) of the Taï National Park, Côte d’Ivoire

According to sexual selection theory, females should selectively mate with high-quality males to enhance offspring survival and maximize reproductive success. Yet, chimpanzee (Pan troglodytes) females are known to mate promiscuously. Although there is substantial rationale for a promiscuous mating strategy, there is also a strong expectation that females should be selective, and the question arises as to whether promiscuity precludes female choice. The aims of this study are to: (1) compare wild female chimpanzee sexual strategies throughout estrus, and (2) determine whether females exhibit mate preferences for particular males. Over 2,600 h of data were collected on two habituated chimpanzee (Pan troglodytes verus) communities in the Taï National Park, Côte dIvoire. Female mate preferences were measured by quantifying proceptivity and receptivity toward males. Results indicate that all females exhibited proceptivity and resistance to male solicitations, but that there was substantial variation in their magnitudes within and among females. Female proceptivity rates were lower and resistance rates were higher in the periovulatory period (POP) when conception is most likely. Females were more selective during POP, and more promiscuous outside of POP, suggesting that females may follow a mixed reproductive strategy, being selective when conception is likely and more promiscuous when conception is unlikely. Results from this study emphasize the importance of considering the fertility window when determining female mate preferences, and of examining female behavior in POP and non-POP phases separately when evaluating hypotheses for multi-male mating.Communicated by C. Nunn     

Nest distribution affects behaviour and mating success in a marine fish

The distribution of breeding resources, such as nest sites, can have a pronounced impact on a population by affecting the proportion of individuals that succeed to breed and hence, the variation in reproductive success. Aggregation of important resources can lead to resource monopolisation by a limited number of individuals and thus affect the intensity of sexual selection. In this study, we tested, by contrasting two experimental treatments (dispersed vs. aggregated), how nest distribution affects: (1) mating behaviour, (2) male nest occupation and mating success, and (3) reproductive success and the opportunity for selection. We used the two-spotted goby (Gobiusculus flavescens), a small marine fish with a resource-based mating system, as our model species. When nests were aggregated, a larger proportion of the males behaved aggressively, fewer males succeeded in occupying a nest, fewer males became mated, and those males that mated received fewer eggs from spawning females. These effects resulted in a higher variance in reproductive success and hence, a higher opportunity for selection (I _rs ), in the aggregated treatment. We suggest that the results are a direct consequence of males defending a territory around their nest, preventing competitively inferior males from breeding. However, we found no significant selection differentials for body length or condition of males in either treatment. Our results support the hypothesis that aggregation of essential resources like nests promotes resource monopolisation. In species facing highly clumped nesting resources in the wild, monopolisation may negatively impact population productivity but could lead to strong selection on traits that promote male competitive ability.     

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.     

The genetic mating system of a sea spider with male-biased sexual size dimorphism: evidence for paternity skew despite random mating success

Male-biased size dimorphism is usually expected to evolve in taxa with intense male–male competition for mates, and it is hence associated with high variances in male mating success. Most species of pycnogonid sea spiders exhibit female-biased size dimorphism, and are notable among arthropods for having exclusive male parental care of embryos. Relatively little, however, is known about their natural history, breeding ecology, and mating systems. Here we first show that Ammothella biunguiculata, a small intertidal sea spider, exhibits male-biased size dimorphism. Moreover, we combine genetic parentage analysis with quantitative measures of sexual selection to show that male body size does not appear to be under directional selection. Simulations of random mating revealed that mate acquisition in this species is largely driven by chance factors, although actual paternity success is likely non-randomly distributed. Finally, the opportunity for sexual selection (I _s), an indirect metric for the potential strength of sexual selection, in A. biunguiculata males was less than half of that estimated in a sea spider with female-biased size dimorphism, suggesting the direction of size dimorphism may not be a reliable predictor of the intensity of sexual selection in this group. We highlight the suitability of pycnogonids as model systems for addressing questions relating parental investment and sexual selection, as well as the current lack of basic information on their natural history and breeding ecology.     

Sex-specific conditional mating preferences in a cichlid fish: implications for sexual conflict

Conditional mating strategies enable individuals to modulate their mating behaviour depending on ‘individual status’ to maximise fitness. Theory predicts that variation in individual quality can lead to differences in mating preferences. However, empirical evidence is scarce particular in terms of variation in male and female strategies. Here, we experimentally investigated quality-dependent variation in mating preferences concerning reliable quality indicators in Pelvicachromis taeniatus, a colourful cichlid fish with mutual mate choice and ornamentation. Males as well as females were artificially manipulated in phenotypic quality by different feeding regimes. Ornamentation was connected to individual quality in both sexes. Males and females showed conditional mating strategies in different directions. Males showed prudent choice by preferring females of similar quality. In contrast to males, low-quality females preferred highly ornamented males, whereas high-quality females showed neither preferences for high- nor for low-quality males. The results suggest that individuals aim for specific benefits depending on individual quality. Furthermore, the conflicting conditional mating preferences of males and females might lead to sexual conflict, implicating a highly dynamical mating system that evolves even in absence of environmental changes.     

Pre-copulatory sexual selection in the cigarette beetle Lasioderma serricorne

Traditional concepts of sexual selection and sexual conflict make different predictions about the costs and benefits to females of exposure to males with higher mating success. The traditional concepts of sexual selection assume that females benefit from their mate choices, whereas sexual conflict assumes that the females suffer greater costs by mating with males who have greater mating success and thus reduce their fitness. In order to understand how mate choice evolves, it is necessary to estimate the overall effect of mate choice on female fitness. However, relatively few studies have conducted that investigation. In this study, we investigated the direct and indirect effects of mating with attractive males on the fitness of females in the cigarette beetle Lasioderma serricorne. Mating with attractive males increased the number of female offspring but did not affect female longevity. Additionally, we found evidence that attractive males sire highly attractive sons. Thus, mating with an attractive male provides direct and indirect benefits but no fitness cost to female L. serricorne.     

Parental investment, potential reproductive rates, and mating system in the strawberry dart-poison frog, Dendrobates pumilio

We studied the effect of relative parental investment on potential reproductive rates (PRRs) to explain sex differences in selectivity and competition in the dart-poison frog Dendrobates pumilio. We recorded the reproductive behavior of this species in a Costa Rican lowland rainforest for almost 6 months. Females spent more time on parental care than males, and `time out' estimates suggest that PRRs of males are much higher than than those of females, rendering females the limiting sex in the mating process. Males defended territories that provide suitable calling sites, space for courtship and oviposition, and prevent interference by competitors. Male mating success was highly variable, from 0 to 12 matings, and was significantly correlated with calling activity and average perch height, but was independent of body size and weight. Estimates of opportunity for sexual selection and variation in male mating success are given. The mating system is polygamous: males and females mated several times with different mates. Females were more selective than males and may sample males between matings. The discrepancy in PRRs between the sexes due to differences in parental investment and the prolonged breeding season is sufficient to explain the observed mating pattern i.e., selective females, high variance in male mating success, and the considerable opportunity for sexual selection. Received: 9 June 1998 / Received in revised form: 27 March 1999 / Accepted: 3 April 1999     

The genetic mating system of a sex-role-reversed pipefish (Syngnathus typhle): a molecular inquiry

In the pipefish Syngnathus typhle as in other species of Syngnathidae, developing embryos are reared on the male's ventral surface. Although much laboratory research has been directed toward understanding sexual selection in this sex-role-reversed species, few studies have addressed the mating behavior of S. typhle in the wild, and none has capitalized upon the power of molecular genetic assays. Here we present the first direct assessment of the genetic mating system of S. typhle in nature. Novel microsatellite loci were cloned and characterized from this species, and employed to assay entire broods from 30 pregnant, field-captured males. Genetic analysis of 1340 embryos revealed that 1–6 females (mean = 3.1) contributed to each brooded clutch, the highest rate of multiple maternity yet documented in any pipefish. Evidence of multiple mating by females was also detected. Thus, this population of S. typhle displays a polygynandrous mating system, a finding consistent with previous field and laboratory observations. Our results, considered together with similar studies of other syngnathid species, provide preliminary support for the hypothesis that the genetic mating system is related to the evolution of sexual dimorphism in the fish family Syngnathidae. Received: 19 January 1999 / Received in revised form: 15 April 1999 / Accepted: 9 May 1999     

Mate choice among sympatric fur seals: female preference for conphenotypic males

When closely related species breed in sympatry, and where hybrids have lower fitness, reinforcement theory predicts that selection should favour mechanisms that reduce the probability of interspecific matings. If this situation arises among species that exhibit resource defence polygyny where males and females of different species reside in the same territories, there may be some conflict between mate choice based on territory-holding ability (sexual selection) and mate choice for correct species. We investigated this in a population of fur seals where three species are sympatric and where some females breed in the territories of heterospecific males, and where interspecific matings and hybrid pups are observed. The territorial status of males and the birthing sites of females were determined during daily observations, as were the movements of males and females, the location of matings and mating partners. DNA extracted from skin samples was used to determine paternities using DNA fingerprinting and the mtDNA genotype of individuals. Individuals were also classed on the basis of species-typical phenotype. We found that extra-territory inseminations (ETIs) were significantly more prevalent (67%) when territorial males and resident females were of different phenotype than when of similar phenotype (27%), but mtDNA genotype had no effect on the rate of ETIs. ETIs were probably by males with the same phenotype, as pups born to these females in the following season had the same phenotype as their mothers, suggesting they were not hybrids. These results suggest that within the resource defence polygynous mating system of these sympatric fur seals, female mate choice is more influenced by male phenotype than genotype. Contrary to our predictions, our study indicates that potential conflict between mate choice based on sexual selection and species recognition is unlikely, because females have some capacity to discriminate between males both within and between species on phenotypic traits additional to those under sexual selection. Although at least 25% of the pups born in this study were hybrid, this study can only support reinforcement theory if hybrids have reduced fitness. The fitness of hybrids among the species studied is currently unknown. Received: 19 January 1998 / Accepted after revision: 12 September 1998     

Cooperatively breeding superb fairy-wrens show no facultative manipulation of offspring sex ratio despite plausible benefits

We report a long-term study of offspring sex ratios in the cooperatively breeding superb fairy-wren Malurus cyaneus. Detailed study of this species had revealed a suite of potentially strong selection pressures on the sex ratio. First, females gain substantial fitness benefits from the presence of helpers; so females without male helpers would benefit from any strategy that increased the probability of recruiting help, such as overproduction of sons (local resource enhancement hypothesis), but large numbers of helper males compete among themselves, favouring the production of daughters (local resource competition). Second, daughters fledged early in the season have far greater chances of recruitment to the breeding population than late-fledged daughters, so mothers would benefit from production of daughters early in the breeding season (early bird hypothesis). Third, extra-group mate choice imposes strong sexual selection on males, suggesting that females mating with attractive sires could benefit from investing in sons (sexual selection hypothesis). However, the predictions from these and other sex ratio hypotheses were rejected. The only convincing evidence for manipulation of the sex ratio was a slight bias towards sons (11 sons to 10 daughters) that occurred regardless of context. This result does not support current theory.