Sexual selection and assortative mating: an experimental test

Mate choice and mate competition can both influence the evolution of sexual isolation between populations. Assortative mating may arise if traits and preferences diverge in step, and, alternatively, mate competition may counteract mating preferences and decrease assortative mating. Here, we examine potential assortative mating between populations of Drosophila pseudoobscura that have experimentally evolved under either increased (‘polyandry’) or decreased (‘monogamy’) sexual selection intensity for 100 generations. These populations have evolved differences in numerous traits, including a male signal and female preference traits. We use a two males: one female design, allowing both mate choice and competition to influence mating outcomes, to test for assortative mating between our populations. Mating latency shows subtle effects of male and female interactions, with females from the monogamous populations appearing reluctant to mate with males from the polyandrous populations. However, males from the polyandrous populations have a significantly higher probability of mating regardless of the female's population. Our results suggest that if populations differ in the intensity of sexual selection, effects on mate competition may overcome mate choice.     

Cultural influences on female mate choice: an experimental test in cowbirds, Molothrus ater

Previous studies of brown-headed cowbirds Molothrus ater, have shown that social learning and cultural transmission can influence courtship and mating patterns. These earlier studies did not test whether cultural background influenced mate choice in females and therefore whether culture could potentially play a role in sexual selection in this species, as has been suggested by recent theory. Here, we tested whether culture influences female mate choice in brown-headed cowbirds. Female cowbirds from a South Dakota population were housed with adult cowbirds from the same South Dakota population or with adult cowbirds from a behaviourally distinct population from Indiana. We tested the mating preferences of females of the South Dakota culture and females of the Indiana culture in sequential mate-choice trials with males, controlling for intrasexual interactions. The males were South Dakota cowbirds that had also been housed either in the South Dakota culture or in the Indiana culture. Females showed mating preferences for males from their own culture. These results suggest that mate choice in female cowbirds can be influenced by cultural background. We briefly discuss the effect that culture may have on sexual selection and on the evolution of female mating preferences. Copyright 1999 The Association for the Study of Animal Behaviour.     

Sexual conflict over mating in red-sided garter snakes (Thamnophis sirtalis) as indicated by experimental manipulation of genitalia

Sexual conflict over mating can result in sex-specific morphologies and behaviours that allow each sex to exert control over the outcome of reproduction. Genital traits, in particular, are often directly involved in conflict interactions. Via genital manipulation, we experimentally investigated whether genital traits in red-sided garter snakes influence copulation duration and formation of a copulatory plug. The hemipenes of male red-sided garter snakes have a large basal spine that inserts into the female cloaca during mating. We ablated the spine and found that males were still capable of copulation but copulation duration was much shorter and copulatory plugs were smaller than those produced by intact males. We also anaesthetized the female cloacal region and found that anaesthetized females copulated longer than control females, suggesting that female cloacal and vaginal contractions play a role in controlling copulation duration. Both results, combined with known aspects of the breeding biology of red-sided garter snakes, strongly support the idea that sexual conflict is involved in mating interactions in this species. Our results demonstrate the complex interactions among male and female traits generated by coevolutionary processes in a wild population. Such complexity highlights the importance of simultaneous examination of male and female traits.     

Sex peptide causes mating costs in female Drosophila melanogaster

Conflicts between females and males over reproductive decisions are common . In Drosophila, as in many other organisms, there is often a conflict over how often to mate. The mating frequency that maximizes male reproductive success is higher than that which maximizes female reproductive success . In addition, frequent mating reduces female lifespan and reproductive success , a cost that is mediated by male ejaculate accessory gland proteins (Acps) . We demonstrate here that a single Acp, the sex peptide (SP or Acp70A), which decreases female receptivity and stimulates egg production in the first matings of virgin females , is a major contributor to Acp-mediated mating costs in females. Females continuously exposed to SP-deficient males (which produce no detectable SP ) had significantly higher fitness and higher lifetime reproductive success than control females. Hence, rather than benefiting both sexes, receipt of SP decreases female fitness, making SP the first identified gene that is likely to play a central role in sexual conflict.     

Effect of Male Accessory Gland Products on Egg Laying in Gastropod Molluscs

In internally fertilizing animals, seminal fluid is usually added to the spermatozoa, together forming the semen or ejaculate. Besides nourishing and activating sperm, the components in the seminal fluid can also influence female physiology to augment fertilization success of the sperm donor. While many studies have reported such effects in species with separate sexes, few studies have addressed this in simultaneously hermaphroditic animals. This video protocol presents a method to study effects of seminal fluid in gastropods, using a simultaneously hermaphroditic freshwater snail, the great pond snail Lymnaea stagnalis, as model organism. While the procedure is shown using complete prostate gland extracts, individual components (i.e., proteins, peptides, and other compounds) of the seminal fluid can be tested in the same way. Effects of the receipt of ejaculate components on egg laying can be quantified in terms of frequency of egg laying and more subtle estimates of female reproductive performance such as egg numbers within each egg masses. Results show that seminal fluid proteins affect female reproductive output in this simultaneous hermaphrodite, highlighting their importance for sexual selection.     

Sexual selection on Drosophila serrata male pheromones does not vary with female age or mating status

Mate preferences are costly and are thought to evolve due to the direct and/or indirect benefits they provide. Such costs and benefits may vary in response to intrinsic and extrinsic factors with important evolutionary consequences. Limited attention has been given to quantifying such variation and understanding its causes, most notably with respect to the direction and strength of preferences for multivariate sexual displays. In Drosophila serrata, female preferences target a pheromone blend of long‐chain cuticular hydrocarbons (CHCs). We used a factorial design to test whether female age and mating status generated variation in the strength and direction of sexual selection on male CHCs. Replicate choice mating trials were conducted using young and old females (4 or 10 days post‐emergence) that were either virgin or previously mated. The outcome of such trials is known to capture variation in female mate preferences, although male–male interactions may also contribute. Directional sexual selection on male CHCs was highly significant within each treatment, but there was little evidence of any variation among treatments. The absence of treatment effects implies that the multivariate combination of male CHCs preferred by females was constant with respect to female age and mating status. To the extent that male–male interactions may also contribute, our results similarly imply that these did not vary among treatments groups. With respect to D. serrata mate preferences, our results suggest that either plasticity with respect to age and mating status is not beneficial to females, or preference expression is somehow constrained.     

Indications for female mate choice in grey-cheeked mangabeys <Emphasis Type="Italic">Lophocebus albigena johnstoni</Emphasis> in Kibale National Park,Uganda

Female sexual strategies affect male strategies and can play an important role in shaping mating systems. We investigated female sexual behaviour within five groups of grey-cheeked mangabeys in Kibale National Park, Uganda, and tested the hypothesis that females exhibit mate choice using as indications the prevalence of (1) females soliciting matings by presenting to males and (2) females refusing to mate with approaching males. In addition, we describe how these behaviours as well as grooming and copulation calls are distributed over high-ranking, low-ranking and migrating males and discuss these patterns with regard to trade-offs that could play a roll in female mate choice in multi-male groups. Females were promiscuous and initiated almost half of the matings, with both resident and migrating males. More than half of male mating approaches were refused by peak females. Female mate choice in this species may depend on individual female preferences, oestrus phase and male tactic.     

Sexual selection in hermit crabs: a review and outlines of future research

The information currently available on sexual selection in hermit crabs is reviewed to identify the role of males and females before, during and after mating. According to this information, possible mechanisms of male–male competition, female choice and/or sexual conflict are suggested. Important male components that may affect mating success include dragging the female shell, rotations of the female's shell and male cheliped palpations, and male size and/or shell characteristics (species and size). Possible female determinants of male mating/fertilization success include size (as an indicator of egg production capacity), signalling of sexual receptivity to males, delay from mate guarding to copulation and mating duration. Avenues for deeper exploration in males include the role of the number and morphometry of male sexual tubes during sperm transfer, and whether ejaculate size and sperm number can be adjusted with variable situations of sperm competition intensity and risk. In females it would be interesting to investigate the chemical and behavioural mechanisms affecting spermatophore breakage for sperm release and the variable duration from sperm transfer to spawning. Given these possibilities, and that sperm is externally deposited on the female's body but inside her shell (except for those species that do not use shells, e.g. Birgus , or species where shells are rather small and do not cover the body totally, e.g. Parapagurus ), we conclude that hermit crabs are unique subjects for separating male and female effects, particularly with respect to the applicability of current ideas in sexual selection such as female choice and sexual conflict. Some practical ideas are provided to disentangle both hypotheses using these animals.     

Mating order-dependent female mate choice in the polygynandrous common lizard Lacerta vivipara

Recent studies indicate that directional female mate choice and order-dependent female mate choice importantly contribute to non-random mating patterns. In species where females prefer larger sized males, disentangling different hypotheses leading to non-random mating patterns is especially difficult, given that male size usually correlates with behaviours that may lead to non-random mating (e.g. size-dependent emergence from hibernation, male fighting ability). Here we investigate female mate choice and order-dependent female mate choice in the polygynandrous common lizard (Lacerta vivipara). By sequentially presenting males in random order to females, we exclude non-random mating patterns potentially arising due to intra-sexual selection (e.g. male–male competition), trait-dependent encounter probabilities, trait-dependent conspicuousness, or trait-dependent emergence from hibernation. To test for order-dependent female mate choice we investigate whether the previous mating history affects female choice. We show that body size and body condition of the male with which a female mated for the first time were bigger and better, respectively, than the average body size and body condition of the rejected males. There was a negative correlation between body sizes of first and second copulating males. This indicates that female mate choice is dependent on the previous mating history and it shows that the female’s choice criteria are non-static, i.e. non-directional. Our study therefore suggests that context-dependent female mate choice may not only arise due to genotype-environment interactions, but also due to other female mating strategies, i.e. order-dependent mate choice. Thus context-dependent female mate choice might be more frequent than previously thought.     

Female mate choice and mating costs in the polyandrous butterflyPieris napi (Lepidoptera: Pieridae)

Males of the green-veined white butterfly (Pieris napi L.) transfer large ejaculates that represent on average 15% of their body mass when mating for a first time. Shortly after mating a male is able to transfer only a small ejaculate when mating a second time. Male ejaculate production plays a crucial role in the mating system ofP. napi because females use male-derived nutrients for egg production and somatic maintenance. Here we study how timing of female rematings and copulation duration are influenced by the mating history of their mates and, also, study if females exert mate choice to minimize their mating costs. Mating with a recently mated male increased female mating costs by increasing time in copula and mating frequency. Virgin females that mated with virgin males remated after an average of 6 days, whereas virgin females that mated with recently mated males remated after an average of 2 days. Moreover, copulations involving recently mated males lasted on average almost 7 h, whereas copulations involving virgin males lasted on average 2 h. Recently mated males were eager to remate, in spite of the fact that the size of the ejaculate they transfer is small and that they remain in copula for a long time. Hence it seems that males are more successful in the sexual conflict over mating decisions and that females do not minimize mating costs by choosing to mate preferentially with virgin males.     

Coolidge effect in pond snails: male motivation in a simultaneous hermaphrodite

Background  

The simultaneously hermaphroditic pond snail, Lymnaea stagnalis, can mate in the male and female role, but within one copulation only one sexual role is performed at a time. Previous work has shown that male motivation is determined by the availability of seminal fluid in the prostate gland, which is detected via a nervous connection by the brain area controlling male behaviour. Based on this knowledge, patterns of sexual role alternations within mating pairs can be explained.     

Sexual Inhibition in <Emphasis Type="Italic">Spalangia endius</Emphasis> Males After Mating and Time for Ejaculate Replenishment

Although males are often stereotyped as always sexually responsive, a previous study with the parasitoid wasp Spalangia endius showed that males exhibit a post-mating decrease in sexual responsiveness. The present study examined the duration of the decrease and whether waiting to remate increased the amount of ejaculate that a male provided to his second mate. Mated males were back to being as sexually responsive as virgin males by about 5 min after mating. The amount of ejaculate that females received from already mated males was not significantly related to the duration between the male’s first and second mating. The short-term decrease in sexual responsiveness of a mated male may prevent him from immediately trying to remate with the same female because it gives her time to get away.     

Female mate choice and male–male competition in Tonkean macaques: Who decides?

The theory of sexual selection predicts that females should be discriminatory in the choice of sexual partners. Females can express their choice in two ways. In direct mate choice, they show preferences for certain partners. In indirect mate choice, they select partners by displaying sexually attractive traits, thus eliciting contest competition between males. We focused on a primate species in which females advertise the timing of their ovulation and studied the balance between these two choice strategies. We tested predictions related to three hypotheses about direct and indirect female choice, namely the best‐male, graded‐signal and weak‐selectivity hypotheses. We investigated the sexual and agonistic interactions occurring during oestrous periods in five captive groups of Tonkean macaques (Macaca tonkeana). The results showed that dominant males used mate guarding to monopolise sexual access to parous females that were in the fertile stage of their reproductive cycle, while lower‐ranking males monitored only nulliparous females. The distribution of sexual presentations indicated that females accepted different types of partners, supporting the weak‐selectivity hypothesis regarding direct mate choice. The analysis of behavioural sequences revealed that mate‐guarding males used mild coercive behaviours to prevent females from mating with other males at conception time. The distribution of mounts showed that females mainly mated with dominant males, which leads us to argue that the best‐male hypothesis provides the most parsimonious explanation regarding indirect mate choice in Tonkean macaques. At the individual level, it may be concluded that male competitive strategies prevented females from exercising direct mate choice. At the evolutionary level, however, female sexual advertising and thus indirect choice promoted competition between males. The outcome is that indirect mate choice appears more important than direct mate choice in female Tonkean macaques.     

Brainless but not clueless: earthworms boost their ejaculates when they detect fecund non-virgin partners

In many animals in which females store sperm, males may detect female mating status and, in order to outcompete rival sperm, increase ejaculate size when copulating with non-virgin females. Although most studies have been restricted to organisms with separate sexes, theoretical models suggest that sperm competition should also be an important selective agent shaping life-history traits in simultaneous hermaphrodites. Nevertheless, the empirical support for ejaculate adjustment in a mating opportunity is scarce in hermaphrodites. In the present study, we performed a double-mating experiment to determine whether earthworms (Eisenia andrei) detect the mating status of their partners and whether they respond by adjusting their ejaculate. We found that earthworms triplicated the donated sperm when mating with a non-virgin mate. Moreover, such increases were greater when the worms were mated with larger (more fecund) partners, indicating that earthworms perform a fine-tune control of ejaculate volume. The results of the present study suggest that, under high intensity of sperm competition, partner evaluation is subject to intense selection in hermaphrodite animals, and donors are selective about to whom they donate how much sperm.     

Conflicting intersexual mate choices maintain interspecific sexual interactions

Reproductive interference, interspecific sexual interactions that affect reproductive success, is found in various taxa and has been considered as a fundamental source of reproductive character displacement (RCD). Once RCD has occurred, persistent interspecific sexual interactions between species pairs are expected to diminish. However, reproductive interference has been reported from some species pairs that sympatrically coexist. Thus, the question arises, can reproductive interference persist even after RCD? We modeled the evolutionary dynamics of signal traits and mate recognition that determine whether interspecific sexual interactions occur. Our models incorporate male decision making based on the recognition of signal traits, whereas most previous models incorporate only female decision making in mate selection. Our models predict the following: (1) even when male decision making is incorporated, males remain promiscuous; (2) nevertheless, the frequency of interspecific mating is maintained at a low level after trait divergence; (3) the rarity of interspecific mating is due to strict female mate recognition and the consequent refusal of interspecific courtship by females; and (4) the frequency of interspecific mating becomes higher as the cost to females of refusing interspecific courtship increases. These predictions are consistent with empirical observations that males of some species engage in infrequent heterospecific mating. Thus, our models predict that reproductive interference can persist even after RCD occurred.     

Multiple paternity and postcopulatory sexual selection in a hermaphrodite: what influences sperm precedence in the garden snail Helix aspersa?

Sperm competition has been studied in many gonochoric animals but little is known about its occurrence in simultaneous hermaphrodites, especially in land snails. The reproductive behaviour of the land snail Helix aspersa involves several features, like multiple mating, long-term sperm storage and dart-shooting behaviour, which may promote sperm competition. Cryptic female choice may also occur through a spermatheca subdivided into tubules, which potentially allows compartmentalized sperm storage of successive mates. In order to determine the outcome of postcopulatory sexual selection in this species, we designed a cross-breeding experiment where a recipient ('female') mated with two sperm donors ('males'). Mates came from either the same population as the recipient or from a distinct one. To test for the influence a recipient can have on the paternity of its offspring, we excluded the effects of dart shooting by using only virgin snails as sperm donors because they do not shoot any dart before their first copulation. We measured the effects of size of mates as well as time to first and second mating on second mate sperm precedence (P2; established using microsatellite markers). Multiple paternity was detected in 62.5% of clutches and overall there was first-mate sperm precedence with a mean P2 of 0.24. Generalized linear modelling revealed that the best predictors of paternity were the time between matings and the time before first mating. Overall, both first and second mates that copulated quickly got greater parentage, which may suggest that postcopulatory events influence patterns of sperm precedence in the garden snail.     

Intra- and Intersexual Conflicts and Cooperation in the Evolution of Mating Strategies: Lessons Learnt From Ungulates

The traditional narrow focus on male mate competition in studies of mammalian mating strategies has been successful in explaining many conspicuous outcomes of sexual selection. However, focusing on ungulates, I here review increasing evidence that a comprehensive understanding of sexually selected adaptations requires consideration of a broader range of sex roles, particularly those relating to female behaviour. I show how mate competition and mate choice in both sexes can interact and often lead to intra- and intersexual conflicts and sometimes also cooperation. By causing phenotypic selection, these behavioural interactions can shape evolution although the outcome depends on genetic constraints. I conclude that to advance the understanding of mammalian mating systems we must broaden our conceptual framework from being largely focused on male competitive strategies to encompass coevolutionary dynamics between the mating strategies of both sexes. Future challenges include clarifying (1) the ecological basis for the inter- and intraspecific diversity in sex roles, (2) the condition-dependence of female mating strategies, and (3) the ultimate causes of mate competition and promiscuity in females.     

Evolution of female remating behaviour following experimental removal of sexual selection

The relatively small number of ova produced by a female can be fertilized by a single ejaculate in most species. Why females of many species mate with multiple males is therefore enigmatic, especially given that costs associated with remating have been well documented. Recently, it has been argued that females may remate at a maladaptive rate as an outcome of sexually antagonistic coevolution: the evolutionary tug-of-war between manipulation by one sex and resistance to being manipulated by the other sex. We tested this hypothesis experimentally for the evolution of the female remating interval in a naturally promiscuous species, Drosophila melanogaster. In two replicate populations, sexual selection was removed through enforced monogamous mating with random mate assignment, or retained in polyandrous controls. Monogamy constrains the reproductive success of mates to be identical, thereby converting prior conflicts between mates into opportunities for mutualism. Under these experimental conditions, the sexually antagonistic coevolution hypothesis generates explicit predictions regarding the direction of evolutionary change in female remating behaviour. These predictions are contingent upon the mechanism of male manipulation, which may be mediated biochemically by seminal fluids or behaviourally by courtship. Levels of divergence in female remating interval across lines, and in male ejaculatory and courtship effects on female remating, were quantified after 84 generations of selection. Data refute the hypothesis that the evolutionary change in female remating behaviour was due to sexually antagonistic coevolution of courtship signal and receiver traits. The data were, however, consistent with a hypothesis of sexual conflict mediated through ejaculate manipulation. Monogamy-line males evolved ejaculates that were less effective in inducing female non-receptivity and monogamy-line females evolved to remate less frequently, symptomatic of lowered resistance to ejaculate manipulation. The consistency of the results with alternative hypotheses to explain female promiscuity are discussed.     

Sexual selection and speciation in mammals,butterflies and spiders

Recently refined evolutionary theories propose that sexual selection and reproductive conflict could be drivers of speciation. Male and female reproductive optima invariably differ because the potential reproductive rate of males almost always exceeds that of females: females are selected to maximize mate 'quality', while males can increase fitness through mate 'quantity'. A dynamic, sexually selected conflict therefore exists in which 'competitive' males are selected to override the preference tactics evolved by 'choosy' females. The wide variation across taxa in mating systems therefore generates variance in the outcome of intrasexual conflict and the strength of sexual selection: monandry constrains reproductive heterozygosity and allows female choice to select and maintain particular (preferred) genes; polyandry promotes reproductive heterozygosity and will more likely override female choice. Two different theories predict how sexual selection might influence speciation. Traditional ideas indicate that increased sexual selection (and hence conflict) generates a greater diversity of male reproductive strategies to be counteracted by female mate preferences, thus providing elevated potentials for speciation as more evolutionary avenues of male-female interaction are created. A less intuitively obvious theory proposes that increased sexual selection and conflict constrains speciation by reducing the opportunities for female mate choice under polyandry. We use a comparative approach to test these theories by investigating whether two general measures of sexual selection and the potential for sexual conflict have influenced speciation. Sexual size dimorphism (across 480 mammalian genera, 105 butterfly genera and 148 spider genera) and degree of polyandry (measured as relative testes size in mammals (72 genera) and mating frequency in female butterflies (54 genera)) showed no associations with the variance in speciosity. Our results therefore show that speciation occurs independently of sexual selection.