Male genital morphology influences paternity success in the millipede <Emphasis Type="Italic">Antichiropus variabilis</Emphasis>

The genitalia of internally fertilizing animals are among the most diverse of all sexual characters. It is currently argued that genitalia evolve rapidly and divergently due to intense post-copulatory sexual selection. If true, male genital morphology should be subject to directional selection, whereby males with particular genital morphologies achieve greater paternity success. There is mounting evidence that male genital morphology can influence competitive fertilization success; however, the form of selection acting on genitalia has rarely been explored. We conducted competitive fertilization experiments using Antichiropus variabilis millipedes. Using microsatellite loci, we determined the paternity of offspring following double matings. The last male to mate had a significant paternity advantage. While no aspect of the behavior of last males was correlated with paternity success, variation in genital morphology did account for variation in last male paternity. Male genitalia were subject to nonlinear selection, with both convex (stabilizing) selection and concave (disruptive) selection acting on genital shape. This is the first study to provide evidence for sperm precedence in a millipede and only the second to document the form of post-copulatory sexual selection operating on male genital morphology. We discuss the implications of our results for the evolution of genitalia in A. variabilis and, more broadly, how our findings relate to alternative theories of genital evolution.     

Is the bat os penis sexually selected?

. The mammalian os penis or baculum is an extremely diverse bone but our understanding of the selective forces behind this diversity remains poor. While genital morphology is generally assumed to be sexually selected, there have been relatively few attempts to test this hypothesis. Here we investigate associations between baculum length and two measures of sexual selection intensity (mating system and testis mass) across bats. Analyses were conducted using both species-level data and phylogenetic comparative techniques. Controlling for the effect of male body mass, baculum length was positively associated with relative testis mass in all cross-species analyses. Additionally, in an analysis that also included mating system, there was an interaction between testis mass, body mass and mating system that significantly influenced baculum length. However, after using independent contrasts to control for phylogenetic inertia in these data, baculum length was not significantly associated with mating system, testis mass or body mass. Thus, increased length of the baculum in bats appears not to be associated with increased sperm competition risk or sexual selection intensity.     

Do female bank voles (Clethrionomys glareolus) mate multiply to improve on previous mates?

Contrary to classical sexual selection theories, females of many taxa mate with multiple males during one reproductive cycle. In this study, we conducted an experiment on the “trade-up hypothesis”, which proposes that females remate if a subsequently encountered male is potentially superior to previous mates to maximize the genetic quality of their offspring. We presented bank vole females (Clethrionomys glareolus) sequentially with two males of known dominance rank in different orders, i.e., either first subordinate and second dominant, first dominant and second subordinate, or two males that were equal in dominance (high ranking) and observed their mating behavior. We found that 92% of the females mated multiply and did not base their remating decision on male social status. Therefore, polyandry cannot be explained by the “trade-up hypothesis” based on dominance rank in this species. However, we found that dominant males sired significantly more offspring than subordinate males. This varied according to mating order: dominant males sired more offspring when they were second than when they were first. Moreover, litter sizes were significantly smaller when the dominant male was first (smallest relative success of dominant males) compared to litter sizes when mating order was reversed or both males equal in status. Our results suggest that even though multimale mating includes males that are of poorer quality and thus potentially decreases the fitness of offspring, most of a female’s offspring are sired by dominant males. Whether this is due to cryptic female choice, sperm competition, or a combination of both, remains to be tested.     

The lemur syndrome unresolved: extreme male reproductive skew in sifakas (<Emphasis Type="Italic">Propithecus verreauxi</Emphasis>), a sexually monomorphic primate with female dominance

The primates of Madagascar (Lemuriformes) are unusual among mammals in that polygynous species lack sexual dimorphism, and females dominate males socially in most species. Moreover, lemur groups are relatively small and characterized by even adult sex ratios despite the fact that one male should be able to exclude other males from the group. One hypothesis to explain this combination of behavioral, morphological, and demographic traits (the “lemur syndrome”) postulates that male–male competition is relaxed and, hence, variance in male reproductive success is low. Reproductive skew theory provides a framework for testing this and several related predictions about lemur social evolution. Specifically, low reproductive skew is also predicted if dominant males or adult females make reproductive concessions to subordinates or if the latter group successfully pursues alternative reproductive tactics. However, suitable data on paternity, demography, and behavior for a conclusive test of these predictions have not been available in the past. In this paper, we show that male reproductive success in ten groups of Verreaux’s sifakas (Propithecus verreauxi) was extremely skewed in favor of the dominant male over 9 years. Our genetic analyses also revealed that more than a third of all groups are effectively harem groups because only one male was unrelated to the resident female(s). In groups with two or more non-natal males, the dominant sired 91% of 33 infants. Together, males pursuing one of several alternative reproductive tactics, such as roaming among several groups or immigrating peacefully, sired only 11% of infants. Thus, female sifakas do not control group composition by offering reproductive opportunities to subordinate males as staying incentives, intrasexual selection is not relaxed, and dominant males prevail in a tug-of-war over subordinate males. Because male reproductive skew in sifakas is even more pronounced than in harem-living anthropoids studied to date, intrasexual selection is clearly not relaxed, and the lemur syndrome is more puzzling than ever.     

Reproductive success of male bank voles (<Emphasis Type="Italic">Clethrionomys glareolus</Emphasis>): the effect of operational sex ratio and body size

The operational sex ratio (OSR) may influence the intensity of competition for mates and mate choice and is therefore thought to be a major factor predicting the intensity and direction of sexual selection. We studied the opportunity for sexual selection, i.e., the variance in male reproductive success and the direction and intensity of sexual selection on male body mass in bank vole (Clethrionomys glareolus) enclosure populations with experimentally manipulated sex ratios. The opportunity for sexual selection was high among male-biased OSRs and decreased towards female-biased OSRs. Paradoxically, selection for large male body mass was strongest in female-biased OSRs and also considerable at intermediate OSRs, whereas at male-biased OSRs, only a weak relationship between male size and reproductive success was found. Litters in male-biased OSRs were more likely to be sired by multiple males than litters in female-biased OSRs. Our results suggest that the intensity and direction of sexual selection in males differs among different OSRs. Although the direction of sexual selection on male body mass was opposite than predicted, large body mass can be favored by sexual selection. Naturally varying OSRs may therefore contribute to maintain variation in male sexually selected traits.     

Genital shape correlates with sperm transfer success in the praying mantis Ciulfina klassi (Insecta: Mantodea)

The rapid divergence of male genitalia is a widely observed evolutionary phenomenon. Although sexual selection is currently regarded as providing the most likely driving force behind genital diversification, the mechanisms responsible are still debated. Here, we investigate the relationship between male genital morphology and sperm transfer in the praying mantid Ciulfina klassi using geometric morphometrics. The shape of male genitalia in C. klassi influenced sperm transfer duration and the number and proportion of sperm transferred, suggesting that genital morphology is under sexual selection in this species. Genital size however was not correlated with any aspect of sperm transfer. Intriguingly, two of the major genital shape components correlated positively with the number of sperm transferred, but negatively with sperm transfer duration. Hence, males that most effectively transfer sperm to the female spermatheca do so in a relatively short period of time. A direct negative relationship was also found between sperm transfer duration and sperm transfer success. Overall, our study suggests that the variable genital shape of Ciulfina may have been selected for more efficient sperm transfer.     

Testing a post-copulatory pre-zygotic reproductive barrier in a passerine species pair

Sexual selection may drive speciation, but most research focuses on pre-copulatory sexual selection, overlooking post-copulatory processes. Post-copulatory sexual selection in allopatric populations could drive divergence in post-copulatory pre-zygotic (PCPZ) phenotypes, limiting gene flow upon secondary contact. Here, we performed in vitro experiments examining one potential PCPZ barrier between two closely related passerine species, house sparrows (Passer domesticus) and Spanish sparrows (Passer hispaniolensis). In birds, crossing in the vagina may be particularly challenging for sperm, so we tested the effect of female reproductive tract fluids on sperm swimming speed and motility. If a PCPZ barrier exists at this stage of the fertilization process, heterospecific female fluids are predicted to reduce sperm swimming speed or motility relative to conspecific female fluid. We found that house sparrow female fluids affected the two species’ sperm asymmetrically, depending on the control sperm velocity and male species. Overall, however, sperm performed equally in conspecific and heterospecific female fluids, and the species had similar sperm morphology and sperm swimming performance. Low divergence in PCPZ phenotypes between species, perhaps because post-copulatory sexual selection is stabilizing or only moderately strong in these taxa, may be insufficient to cause an overall PCPZ barrier. Reinforcement may be unlikely to drive PCPZ barriers for this species pair, because relatively effective pre-copulatory barriers exist between the species, and because hybrids can be quite successful. Testing the role of PCPZ barriers in birds with more divergent PCPZ phenotypes will improve our understanding of speciation in passerines.     

Does delayed fertilization facilitate sperm competition in bats?

Reproductive delays between mating and birth may provide a previously unconsidered avenue for post-copulatory sexual selection in mammals. In particular, delayed fertilization could provide an enhanced opportunity for sperm competition by extending the time for ejaculates to interact in the female reproductive tract. We tested the prediction that species with delayed fertilization exhibit greater degrees of sperm competition than those without delays by examining testis volume (a proxy for sperm competition) in 38 species of bats. Examination of fluid-preserved museum specimens of bat species with and without delays revealed that species with delays (in particular those with delayed fertilization) had significantly larger testes than species without them. Although it predicts the presence of delayed fertilization, hibernation did not predict relative testis size. We conclude that, once they evolve, reproductive delays may facilitate sperm competition.     

Sexual cannibalism facilitates genital damage in <Emphasis Type="Italic">Argiope lobata</Emphasis> (Araneae: Araneidae)

Sperm competition is a potent driving force in evolution leading to a remarkable variety of male adaptations that prevent or reduce fertilization by rivals. An extraordinary defensive strategy against sperm competition has evolved in a number of web spiders where males break off parts of their paired genitalia in order to obstruct the copulatory openings of females (mating plug). A recent comparative analysis on the family level reports that genital damage is most frequent in species with sexual cannibalism although, as yet, a functional association between sexual cannibalism and genital damage has not been found. Using the moderately sexually cannibalistic orb-web spider Argiope lobata, we show for the first time that males cannibalized during their first copulation damaged their pedipalps with significantly higher probability (74%) than males that escaped (15%). Of all males that damaged their genitalia, 44% were able to place a genital fragment inside the copulatory opening of the female, resulting in a relatively low total plugging rate of 14%. Successful obstruction of the female copulatory opening reduced the share of paternity of subsequent males (P ₂ = 0.06%), thus, indicating that genital damage may have evolved as a response to sperm competition in this species as well. However, the low incidence of successful plugging and the strong relationship between sexual cannibalism and genital damage suggest that apart from paternity protection, the nature of genital damage in A. lobata is further shaped by sexual conflict or cryptic female choice.     

Female bank voles (Clethrionomys glareolus) prefer dominant males; but what if there is no choice?

Both intra-sexual competition between males and female mate choice have been found to affect mating behaviour in rodents. We studied female choice in the bank vole (Clethrionomys glareolus) under circumstances where male-male competition was excluded and the female could interact and mate freely with the males. Mating behaviour was observed in two situations: (1) the female encountered two males with a clear dominance relationship; and (2) the two males were equal in their social status. In all tests where a female in postpartum oestrus had a choice between males of different social rank she mated with the dominant one. When choosing between an even pair of males there was no difference in the frequency of lordotic responses, mounts or intromissions the female exhibited with either male before mating with one of them. The mean ejaculation latency was significantly longer in the tests with an even pair of males than in the tests where male hierarchy was clear. These results show that bank vole females are able to discriminate males according to their social status and strongly prefer dominant males as mating partners. However, when the females were presented with two equal males, they seemed to be unable to make a choice. The ability to choose the mating partner when the males are clearly different may be an important direct benefit for the female in terms of time saved during mating and thus decreased risk of predation and infanticide. Received: 16 March 1995/Accepted after revision: 11 February 1996     

Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)—male monopolisation, female mate choice or post-copulatory mechanisms?

One of the basic principles of sexual selection is that male reproductive success should be skewed towards strong males in species with anisogamous sex. Studies on primate multi-male groups, however, suggest that other factors than male fighting ability might also affect male reproductive success. The proximate mechanisms leading to paternity in multi-male primate groups still remain largely unknown since in most primate studies mating rather than reproductive success is measured. Furthermore, little research focuses on a female’s fertile phase. The aim of this study was to investigate the relative importance of male monopolisation and female direct mate choice for paternity determination. We also investigated the extent to which paternity was decided post-copulatory, i.e. within the female reproductive tract. We used a combined approach of behavioural observations with faecal hormone and genetic analysis for assessment of female cycle stage and paternity, respectively. The study was carried out on a group of wild long-tailed macaques living around the Ketambe Research Station, Gunung Leuser National Park, Indonesia. Our results suggest that both male monopolisation and post-copulatory mechanisms are the main determinants of male reproductive success, whereas female direct mate choice and alternative male reproductive strategies appear to be of little importance in this respect. Female cooperation may, however, have facilitated male monopolisation. Since paternity was restricted to alpha and beta males even when females mated with several males during the fertile phase, it seems that not only male monopolisation but also post-copulatory mechanisms may operate in favour of high-ranking males in long-tailed macaques, thus reinforcing the reproductive skew in this species.     

Sexual conflict,sexual selection and sperm competition in the spawning decisions of bitterling, <Emphasis Type="Italic">Rhodeus</Emphasis><Emphasis Type="Italic">sericeus</Emphasis>

Sexual selection may operate through either direct selection on preference genes or indirect genetic benefits. However, in many species both direct and indirect selection may operate and can influence female mate and oviposition choice. Adaptations by males for sperm competition can also affect female mate and oviposition choice and can lead to sexual conflict. We investigated the role of direct and indirect benefits and male adaptation to sperm competition for female oviposition decisions in the bitterling, Rhodeus sericeus, a freshwater fish that spawns on the gills of living unionid mussels. Field experiments showed that females chose mussels for spawning on the basis of the number of embryos already in mussels and the body size and/or extent of red coloration of the eyes of territorial males. There was also a significant interaction between these direct and indirect benefits of oviposition choice. Territorial male bitterling avoided leading females to mussels into which rivals had already released sperm. Males also increased their rate of sperm release into mussels in response to sperm release by sneaking males. We discuss the possibility that sexual conflict in oviposition choice occurs in this species.     

Effects of female mating status on copulation behaviour and sperm expenditure in the freshwater crayfish <Emphasis Type="Italic">Austropotamobius italicus</Emphasis>

Sperm competition models predict that males should adjust their sperm expenditure according to the risk and/or intensity of sperm competition. In this paper, we analysed copulatory behaviour of both sexes and sperm expenditure in relation to female mating status (virgin or mated) in the freshwater crayfish Austropotamobius italicus, a species where males have been reported to feed on and remove sperm laid by other males. The same females were allowed to be inseminated sequentially by two males, and we compared the sexual behaviours of partners between the first (virgin females) and the second mating (mated females). We found that female resistance did not differ between the first and the second mating, nor males refused or took more time to mount a mated female. However, when mating with a mated female, males reached an effective copulation position significantly later. This occurred because second-mating males removed, by eating, all or most spermatophores previously deposited by first males. As removal was often incomplete, this resulted in a larger amount of sperm being deposited on female ventral parts after the second mating, although second males did not allocate more sperm to mated females than first males did. Thus, the peculiar mode of sperm competition, where males remove previously deposited sperm, and the consequent predictable strong last male prevalence in paternity likely led to the observed lack of adjustment of sperm expenditure to female mating status in this species.     

The relative roles of predation and sperm competition on the duration of the post-copulatory association between the sexes in the blue crab, Callinectes sapidus

In many species, post-copulatory mate guarding prevents other males from mating with the guarded female. In crabs, males stay with their mates to protect the female from predators because, in some species, mating occurs when she is soft and vulnerable after molting. I tested the relative roles of sperm competition and predation on the duration of the post-copulatory association in the blue crab, Callinectes sapidus. Unpaired females suffered greater predation mortality than paired females and males stayed with the female longer in the presence of predators than in their absence, suggesting that the post-copulatory association protects females during their vulnerable period. However, the association may also occur in blue crabs because of sperm competition since spermathecal contents of females in the field indicate that 12.4% mated twice. Females experimentally mated with two males contained both males ejaculates and each ejaculate had access to the unfertilized eggs, suggesting that the size of a male's ejaculate influences his fertilization rate in a multiply-mated female. Males stayed longest in response to a high risk of sperm competition. Longer post-copulatory associations allowed the first male's ejaculate to harden into a type of sperm plug, which limited the size of a second inseminator's ejaculate in a non-virgin female as compared with a virgin. Males passed larger ejaculates in the presence of rivals and when previous ejaculates were in the female spermathecae, another response to sperm competition. Larger ejaculates may need longer post-copulatory associations before a more effective sperm plug forms. Large males stayed with the female longer, which is consistent with their ability to pass larger ejaculates than small males and suggests that there may be costs to minimizing the duration of the post-copulatory association. In the field, associations last long enough to protect the female during her vulnerable phase and may ensure that the guarding male fertilizes the most eggs in the female, even if she remates. Thus, the post-copulatory association protects female blue crabs from additional inseminators as well as from predators. Received: 23 January 1996 / Accepted after revision: 9 November 1996     

No evidence that sperm morphology predicts paternity success in wild house wrens

Postcopulatory sexual selection (PCSS) in internally fertilizing vertebrates is a topic of great interest, yet relatively little is known about the characteristics of sperm and ejaculates that confer an advantage in PCSS. In this study, we investigated several measures of sperm morphology that potentially contribute to fertilization success under PCSS. We tested whether sperm morphology related to success in PCSS (via extra-pair paternity) in house wrens (Troglodytes aedon). We found no evidence that sperm morphology differed between extra-pair sires and the within-pair males they cuckolded, nor that sperm morphology correlated with the proportion of within-pair offspring sired, the number of extra-pair offspring sired, or the total annual reproductive success. Male behavioral strategies may affect the probability that their sperm compete with other males’ sperm and that their sperm succeed under competition. Effects of these behavioral strategies, as well as differences between males in sperm number, could mask the effects of sperm morphology on the outcome of PCSS. Despite moderate levels of extra-pair paternity, selection on sperm may be relatively weak in house wrens. Further work is needed to understand general patterns in how sperm morphology relates to fertilization success within species.     

Operational sex ratio and alternative reproductive behaviours in the European bitterling,<Emphasis Type="Italic"> Rhodeus sericeus</Emphasis>

We investigated the effects of male population density and male-biased operational sex ratio (OSR) with constant and limited resource density on male mating tactics shown by a freshwater fish, the European bitterling, Rhodeus sericeus. This species spawns inside living unionid mussels. Large males defended territories and were aggressive towards conspecifics under equal sex ratios. They also monopolised pair spawnings with females, releasing 98% of all sperm clouds during mating. However, the mating tactic changed at high male density where large males ceased to be territorial and instead competed with groups of smaller males to release sperm when females spawned. Large, medium and small males now obtained 61%, 33%, and 6% of sperm releases respectively, thereby reducing the opportunity for sexual selection by half. Females spawned at equal rates in the two densities of males, despite lower courtship at high density. These results run counter to the usual expectation that an increasingly male-biased OSR should lead to higher variance in male mating success. Instead, the use of alternative reproductive behaviours by males can lead to lower resource competition and mating variance at high male densities.     

Pre- and post-mating sexual selection both favor large males in a rainbowfish

Sexual selection can act through female choice and male–male competition. Although both processes can act simultaneously, they are typically studied independently. Here, we adopt a more integrated approach to studying sexual selection by incorporating measures of both processes using the western rainbowfish Melanotaenia australis, a freshwater fish endemic to northwestern Australia. We assessed male–male competition and female choice separately while measuring the performance of individual males under both processes and used paternity analyses to estimate male reproductive success. We then related the performance of males during each of these stages to their phenotype, which was described using linear measures of size and color pattern traits, and spectrographic measures of the reflectance of color patches. We found that female choice favored relatively large males and that these preferences were consistent within individual females and repeatable between different females. Larger males were also more dominant in the competition trials and sired the majority of offspring produced when females spawned. There was little evidence to suggest that sexual selection acted on male color patterns either via female choice or male contest competition or during subsequent post-mating episodes of sexual selection. We conclude, therefore, that male–male competition and female choice act concordantly to favor relatively large males and that these patterns of mating success are reflected during post-mating episodes of sexual selection.     

Male genital traits and mating interval affect male fertilization success in the water strider Gerris lacustris

Parker's seminal work brought attention to the possibility of postmating sexual selection by non-random fertilization success. Mechanisms for these processes are still only partly understood and there is clearly a need for more studies of intraspecific variation in sperm precedence. Here, we report results from an experimental study of the variation in fertilization success between males of the water strider Gerris lacustris. Genital morphology, male body size, and copulation duration were examined as possible correlates of paternity. The significance of guarding duration was also analysed. Only male genital morphology was correlated to fertilization success. This is one of the first studies showing a relationship between male genital traits and fertilization success, supporting the view that sexual selection may be responsible for the rapid and divergent evolution of genital structures in animals with internal fertilization. The fertilization success of last males varied considerably after double matings with a short mating interval (10 min). Last-male priority ranged from 0 to 100% and usually one of the males involved fertilized almost all the eggs. After double matings with a short mating interval, the proportion of eggs fertilized by the last male averaged 0.68 and was greater than 0.5. In contrast, the average fertilization success was biased towards the first male when the matings were more spread out over time (24 h). These results do not support earlier suggestions of a widespread last-male sperm priority in water striders. Received: 28 July 1998 / Received in revised form: 15 March 1999 / Accepted: 28 March 1999     

Repeatability and heritability of sperm competition outcomes in males and females of <Emphasis Type="Italic">Tribolium castaneum</Emphasis>

Differences among males in their success in achieving fertilisations when females mate with more than one partner are now recognised as an important target of sexual selection. However, very few studies have attempted to determine whether particular males are consistently successful in sperm competition and whether success in sperm competition is a heritable trait. Additionally, the potential heritability of female traits that influence the outcome of sperm competition has received only limited attention. Using the polyandrous beetle Tribolium castaneum, we examined repeatability of male success in sperm competition by mating pairs of males carrying different visible genetic markers to a string of different females. Males showed consistency in their ability to successfully transfer sperm to females, but not in their success in sperm competition. Furthermore, when we independently compared success in sperm competition of fathers with their sons, we found no evidence for heritability of this trait. Similarly, females that exhibited high or low first male sperm precedence did not tend to have daughters that showed the same pattern. Our results suggest that we should be wary of assuming that success in sperm competition is heritable through either sex.