Not just a chastity belt: the functional significance of mating plugs in garter snakes,revisited

During the spring emergence of red‐sided garter snakes (Thamnophis sirtalis parietalis) in Manitoba, Canada, the operational sex ratio is strongly skewed towards males, who scramble to locate and court newly emerged females. A high frequency of multiple paternity litters suggests that the females are promiscuous; the gelatinous copulatory plugs (CPs) deposited by males may confer fitness benefits via passive mate guarding. Because precopulatory female choice is limited in large mating aggregations, sexual conflict may place a premium on preventing females from ejecting male sperm. In snakes, sperm are produced in the testes and delivered through the ductus deferens, and the CP is thought to be produced by the renal sexual segment and conveyed through the ureter. We manipulated the delivery of the two fluids separately by surgically ligating the ducts. Ureter‐ligated males did not produce a CP, causing their sperm to leak out of the female's cloaca immediately after copulation. Contrary to previous suggestions, histology revealed sperm distributed throughout the CP. Thus, the CP may function as a spermatophore: the protein matrix contains the sperm, which are liberated gradually as the plug dissolves. The likelihood of a male depositing a CP fell significantly after his second mating, perhaps limiting his reproductive success. These results challenge the hypothesis that passive mate guarding is the primary function of the CP in T. sirtalis parietalis. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 893–907.     

Sex‐specific repeatabilities and effects of relatedness and mating status on copulation duration in an acridid grasshopper

In species with direct sperm transfer, copulation duration is a crucial trait that may affect male and female reproductive success and that may vary with the quality of the mating partner. Furthermore, traits such as copulation duration represent the outcome of behavioral interactions between the sexes, for which it is important—but often difficult—to determine which sex is in phenotypic control. Using a double‐mating protocol, we compared copulation durations between (1) virgin and nonvirgin and (2) sibling and nonsibling mating pairs in rufous grasshoppers Gomphocerippus rufus. Nonvirgin copulations took on average approximately 30% longer than virgin copulations, whereas relatedness of mating partners was not a significant predictor of copulation duration. Longer nonvirgin copulations may represent a male adaptation to sperm competition if longer copulations allow more sperm to be transferred or function as postinsemination mate guarding. The absence of differences between pairs with different degrees of relatedness suggests no precopulatory or preinsemination inbreeding avoidance mechanism has evolved in this species, perhaps because there is no inbreeding depression in this species, or because inbreeding avoidance occurs after copulation. Controlling for the effects of male and female mating status (virgin vs. nonvirgin) and relatedness (sibling vs. nonsibling), we found significant repeatabilities (R) in copulation duration for males (R = 0.33; 95% CI: 0.09–0.55) but not for females (R = 0.09; 95% CI: 0.00–0.30). Thus, copulation durations of males more strongly represent a nontransient trait expressed in a consistent manner with different mating partners, suggesting that some aspect of the male phenotype may determine copulation duration in this species. However, overlapping confidence intervals for our sex‐specific repeatability estimates indicate that higher sampling effort is required for conclusive evidence.     

Pre‐ and postcopulatory sexual selection act in concert to determine male reproductive success in Tribolium castaneum

To capture how sexual selection shapes male reproductive success across different stages of reproduction in Tribolium castaneum (Coleoptera, Tenebrionidae), we combined sequential sperm defence (P1) and sperm offence (P2) trials with additional trials where both males were added simultaneously to the female. We found a positive correlation between the relative paternity share in simultaneous male–male competition trials and the P2 trial. This suggests that males preferred by females as sires achieve superior fertilization success during sperm competition in the second male position. In simultaneous male–male competition trials, where pre‐, peri‐ and postcopulatory sexual selection were all allowed to act, the relative paternity share of preferred males was more than 20% higher than in P2 sperm competition trials where precopulatory female choice was disabled. Additional behavioural observations revealed that mating with more attractive males resulted significantly more frequently in offspring production than mating with less attractive males. Thus, by comparing male fertilization success in trials where precopulatory choice was turned off with more inclusive estimates of fertilization success where pre‐ and pericopulatory choice could occur, we show that female mate choice may effectively inhibit sperm competition. Female mate choice and sperm competition (P2) are positively correlated, which is consistent with directional sexual selection in this species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 67–75.     

Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve,Madagascar

Observations of reproductive behavior in free-ranging Lemur catta were carried out during one annual cycle. Variability in the behavior of female ringtailed lemurs during parturition appears to be mainly a function of the female's parity and thus her experience. Females within a troop show estrous asynchrony and characteristically mate with more than one male. Females also exhibit proceptive behavior toward and mate with some males from other troops and with transferring males. The potential for a male to monopolize mating opportunities during a female's short estrous period is therefore limited. Male mating strategies in ringtailed lemurs can be seen as adaptations to female mate choice during a highly restricted breeding season. In this species the dominance hierarchy does not break down with regard to the order of mating. The highest ranking male (central male) mates first and shows precopulatory guarding and longer postejaculatory guarding, which may increase his chances of siring the offspring. Subsequent mating partners have developed various counterstrategies to mitigate mating order effects.     

Male Choice and Male-male Competition in Idotea baitica (Crustacea,Isopoda)

Sexual selection in mate-guarding Crustacea may involve several processes: male choice, male-male competition, and female choice. To evaluate the relative importance of the different processes in mate choice of the aquatic isopod I. baitica we studied 1) the mate-choice criteria of males, 2) effects of sex ratio on the outcome of the mating contest, and 3) the role of size in male-male interactions. When given a choice between a small and a large female, males most often chose the one that matured earlier for parturial ecdysis. Maturity was a more important choice criterion than female size, but these also correlated positively. Large males had a mating advantage in both male- and female-biased sex ratios; pairing was size-assortative only in the male-biased ratio where guarding was also longer. If an extra male was placed with a precopulatory pair, 30 % take-overs occurred, large males surpassing. Present and earlier work suggests that male size is an asset in both intra- and intersexual interactions. There is little or no direct phenotypic sexual selection on female size: sexual selection for large males presumably contributes to the evolution of sexual size dimorphism in I. baitica.     

UNDERSTANDING PROMISCUITY: WHEN IS SEEKING ADDITIONAL MATES BETTER THAN GUARDING AN ALREADY FOUND ONE?

Paternity protection and the acquisition of multiple mates select for different traits. The consensus from theoretical work is that mate‐guarding intensifies with an increasing male bias in the adult sex ratio (ASR). A male bias can thus lead to male monogamy if guarding takes up the entire male time budget. Given that either female‐ or male‐biased ASRs are possible, why is promiscuity clearly much more common than male monogamy? We address this question with two models, differing in whether males can assess temporal cues of female fertility. Our results confirm the importance of the ASR: guarding durations increase with decreasing female availability and increasing number of male competitors. However, several factors prevent the mating system from switching to male monogamy as soon as the ASR becomes male biased. Inefficient guarding, incomplete last male sperm precedence, any mechanism that allows sperm to fertilize eggs after the male's departure, and (in some cases) the unfeasibility of precopulatory guarding all help explain cases where promiscuity exists on its own or alongside temporally limited mate‐guarding. Shortening the window of fertilization shifts guarding time budgets from the postcopulatory to the precopulatory stage.     

No evidence for external genital morphology affecting cryptic female choice and reproductive isolation in Drosophila

Genitalia are one of the most rapidly diverging morphological features in animals. The evolution of genital morphology is proposed to be driven by sexual selection via cryptic female choice, whereby a female selectively uptakes and uses a particular male's sperm on the basis of male genital morphology. The resulting shifts in genital morphology within a species can lead to divergence in genitalia between species, and consequently to reproductive isolation and speciation. Although this conceptual framework is supported by correlative data, there is little direct empirical evidence. Here, we used a microdissection laser to alter the morphology of the external male genitalia in Drosophila, a widely used genetic model for both genital shape and cryptic female choice. We evaluate the effect of precision alterations to lobe morphology on both interspecific and intraspecific mating, and demonstrate experimentally that the male genital lobes do not affect copulation duration or cryptic female choice, contrary to long‐standing assumptions regarding the role of the lobes in this model system. Rather, we demonstrate that the lobes are essential for copulation to occur. Moreover, slight alterations to the lobes significantly reduced copulatory success only in competitive environments, identifying precopulatory sexual selection as a potential contributing force behind genital diversification.     

Delayed copulation as a means of female choice by the hermit crab Pagurus filholi

Male hermit crabs perform precopulatory mate-guarding behavior during their reproductive season. As females generally cannot reject guarding attempts by males, male guarding prevents females from inspecting and choosing other male mates. However, as guarding males are often replaced by other males through competition for females during the guarding phase, females may be able to select males by delaying their copulation. To examine the possibility of female choice by hermit crabs, we investigated whether female Pagurus filholi that were being guarded in the field were ready to copulate and spawn. We found that about 30% of females guarded in the field were ready to spawn, indicating that guarded females delayed copulation with their current male. Our results suggest that by delaying copulation females may exploit male–male competition to choose dominant males. However, delaying copulation reduced the spawning potential of females. Hence, there is a trade-off between waiting for the opportunity to mate with a dominant male and decreased spawning success if females exploit male–male competition.     

Mating behavior in the tydeid miteHomeopronematus anconai (Acari: Tydeidae)

The mating behavior ofHomeopronematus (Pronematus) anconai (Baker) is described. This is the first report of direct sperm transfer in the family Tydeidae (Acari: Actinedida). Male guarding of pharate females and male agonistic behavior was observed. Successful mating occurred only during the first day of active female life. Specialized male structures, a hook on femur IV and a modified seta on genu IV, were examined by scanning electron microscope. These structures appear to be involved in holding the female during copulation.     

Post-copulatory Mounting Behavior of the West Indian Sweetpotato Weevil, Euscepes postfasciatus (Fairmaire) (Coleoptera: Curculionidae)

Post‐copulatory associations between males and females have been found in a variety of insects and are often described as mate guarding. Males of the West Indian sweetpotato weevil Euscepes postfasciatus (Fairmaire) mount the female's back after copulation. Two hypotheses have been advanced to explain this behavior: mate guarding to prevent future copulations by rivals (hypothesis 1), and mate guarding to gain additional copulations (hypothesis 2). We conducted three experiments to test predictions from these hypotheses. Our results disproved hypothesis 1 because the duration of the post‐copulatory association was very brief in comparison with the length of the refractory phase all females showed after copulation. When we prevented females from resisting copulations during the post‐copulatory mounted phase males copulated again, while under normal conditions, a second copulation was never observed. This result may indicate the presence of a sexual conflict over mating. However, we propose an alternative interpretation of the result, namely that after mating, males test whether the copulation has successfully reduced female receptivity by attempting to remate. If females resist the mating, males leave.     

飞蝗抱对行为的进化意义及两型间相异的交配策略

飞蝗Locusta migratoriaL.不仅交配时间长,而且进行频繁的、长时间的交配前抱对。一般认为,交配前抱对行为是雄虫为了等待时机获取适时的交配。最近的研究表明,飞蝗的交配时间与P2值(最后交配雄虫子代的比例)、交配前抱对时间与交配时间存在显著的正相关关系,即飞蝗长时间的交配前抱对行为能延长其后续的交配时间,从而提高P2值。飞蝗具变型现象,散居型和群居型在形态特征、生理机能、行为及体色等方面存在明显差异。最近的研究结果显示,散居型较群居型具更高的P2值,较短的交配前抱对和较长的交配时间。冲绳和筑波种群散居型成虫的交配前抱对时间与交配时间存在显著的正相关关系,而群居型无此相关性。这些结果证实飞蝗散居型和群居型之间存在着繁殖策略的差异。     

Female mate choice in relation to heterozygosity in Tribolium castaneum

Abstract Female mate choice, both before and after copulation, is pervasive among insect species. It is often hypothesized that females would preferentially mate with males that are genetically dissimilar to promote the genetic variability of the offspring. We used various strains of red flour beetle, Tribolium castaneum, and tested the effect of male and female genetic backgrounds on precopulatory and post‐copulatory female mate choice. Simultaneous mate choice experiments using previously well established pheromone assays did not detect female preference for males of different strains. Post‐copulatory female mate choice was examined through paternity analysis. Two parameters were used to measure post‐copulatory female mate choice, including male defence capacity (P₁, proportion of offspring sired by the first male when a female mated with two males consecutively) and offence capacity (P₂, proportion of offspring sired by the second of two males to mate with a female). When female and male beetle strains were same, defence capacity was significantly higher than when female and male strains were different. However, such a pattern was not observed for offence capacity. The results suggest that female precopulatory mate choice is not affected by genetic background, but the outcome of post‐copulatory processes depends on the genetic background of male and female beetles.     

Female mate choice across mating stages and between sequential mates in flour beetles

Few studies have examined how female premating choice correlates with the outcome of copulatory and post-copulatory processes. It has been shown that polyandrous Tribolium castaneum females discriminate among males before mating based on olfactory cues, and also exert cryptic choice during mating through several mechanisms. This study tested whether a male's relative attractiveness predicted his insemination success during copulation. Bioassays with male olfactory cues were used to rank two males as more and less attractive to females; each female was then mated to either her more attractive male followed by less attractive male, or vice versa. Dissections immediately after second copulations revealed a significantly higher percent of successful inseminations for females that remated with more attractive males compared with those that remated with less attractive males. These results indicate that cryptic female choice during copulation reinforces precopulatory female choice in T. castaneum, and suggest that females could use cryptic choice to trade up to more attractive males, possibly gaining better phenotypic or genetic quality of sires.     

The effect of hunger on mating behaviour and sexual selection for male body size in Gerris buenoi

The set of mating behaviours expressed by an individual may depend upon the state of that individual and local environmental conditions. Understanding how these factors affect mating behaviours may elucidate how a mating system operates, and its consequences for the form and strength of sexual selection. We conducted two experiments on the water striderGerris buenoi to (1) determine the effect of hunger on the mating behaviour of both sexes and (2) examine female choice for large males. In our first experiment, we manipulated hunger (20 h starvation) in both sexes and recorded mating, male harassment, copulation duration and guarding duration. We predicted that hunger would increase female reluctance to mate because mating conflicts with foraging. Female hunger (20 h starvation) decreased mating rate by two-thirds but had no significant effect on male mating behaviour. In a second experiment, we examined the effect of female hunger, and resulting reluctance, on sexual selection for large male size. Hungry females (5 h starvation) were placed with two fed males (one large, one small) and we recorded male premating and mating behaviours. We observed significant large-male mating advantage when females were hungry, but not when satiated. Mating efforts (harassment, premating struggles) were similar for both male phenotypes in both female hunger treatments, suggesting that the mating advantage of large males resulted from increased reluctance of hungry females to mate. Neither male body size nor female hunger explained a significant amount of variation in copulation duration or guarding duration. We discuss our results in light of two competing hypotheses for female choice (active and passive) on male body size and suggest that passive choice for large males acts in this system. Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour     

Primate copulation calls and postcopulatory female choice

Females in some species of Old World monkeys and apes vocalizeafter copulation, but the function of these vocalizations isnot clear. In this article, we examine the hypothesis that copulationcalls are a form of postcopulatory female choice. Accordingto this hypothesis, copulation calls are honest signals of fertility(i.e., ovulation) that are used by females to encourage mateguarding by their preferred mating partners and reduce the likelihoodof sperm competition. Evidence in favor of this hypothesis isreviewed and discussed in relation to other hypotheses. We suggestthat the evolution of female copulation calls in primates islinked to the evolution of other female mating signals suchas exaggerated sexual swellings, the potential for sperm competition,and the opportunity for precopulatory female mate choice.     

Competing for last place: Mating behaviour in a pill-box crab, Halicarcinus cookii (Brachyura: Hymenosomatidae)

The mating strategy of Halicarcinus cookii was investigated to ascertain how males maximised their fitness through mate choice. An intertidal population at Kaikoura, New Zealand, was dominated by mature crabs of both sexes in summer and by immature crabs in the colder months. More than 95% of mature females were ovigerous with early stage and late stage broods found in almost every month, indicating that egg production and larval release is continuous. The operational sex ratio was less than 1 male/female in summer, but often more than 1.0 in the colder months. The gonosomatic index increased along with brood development so that as soon as zoeae were released, the next clutch of eggs was ready to be fertilised. Males searched for receptive females and began pre-copulatory mate guarding without any courtship display. They mated preferentially with late stage or non-ovigerous females: copulation duration was longest for stage 5 females as was post-copulatory guarding (mean 18.3 h). Late stage females were up to 14% of the female population. Mate attraction seems to be the result of an ovarian signal rather than from the developing brood. Manipulation of the sex ratio had effects upon copulation duration and post-copulatory guarding: presence of a rival male increased duration of guarding. Females showed precocious mating in the penultimate instar and were able to lay fertilised eggs after their pubertal moult in the absence of males. H. cookii females have many mates, but males attempt to ensure paternity by preferentially pursuing mature females close to egg laying and by guarding these females after copulation. These behaviours are all elements of a competitive strategy to ensure that a male loses (not wins) the race to copulate because females have a ventral seminal receptacle, giving sperm precedence to the last male to mate. Male mating behaviour is a consequence and evolutionary response to female morphology.     

Mate discrimination in Littorina littorea (L.) and L. saxatilis (Olivi) (Mollusca:Prosobranchia)

The ability of males of Littorina littorea and L. saxatilis to discriminate between mates of different sex, species and size was examined. In partner choice experiments males of L. littorea had the possibility to initiate a copulation with either a female or a male. The males did not show a preference for either sex. There was therefore no evidence that they could determine the sex of a conspecific prior to copulation. The duration of intrasexual copulation was considerably shorter than for intersexual copulation, both in the field and in laboratory experiments. For the two species, intersexual copulations were far more frequent than intrasexual ones. This can partly be explained by the difference in copulation time.Few interspecific copulating pairs were found on the shore. This may reflect a low interspecific encounter rate rather than a mechanism of species recognition. On all of these occasions, however, the active male was of L. saxatilis. It is argued that selection against precopulatory species and sex recognition is a more likely explanation than an hypothesis that states that the required mutations for precopulatory mate identification has not yet occurred. L. littorea males copulated longer with large than with small females. Copulation time was short with parasitized females, which are sterile or of low fecundity. The allocation of mating effort by males is discussed.     

A time-sequence functional analysis of mating behaviour and genital coupling in Drosophila: role of cryptic female choice and male sex-drive in the evolution of male genitalia

Male genitalia in Drosophila exemplify strikingly rapid and divergent evolution, whereas female genitalia are relatively invariable. Whereas precopulatory and post-copulatory sexual selection has been invoked to explain this trend, the functional significance of genital structures during copulation remains obscure. We used time-sequence analysis to study the functional significance of external genitalic structures during the course of copulation, between D. melanogaster and D. simulans. This functional analysis has provided new information that reveals the importance of male-driven copulatory mechanics and strategies in the rapid diversification of genitalia. The posterior process, which is a recently evolved sexual character and present only in males of the melanogaster clade, plays a crucial role in mounting as well as in genital coupling. Whereas there is ample evidence for precopulatory and/or post-copulatory female choice, we show here that during copulation there is little or no physical female choice, consequently, males determine copulation duration. We also found subtle differences in copulatory mechanics between very closely related species. We propose that variation in male usage of novel genitalic structures and shifts in copulatory behaviour have played an important role in the diversification of genitalia in species of the Drosophila subgroup.     

Males mate guard in absentia through extended effects of postcopulatory courtship in the parasitoid wasp Spalangia endius (Hymenoptera: Pteromalidae)

The proximal mechanisms leading to monandry have been little studied in most insect orders, including Hymenoptera. In the parasitoid wasp Spalangia endius, mated females are less attractive (less often mounted) than virgins and are unreceptive (unlikely to allow copulation). Which aspects of mating are responsible was tested by observing male responses toward females whose mating had been interrupted at various stages. All females were allowed to receive precopulatory courtship and to open their genital aperture to copulate. Then some were interrupted before copulation, some after copulation but before postcopulatory courtship, and some were allowed to complete postcopulatory courtship. Females that had copulated were not less attractive than females that had not. In contrast, females that had received postcopulatory courtship were clearly both less attractive and less receptive. Thus, postcopulatory courtship functions as extended mate guarding, by making the female less attractive and less receptive to subsequent males even after the original male is no longer present. The effect of postcopulatory courtship on female attractiveness was persistent but imperfect: when males were presented sequentially to mated females, most but not all males retreated without mounting, and a female could repulse more than twenty males in succession.     

Male Performance and Body Size Affect Female Re-Mating Occurrence in the Orb-Web Spider Leucauge mariana (Araneae, Tetragnathidae)

Females can affect male probabilities of paternity success through behavioural, morphological and/or physiological processes occurring during or after copulation. These processes under female-control include the acceptance or rejection of mating attempts by subsequent males. Leucauge mariana is an orb weaving spider that shows male mate guarding of penultimate females, male–male competition on female webs and copulatory plugs, suggesting a polyandric mating system. The aim of the present study was to ascertain whether male behaviour during courtship and copulation in L. mariana relate with female re-mating decisions. Forty-three virgin females were exposed to up to three males until they mated. In 24 cases, the copulatory plug was absent after mating and females were exposed the next day to up to three other males. Eighteen females accepted a second mating. Relatively larger females were more receptive to second matings and were more likely to copulate if the second male was smaller. Longer duration of female tapping and abdominal bobbing during courtship, and first copulations with less short insertions and more flubs, were associated with increased female acceptance to second matings. The results indicate cryptic female choice on male courtship and copulatory performance and suggest female-control over the determination of male mating success in this spider species.