Plastic male mating behavior evolves in response to the competitive environment*

Male reproductive phenotypes can evolve in response to the social and sexual environment. The expression of many such phenotypes may also be plastic within an individual's lifetime. For example, male Drosophila melanogaster show significantly extended mating duration following a period of exposure to conspecific male rivals. The costs and benefits of reproductive investment, and plasticity itself, can be shaped by the prevailing sociosexual environment and by resource availability. We investigated these ideas using experimental evolution lines of D. melanogaster evolving under three fixed sex ratios (high, medium, and low male‐male competition) on either rich or poor adult diets. We found that males evolving in high‐competition environments evolved longer mating durations overall. In addition, these males expressed a novel type of plastic behavioral response following exposure to rival males: they both significantly reduced and showed altered courtship delivery, and exhibited significantly longer mating latencies. Plasticity in male mating duration in response to rivals was maintained in all of the lines, suggesting that the costs of plasticity were minimal. None of the evolutionary responses tested were consistently affected by dietary resource regimes. Collectively, the results show that fixed behavioral changes and new augmentations to the repertoire of reproductive behaviors can evolve rapidly.     

Individual plastic responses by males to rivals reveal mismatches between behaviour and fitness outcomes

Plasticity in behaviour is of fundamental significance when environments are variable. Such plasticity is particularly important in the context of rapid changes in the socio-sexual environment. Males can exhibit adaptive plastic responses to variation in the overall level of reproductive competition. However, the extent of behavioural flexibility within individuals, and the degree to which rapidly changing plastic responses map onto fitness are unknown. We addressed this by determining the behaviour and fitness profiles of individual Drosophila melanogaster males subjected to up to three episodes of exposure to rivals or no rivals, in all combinations. Behaviour (mating duration) was remarkably sensitive to the level of competition and fully reversible, suggesting that substantial costs arise from the incorrect expression of even highly flexible behaviour. However, changes in mating duration matched fitness outcomes (offspring number) only in scenarios in which males experienced zero then high competition. Following the removal of competition, mating duration, but not offspring production, decreased to below control levels. This indicates that the benefit of increasing reproductive investment when encountering rivals may exceed that of decreasing investment when rivals disappear. Such asymmetric fitness benefits and mismatches with behavioural responses are expected to exert strong selection on the evolution of plasticity.     

Males use multiple, redundant cues to detect mating rivals

Across many species, males exhibit plastic responses when they encounter mating rivals. The ability to tailor responses to the presence of rivals allows males to increase investment in reproduction only when necessary. This is important given that reproduction imposes costs that limit male reproductive capacity, particularly when sperm competition occurs. Fruitfly (Drosophila melanogaster) males exposed to rivals subsequently mate for longer and thus accrue fitness benefits under increased competition, in line with theory. Here, we show that male D. melanogaster detect rivals by using a suite of cues and that the resulting responses lead directly to significant fitness benefits. We used multiple techniques to systematically remove auditory, olfactory, tactile, and visual cues, first singly and then in all possible combinations. No single cue alone was sufficient to allow males to detect rivals. However, the perception of any two cues from sound, smell, or touch permitted males to detect and respond adaptively to rivals through increased offspring production. Vision was only of marginal importance in this context. The findings indicate adaptive redundancy through the use of multiple, but interchangeable, cues. We reveal the robust mechanisms by which males assess their socio-sexual environment to precisely attune responses via the expression of plastic behavior.     

Plasticity in male mating behavior modulates female life history in fruit flies

In many species, intense male-male competition for the opportunity to sire offspring has led to the evolution of selfish reproductive traits that are harmful to the females they mate with. In the fruit fly, Drosophila melanogaster, males modulate their reproductive behavior based on the perceived intensity of competition in their premating environment. Specifically, males housed with other males subsequently transfer a larger ejaculate during a longer mating compared to males housed alone. Although the potential fitness benefits to males from such plasticity are clear, its effects on females are mostly unknown. Hence, we tested the long-term consequences to females from mating with males with distinct social experiences. First, we verified that competitive experience influences male mating behavior and found that males housed with rivals subsequently have shorter mating latencies and longer mating durations. Then, we exposed females every other day for 20 days to males that were either housed alone or with rivals, and subsequently measured their fitness. We found that females mated to males housed with rivals produce more offspring early in life but fewer offspring later in life and have shorter lifespans but similar intrinsic population growth rates. These results indicate that plasticity in male mating behavior can influence female life histories by altering females’ relative allocation to early versus late investment in reproduction and survival.     

Sexual conflict over mating in Gnatocerus cornutus? Females prefer lovers not fighters

Female mate choice and male–male competition are the typical mechanisms of sexual selection. However, these two mechanisms do not always favour the same males. Furthermore, it has recently become clear that female choice can sometimes benefit males that reduce female fitness. So whether male–male competition and female choice favour the same or different males, and whether or not females benefit from mate choice, remain open questions. In the horned beetle, Gnatocerus cornutus, males have enlarged mandibles used to fight rivals, and larger mandibles provide a mating advantage when there is direct male–male competition for mates. However, it is not clear whether females prefer these highly competitive males. Here, we show that female choice targets male courtship rather than mandible size, and these two characters are not phenotypically or genetically correlated. Mating with attractive, highly courting males provided indirect benefits to females but only via the heritability of male attractiveness. However, mating with attractive males avoids the indirect costs to daughters that are generated by mating with competitive males. Our results suggest that male–male competition may constrain female mate choice, possibly reducing female fitness and generating sexual conflict over mating.     

Extreme cost of rivalry in a monandrous species: male–male interactions result in failure to acquire mates and reduced longevity

Mating system variation is profound in animals. In insects, female willingness to remate varies from mating with hundreds of males (extreme polyandry) to never remating (monandry). This variation in female behaviour is predicted to affect the pattern of selection on males, with intense pre-copulatory sexual selection under monandry compared to a mix of pre- and post-copulatory forces affecting fitness under polyandry. We tested the hypothesis that differences in female mating biology would be reflected in different costs of pre-copulatory competition between males. We observed that exposure to rival males early in life was highly costly for males of a monandrous species, but had lower costs in the polyandrous species. Males from the monandrous species housed with competitors showed reduced ability to obtain a mate and decreased longevity. These effects were specific to exposure to rivals compared with other types of social interactions (heterospecific male and mated female) and were either absent or weaker in males of the polyandrous species. We conclude that males in monandrous species suffer severe physiological costs from interactions with rivals and note the significance of male–male interactions as a source of stress in laboratory culture.     

Fitness consequences of redundant cues of competition in male Drosophila melanogaster

Phenotypic plasticity can allow animals to adapt their behavior, such as their mating effort, to their social and sexual environment. However, this relies on the individual receiving accurate and reliable cues of the environmental conditions. This can be achieved via the receipt of multimodal cues, which may provide redundancy and robustness. Male Drosophila melanogaster detect presence of rivals via combinations of any two or more redundant cue components (sound, smell, and touch) and respond by extending their subsequent mating duration, which is associated with higher reproductive success. Although alternative combinations of cues of rival presence have previously been found to elicit equivalent increases in mating duration and offspring production, their redundancy in securing success under sperm competition has not previously been tested. Here, we explicitly test this by exposing male D. melanogaster to alternative combinations of rival cues, and examine reproductive success in both the presence and absence of sperm competition. The results supported previous findings of redundancy of cues in terms of behavioral responses. However, there was no evidence of reproductive benefits accrued by extending mating duration in response to rivals. The lack of identifiable fitness benefits of longer mating under these conditions, both in the presence and absence of sperm competition, contrasted with some previous results, but could be explained by (a) damage sustained from aggressive interactions with rivals leading to reduced ability to increase ejaculate investment, (b) presence of features of the social environment, such as male and female mating status, that obscured the fitness benefits of longer mating, and (c) decoupling of behavioral investment with fitness benefits.     

Receptive females mitigate costs of sexual conflict

Males typically gain fitness from multiple mating, whereas females often lose fitness from numerous mating, potentially leading to sexual conflict over mating. This conflict is expected to favour the evolution of female resistance to mating. However, females may incur male harassment if they refuse to copulate; thus, greater female resistance may increase costs imposed by males. Here, I show that the evolution of resistance to mating raises fitness disadvantages of interacting with males when mating is harmful in female adzuki bean beetles, Callosobruchus chinensis. Females that were artificially selected for higher and lower remating propensity evolved to accept and resist remating, respectively. Compared with females that evolved to accept remating, females that evolved to resist it suffered higher fitness costs from continuous exposure to males. The costs of a single mating measured by the effect on longevity did not differ among selection line females. This study indicates that receptive rather than resistant females mitigate the fitness loss resulting from sexual conflict, suggesting that even though mating is harmful, females can evolve to accept additional mating.     

Double insurance of paternity by a novel type of mating plug in a monandrous solitary mason bee Osmia bicornis (Hymenoptera: Megachilidae)

Males of some hymenopteran species are able to behaviourally induce unreceptivity to mating in females by a post‐copulatory display (post‐copulatory courtship). This method of preventing further inseminations requires a high degree of female cooperation by the female and is especially susceptible to manipulations. If mating chances are low and sexual competition between males high, males can be expected to evolve additional mechanisms to protect their fertilization opportunities. This hypothesis was checked in the red mason bee Osmia bicornis (Linnaeus, 1758; syn. Osmia rufa). Males of this species were found to use a mating plug as a reinsurance to protect their paternity, although they induce females' monandry by a post‐copulatory display. Male accessory gland secretions transferred during ejaculation form a plastic, spongy plug in the females' vagina that also contains the spermatozoa. This mating plug does not hinder rivals to mate with the female but prevents intermixing of the sperm. Thus, the sperm precedence of the first male is secured. The plug is ejected by the female after approximately 1 day when the spermatheca has been completely filled with sperm. The male accessory gland supply is sufficient for the formation of two to three plugs only and is not replenished. This pattern fits well with the low mating opportunities of O. bicornis males. The evolution of a mating plug in addition to the behavioural induction of unreceptivity to mate in females is discussed. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 28–37.     

同种雄性竞争对手的存在对星豹蛛雄蛛求偶和交配行为的影响

越来越多的研究发现,雄性产生精子(精液)也需付出代价。雄性除了依据配偶质量和竞争对手的竞争强度适应性调整生殖投入外,雄性在求偶和交配行为上也相应产生适应性反应,求偶和交配行为具有可塑性。目前雄性求偶和交配行为可塑性研究主要集中于雌性多次交配的类群中,在雌性单次交配的类群中研究甚少。以雌蛛一生只交配一次而雄蛛可多次交配的星豹蛛为研究对象,比较:(1)前一雄性拖丝上信息物质对后续雄蛛求偶和交配行为的影响,(2)雌雄不同性比对雄蛛求偶和交配行为的影响。研究结果表明,星豹蛛前一雄蛛拖丝上的信息物质对后续雄蛛求偶潜伏期、求偶持续时间和交配持续时间都没有显著影响,但前一雄蛛拖丝上的信息物质对后续雄蛛求偶强度有显著抑制作用。同时,性比对星豹蛛雄蛛求偶和交配行为都没有显著影响。可见,星豹蛛雄蛛对同种雄性拖丝上的化学信息可产生求偶行为的适应性调整,而对性比不产生适应性反应。     

Impaired sperm quality,delayed mating but no costs for offspring fitness in crickets winning a fight

The outcome of male–male contest competition is known to affect male mating success and is believed to confer fitness benefits to females through preference for dominant males. However, by mating with contest winners, females can incur significant costs spanning from decreased fecundity to negative effects on offspring. Hence, identifying costs and benefits of male dominance on female fitness is crucial to unravel the potential for a conflict of interests between the sexes. Here, we investigated males' pre‐ and post‐copulatory reproductive investment and its effect on female fitness after a single contest a using the field cricket Gryllus bimaculatus. We allowed males to fight and immediately measured their mating behaviour, sperm quality and offspring viability. We found that males experiencing a fight, independently of the outcome, delayed matings, but their courtship effort was not affected. However, winners produced sperm of lower quality (viability) compared to losers and to males that did not experience fighting. Results suggest a trade‐off in resource allocation between pre‐ and post‐mating episodes of sexual selection. Despite lower ejaculate quality, we found no fitness costs (fecundity and viability of offspring) for females mated to winners. Overall, our findings highlight the importance of considering fighting ability when assessing male reproductive success, as winners may be impaired in their competitiveness at a post‐mating level.     

The Foraging Costs of Mating Effort in Male Chimpanzees (Pan troglodytes schweinfurthii)

Costs of mating effort can affect the reproductive strategies and lifetime fitness of male primates, but interspecific and interindividual variation in the magnitude and distribution of costs is poorly understood. Male costs have primarily been recognized in seasonally breeding species that experience concentrated periods of mating competition. Here, we examine foraging costs associated with male mating effort in chimpanzees (Pan troglodytes schweinfurthii), a polygynandrous species, in which mating opportunities occur intermittently throughout the year. To quantify male feeding, aggression, and mating, we conducted focal follows on 12 males in a wild community (Kanyawara, Kibale National Park, Uganda) for 11 mo. Males fed less on days when high-value mating opportunities (estrous parous females) were available than on days without any mating opportunities. Reductions in feeding time were related to increased rates of aggression and copulation, indicating that the proximate cause of changes in male foraging was mating effort. Surprisingly, however, there was no relationship between dominance rank and the extent to which feeding time was reduced. High costs of mating effort may reduce the degree of reproductive skew and limit the use of possessive tactics in chimpanzees. We suggest that male bonding in chimpanzees may be favored not only for its benefits but because intragroup competition is so costly. Our results complement the available data on mammals, and primates in particular, by showing that mating effort can have measurable foraging costs even in species, in which breeding is aseasonal and only moderately skewed.     

The role of species‐specific sensory cues in male responses to mating rivals in Drosophila melanogaster fruitflies

Complex sets of cues can be important in recognizing and responding to conspecific mating competitors and avoiding potentially costly heterospecific competitive interactions. Within Drosophila melanogaster, males can detect sensory inputs from conspecifics to assess the level of competition. They respond to rivals by significantly extending mating duration and gain significant fitness benefits from doing so. Here, we tested the idea that the multiple sensory cues used by D. melanogaster males to detect conspecifics also function to minimize “off‐target” responses to heterospecific males that they might encounter (Drosophila simulans, Drosophila yakuba, Drosophila pseudoobscura, or Drosophila virilis). Focal D. melanogaster males exposed to D. simulans or D. pseudoobscura subsequently increased mating duration, but to a lesser extent than following exposure to conspecific rivals. The magnitude of rivals’ responses expressed by D. melanogaster males did not align with genetic distance between species, and none of the sensory manipulations caused D. melanogaster to respond to males of all other species tested. However, when we removed or provided “false” sensory cues, D. melanogaster males became more likely to show increased mating duration responses to heterospecific males. We suggest that benefits of avoiding inaccurate assessment of the competitive environment may shape the evolution of recognition cues.     

Male Age and Experience Increases Mating Success but Not Female Fitness in the Mexican Fruit Fly

Male age and sexual experience are important condition parameters that can influence mate choice and female fitness, yet they are seldom studied simultaneously. Here, we investigated the effect of male age and previous sexual experience on mating success and female fitness in the Mexican fruit fly, Anastrepha ludens (Diptera: Tephritidae). Males were either young or old, sexually experienced or naïve. Older and sexually experienced males obtained more copulations. However, females did not receive benefits in terms of lifetime fecundity, fertility, or longevity from mating with these males. Results suggest that males become more competitive as they age and gain sexual experience and may be able to maintain a high quality ejaculate compared to young males. Older experienced males may be manipulating females into preferentially mating with them at no benefit to females. Alternatively, females may prefer mating with older more experienced males and possibly receive other indirect benefits, but this remains to be tested.     

Costly sexual harassment in a beetle

Abstract The optimal number of mating partners for females rarely coincides with that for males, leading to sexual conflict over mating frequency. In the bruchid beetle Callosobruchus maculatus, the fitness consequences to females of engaging in multiple copulations are complex, with studies demonstrating both costs and benefits to multiple mating. However, females kept continuously with males have a lower lifetime egg production compared with females mated only once and then isolated from males. This reduction in fitness may be a result of damage caused by male genitalia, which bear spines that puncture the female’s reproductive tract, and/or toxic elements in the ejaculate. However, male harassment rather than costs of matings themselves could also explain the results. In the present study, the fitness costs of male harassment for female C. maculatus are estimated. The natural refractory period of females immediately after their first mating is used to separate the cost of harassment from the cost of mating. Male harassment results in females laying fewer eggs and this results in a tendency to produce fewer offspring. The results are discussed in the context of mate choice and sexual selection.     

Sex-specific spatio-temporal variability in reproductive success promotes the evolution of sex-biased dispersal

Inbreeding depression, asymmetries in costs or benefits of dispersal, and the mating system have been identified as potential factors underlying the evolution of sex-biased dispersal. We use individual-based simulations to explore how the mating system and demographic stochasticity influence the evolution of sex-specific dispersal in a metapopulation with females competing over breeding sites, and males over mating opportunities. Comparison of simulation results for random mating with those for a harem system (locally, a single male sires all offspring) reveal that even extreme variance in local male reproductive success (extreme male competition) does not induce male-biased dispersal. The latter evolves if the between-patch variance in reproductive success is larger for males than females. This can emerge due to demographic stochasticity if the habitat patches are small. More generally, members of a group of individuals experiencing higher spatio-temporal variance in fitness expectations may evolve to disperse with greater probability than others.     

The sexual selection paradigm: have we overlooked other mechanisms in the evolution of male ornaments?

Extravagant male ornaments expressed during reproduction are almost invariably assumed to be sexually selected and evolve through competition for mating opportunities. Yet in species where male reproductive success depends on the defence of offspring, male ornaments could also evolve through social competition for offspring survival. However, in contrast to female ornaments, this possibility has received little attention in males. We show that a male ornament that is traditionally assumed to be sexually selected—the red nuptial coloration of the three-spined stickleback—is under stronger selection for offspring survival than for mating success. Males express most coloration during parenting, when they no longer attract females, and the colour correlates with nest retention and hatching success but not with attractiveness to females. This contradicts earlier assumptions and suggests that social selection for offspring survival rather than for sexual selection for mating success is the main mechanism maintaining the ornament in the population. These results suggest that we should consider other forms of social selection beyond sexual selection when seeking to explain the function and evolution of male ornaments. An incorrect assignment of selection pressures could hamper our understanding of evolution.     

Is Fatter Sexier? Reproductive Strategies of Male Squirrel Monkeys (Saimiri sciureus)

Sexually dimorphic traits can evolve through male–male competition or female choice. Squirrel monkeys (genus Saimiri) live in large multimale, multifemale groups and are seasonal breeders with concealed ovulation. In several species of the genus, females are dominant to males. Males show weight gain preceding and during the mating season, which produces a “fattened” appearance in the upper arms, shoulders, and torso. Although much is known about the physiology of fattening, the evolutionary function(s) of this sexually dimorphic trait, including possible benefits and costs, remain(s) unknown. This unusual reproductive physiology of males is suggestive of sexual selection. Here I present data on wild Saimiri sciureus studied in Brazil to describe male reproductive investment in the species and to examine the hypothesis that male fattening is a product of sexual selection. I observed at least nine adult males via focal animal sampling and ad libitum observations during four mating seasons and during an additional 10 nonbreeding season months for comparison. Compared to less robust males, fatter males spent significantly more time near females and less time alone. These males also spent more time engaged in sociosexual activities and less time feeding/foraging, suggesting a trade-off between maintenance and reproductive behaviors. The 2-mo mating season accounted for 62% of all male–male agonism observed over one 12-mo period. These results are suggestive of male–male competition for females. However, males did not coerce females to mate and females often rejected males; this pattern suggests female choice. It is possible that male fattening in Saimiri is a product of both intra- and intersexual selection. Males experience intense reproductive costs related to agonism with other males, and related to time and energy invested in the pursuit of females. Although fattening may mitigate some of these costs by aiding in male–male competition and in female preference, this phenomenon is likely not without physiological costs to adult males.     

Lifetime Number of Mates Interacts with Female Age to Determine Reproductive Success in Female Guppies

In many species, mating with multiple males confers benefits to females, but these benefits may be offset by the direct and indirect costs associated with elevated mating frequency. Although mating frequency (number of mating events) is often positively associated with the degree of multiple mating (actual number of males mated), most studies have experimentally separated these effects when exploring their implications for female fitness. In this paper I describe an alternative approach using the guppy Poecilia reticulata, a livebearing freshwater fish in which females benefit directly and indirectly from mating with multiple males via consensual matings but incur direct and indirect costs of mating as a consequence of male sexual harassment. In the present study, females were experimentally assigned different numbers of mates throughout their lives in order to explore how elevated mating frequency and multiple mating combine to influence lifetime reproductive success (LRS) and survival (i.e. direct components of female fitness). Under this mating design, survival and LRS were not significantly affected by mating treatment, but there was a significant interaction between brood size and reproductive cycle (a correlate of female age) because females assigned to the high mating treatment produced significantly fewer offspring later in life compared to their low-mating counterparts. This negative effect of mating treatment later in life may be important in these relatively long-lived fishes, and this effect may be further exacerbated by the known cross-generational fitness costs of sexual harassment in guppies.     

Exposure to Odors of Rivals Enhances Sexual Motivation in Male Giant Pandas

Males will alter their mating behavior to cope with the presence of their competitors. Even exposure to odors from potential competitors can greatly increase male ejaculate expenditure in a variety of animals including insects, fishes, birds and rodents. Major efforts have been made to examine males'' plastic responses to sperm competition and its fitness benefits. However, the effects of competitor absence on male''s sexual motivation and behaviors remain unclear, which has been proposed to be one of the causes for the poor sexual performance of some captive mammals. This study revealed that sexual motivation can be greatly enhanced in captive male giant pandas (Ailuropoda melanoleuca) by exposure to chemosensory cues from either one or three conspecifics males. It had been shown that potential rivals'' odors increased males'' chemosensory investigation behavior, as well as their observing, following and sniffing behaviors towards estrous females. Behaviors changed regardless of the number of rivals (one or three). Our results demonstrate the effects of potential competition on male giant pandas'' sexual motivation and behavioral coping strategy. We anticipate that our research will provide a fresh insight into the mechanisms underlying poor sexual performance in male captive mammals, and valuable information for the practical management and ex situ conservation of endangered species.