Mating effort and female receptivity: how do male guppies decide when to invest in sex?

Males vary in the degree to which they invest in mating. Several factors can explain this variation, including differences in males’ individual condition and the fact that males allocate their energy depending on the context they face in each mating attempt. Particularly, female quality affects male reproductive success. Here, we studied whether male guppies (Poecilia reticulata) strategically allocated more mating effort, in terms of mating behaviour and male–male competition, when they were matched with a receptive (R) female than a non-receptive one. In accordance with our prediction, we found that males increased their mating behaviour when they were with a receptive female. Even though male guppies can inseminate non-receptive females, we only found high levels of courtship between males that were with a receptive female rather than a non-receptive one. Although there was little affect of female receptivity on male–male competition, we found that males chased and interrupted courtships more with receptive females than with non-receptive females regardless of odour. Finally, we also studied whether the sexual pheromone produced by receptive female guppies is a cue that males use in order to increase their mating effort. We found that males were more attracted to a female when they perceived the sexual pheromone, but only increased their mating and aggressive behaviours when females showed receptive behaviour. This strategic increase in mating effort could result in higher male reproductive success because mating attempts towards receptive females are likely to be less costly and males could have a greater probability of fertilisation.     

Determinants of paternity success in the spider Pholcus phalangioides (Pholcidae: Araneae): the role of male and female mating behaviour

In double mating experiments, we examined whether and to what extent various male and female behavioural traits influence the course of mating and fertilization success in the cellar spider. In males, we focussed on pre-copulatory behaviour and on the rhythmic twisting movements that the male performs with his pedipalps during copulation. In females, we investigated remating decisions and the effect of female termination of copulation. Second males fertilized a high proportion of the eggs (P ₂: median 89%) despite much shorter second matings, with high variation in relative paternity success. The number of pedipalp movements (PPMs) of either male was a better predictor of paternity than copulation duration. Our results suggest that in second matings, PPMs help to remove sperm from previous males, whereas in first matings a high number of PPMs enhances fertilization success, either due to numerical sperm competition or cryptic female choice. Furthermore, we found a negative male age effect on paternity in second matings, implying that age-related deterioration of spermatozoa may promote variation in fertilization success. Female receptivity decreased significantly in second matings; only 70% of the females remated. Females that accepted a second copulation were found to terminate these much earlier and with higher probability than first matings. This suggests that the intensity of conflict between the sexes is higher in second matings. Increased intensity of sexual conflict may be responsible for stronger selection on male traits, as pre-copulatory behaviour and age only affected male copulatory performance and paternity in second matings. Electronic Publication     

Sexual selection and female fitness in <Emphasis Type="Italic">Drosophila simulans</Emphasis>

There is a current debate over the net fitness consequences of sexual selection. Do preferred males increase female fitness or are these males manipulating females for their own benefit? The evidence is mixed. Some studies find that mating with attractive males increases female fitness components, while others show that preferred males decrease measures of female fitness. In this study, we examined some of the fitness consequences of pre-copulatory sexual selection in Drosophila simulans. Virgin females were either paired with one male and given an opportunity for one copulation or were exposed simultaneously to two males. This allowed us to compare female preference (copulation latency) and fitness (longevity, lifetime productivity and rate of offspring production) both with and without the influence of male–male competition. When females had access to a single male, neither female longevity, productivity, nor short-term rate of productivity were associated with female preference, and although females mated more quickly with larger males, male size was also not associated with any female fitness measure. Inclusion of male–male competition showed that female longevity was negatively affected by preference, while productivity and rate of productivity was unaffected. This latter experiment also indicated that females preferred larger males, but again, male size was not associated with female fitness. These results indicate that females may not benefit from mating with preferred males, but they may incur survival costs.     

Predation risk reduces male-male sexual competition in the Trinidadian guppy (Poecilia reticulata)

Because agonistic behaviour can increase an individual's risk of predation, natural selection should favour individuals that modify their behaviour in the face of predation hazard in ways that maximise fitness. We investigated experimentally the effects of an increase in the apparent risk of predation on male-male competition within mixed-sex shoals of the Trinidadian guppy (Poecilia reticulata). We show that males engaged in significantly fewer aggressive interactions with conspecific males in the presence of a fish predator. However, they continued to court and attempt copulations with females at the same rate irrespective of the level of predation risk. In comparison, under predation hazard, female guppies were less responsive sexually and avoided fewer male copulation attempts. Such predator-mediated changes in male-male agonistic interactions and female sexual responsiveness towards males have important implications for the mode and intensity of sexual selection within populations.     

Effects of extreme variation in female morph frequencies on the mating behaviour of male damselflies

Female-limited polymorphism is often attributed to selection to avoid excessive male mating attempts. It is encountered in various taxonomic groups, but is particularly common in damselflies, where one female morph (andromorph) typically resembles the conspecific male in colour pattern, while the other(s) (gynomorph(s)) do not. Two sets of theories have been proposed to explain the phenomenon in damselflies, which can be classified as the learned mate recognition (LMR) and male mimicry (MM) hypotheses. To test predictions of these hypotheses, we evaluated the rate of male sexual response towards female morphs and conspecific males in the damselfly Nehalennia irene. The LMR hypothesis predicts that males should respond sexually to andromorphs at greater rates in populations containing a higher relative frequency of andromorphs. The MM hypothesis predicts that males respond more often sexually to both andromorphs and males as the ratio of andromorphs to males increases. While LMR predicts that the rate of mating attempts towards gynomorphs should vary, the MM predicts that it should be relatively fixed. On experimentally presenting live specimens to focal males in five different populations with extreme variation in female morph frequencies, we observed that as the andromorph frequency and ratio of andromorphs to males increased, the proportion of male mating attempts increased on both andromorphs and males, whereas it decreased on gynomorphs. While the simplest form of the MM hypothesis is rejected, the results support specific predictions of both hypotheses and suggest that future studies should not treat these hypotheses as mutually exclusive.     

Investment in mate choice depends on resource availability in female Galápagos marine iguanas (<Emphasis Type="Italic">Amblyrhynchus cristatus</Emphasis>)

Changes in mate selectivity can significantly alter the direction and strength of sexual selection. When the direct cost of mate search increases selectivity often declines; however, little is known about how the relative cost of mate search affects investment in mate choice. Here, I investigate whether male and female Galápagos marine iguanas (Amblyrhynchus cristatus) alter their investment in mate choice behaviors when resources are limited and the relative cost of mate search is increased. Moderate resource limitation had little effect on male reproductive behavior: in both years, a similar number of males were territorial, and the mean display rate and copulation success of territorial males did not differ. In contrast, female mate search appeared to be affected by the prevailing environmental conditions. During the reproductive season following a moderate El Niño event, when food availability declined, females were in poorer body condition, assessed fewer territorial males, and mated with a male with lower relative reproductive success. Circulating hormone levels also differed between years: when resource availability was limited, receptive females had higher levels of testosterone and stress-induced corticosterone. The frequency and magnitude of climatic fluctuations are expected to increase in the future across many regions of the globe. Determining how sexual selection is shaped by changes in resource availability is vital for predicting the impact of climate change.     

Information content of female copulation calls in wild long-tailed macaques (<Emphasis Type="Italic">Macaca fascicularis</Emphasis>)

Primates are unusual in that many females display sexual signals, such as sex skin swellings/colorations and copulation calls, without any sex role reversal. The adaptive function of these signals remains largely unclear, although it has been suggested that they provide males with information on female reproductive status. For sex skin swellings, there is increasing evidence that they represent a graded signal indicating the probability of ovulation. Data on the functional significance of copulation calls are much scarcer. To clarify the information content of such calls, we recorded copulation calls in wild long-tailed macaques (Macaca fascicularis) and analysed the structure of these calls during the ovarian cycle. Specifically, we correlated selected call parameters with the female oestrogen to progestogen ratio (obtained from faecal samples), which are known to be elevated during the female's fertile phase. In addition, we ran a general linear mixed model for these call parameters, testing factors (cycle phase, occurrence/absence of ejaculation, male dominance status, occurrence/absence of mate guarding) which potentially influence female copulation calls in primates. Our results show that copulation calls of female long-tailed macaques signal mating outcome and rank of the mating partner, but not female reproductive status. They also show for the first time on primates that copulation calls can convey information on whether a female is mate guarded or not. We suspect that the function of these calls is manipulation of male mating and mate-guarding behaviour and that in this way the degree of sperm competition and ultimately male reproductive success is influenced.     

Influence of male harassment and female competition on female feeding behaviour in a sexual–asexual mating complex of mollies (<Emphasis Type="Italic">Poecilia mexicana</Emphasis>, <Emphasis Type="Italic">P. formosa</Emphasis>)

Differential interests between the sexes regarding the number of copulations can result in sexual harassment. Hence, females may have less time available for foraging. Male sexual harassment often leads to fitness reduction in females. We used the mating complex of the bisexual fish Poecilia mexicana and the co-occurring all-female Poecilia formosa to study sexual harassment and its incurred cost on female feeding efficiency. P. formosa is a sperm-dependent parthenogen that requires mating with host males to induce embryogenesis, but the male genes are not used. We therefore predicted P. mexicana males to prefer conspecific females. Hence, costs of male sexual harassment should not occur in unisexuals. While P. formosa are at a disadvantage compared to P. mexicana females due to male mate choice (leading to sperm limitation), this could be traded-off by suffering less from sexual harassment. In our experiment, we found males to direct significantly more pre-copulatory mating behaviour towards conspecific females, whereas actual mating attempts did not differ between species. Contrary to our prediction, both types of females started feeding later and spent less time feeding in the presence of a male partner compared to the time spent feeding with another female, suggesting that females of both species suffer from male harassment. The focal females' feeding time declined with increasing body size of the female competitor, and the same pattern was found when a male was present. We discuss that—besides sexual harassment—other factors such as food competition and female mate choice may affect female feeding efficiency.     

Experience counts: females favor multiply mated males over chemically endowed virgins in a moth (<Emphasis Type="Italic">Utetheisa ornatrix</Emphasis>)

Determining the factors that affect male mating success is essential to understanding how sexual selection operates, including explanations of the adaptive value of female preferences and how variation in male traits is maintained in a population. Although females may appear to choose males based on a single parameter, female mate choice is often a complex series of assessments of male quality that can only be revealed through manipulation of multiple male traits. In the moth Utetheisa ornatrix (Lepidoptera: Arctiidae), females have been shown to judge males primarily on their production of a courtship pheromone, hydroxydanaidal, derived from defensive chemicals acquired as larvae. Recent work, however, suggested that other factors, including prior mating experience by males, may also influence the outcome of precopulatory interactions with females. I ran mating trials with one female and two males to determine whether there were any differences in male mating success based on their prior exposure to females, mating experience, and time between matings. Previously mated males were favored over virgins when both males lacked the pheromone, but courting experience and mating interval did not explain these differences in male mating success. Furthermore, multiply mated males lacking the pheromone were favored over virgin males that produced the pheromone, thus reversing the commonly observed trend of female precopulatory bias towards males with higher levels of the pheromone. These results demonstrate that males with mating experience can secure copulations despite deficiencies in the pheromone, and I provide possible mechanisms and discuss their implications regarding sexual selection.     

The evolution of female copulation calls in primates: a review and a new model

Female copulation calls are mating-associated vocalizations that occur in some species of Old World monkeys and apes. We argue that copulation calls have two immediate functions: to encourage mating attempts by other males and to increase mate guarding by the consort male. We hypothesize that female copulation calls have evolved under the selective pressures of risk of infanticide and sperm competition. When male mate guarding is effective, copulation calls allow females to concentrate paternity in dominant males and benefit from their protection against the risk of infanticide. When mate guarding is ineffective, copulation calls may bring genetic benefits to females through facilitation of sperm competition. We present a quantitative model in which interspecific variation in females' promiscuity predicts their tendency to use copulation calls in conjunction with mating. The model predicts that in species with little female promiscuity, copulation calls should be rare and exhibited only in association with mating with dominant males. In species in which females are highly promiscuous, copulation calls should be frequent and unrelated to male dominance rank. The limited data available to test the model support its main predictions as well as the predicted relation between copulation calls and male dominance rank.

Male genital length and mating status differentially affect mating behaviour in an earwig

Phenotypic variation in male genitalia may affect copulation behaviour, which can have important fitness consequences for males. Male genitalia commonly possess traits that increase male control over copulation, but in species where females control mating, a poor functional understanding often prevents insight into the processes responsible for such effects. Here, I investigate the effect of male genital length on copulation behaviour in the earwig Euborellia brunneri, where both sexes exhibit extremely elongated genitalia that correspond in shape. This model system is particularly suitable because pairs mate repeatedly and females can limit both the number and duration of copulations. I used both virgin and mated males and females in a double-mating design because longer male genitalia confer benefits in sperm competition. Consistent with a greater predicted male mating effort in mated females, the duration of individual copulations increased, but this traded off against mating frequency as cumulative mating duration remained unchanged. In contrast, male genital length increased both individual and cumulative mating duration, regardless of mating status. This difference suggests that, while males may modify copulation duration in response to mating status, females facultatively adjust mating frequency to prevent mating excessively or express preferences for increased male genital length. Notably, this study demonstrates that male genital phenotypes that are successful in sperm competition also enjoy female-mediated mating benefits.     

Correlates of male mating success in great bustard leks: the effects of age, weight, and display effort

We examined how mating success varied in relation to age, weight, body size, and display behavior among great bustard Otis tarda males. The estimated mating success was strongly skewed, with 45% of adult males being involved in copulation attempts and only 9.7% actually seen copulating successfully. Unlike most birds, body size continued increasing in great bustards several years after reaching sexual maturity. Age, weight, and display effort were all significant and independent predictors of male mating success. The higher display effort involved performing longer full-display bouts. Older males could detach from the male flock earlier in the season as well as on each day and spend longer seasonal and daily periods displaying as solitary birds, which contributed to increase their mating success. In contrast, males weighing more did not invest more in display, which suggests that they could be recognized as dominants by other males and selected by females through assessment of their plumage sexual traits. In contrast to most other bird species, the system described for great bustards resembles that found in some lek-mating ungulates, where social rank is a complex trait determined by both age and mass, and as in these mammals, it suggests that sexual selection continues to favor a high male weight in this extremely sexually dimorphic species.     

Female tactics to reduce sexual harassment in the Sumatran orangutan (Pongo pygmaeus abelii)

Orangutan males demonstrate intrasexual dimorphism with corresponding alternative mating strategies. Sexual harassment is the predominant feature of the mating strategy that subadult males pursue. This study investigated the countertactics that females employ to reduce sexual harassment by subadult males. I observed 207 copulations during more than 9,000 h of focal follows of wild Sumatran orangutans at the Suaq Balimbing Research Station over a 23-month period. Rates of copulations initiated by subadult males increased during months of high fruit abundance, and most mating attempts were directed toward females with weaned infants. Simultaneous harassment by multiple subadult males increased significantly during months of high fruit abundance, and nearly all adult female-adult male consortships occurred during periods of high fruit abundance. Females who maintained spatial association with adult males, either via consortship or by nonmating temporary parties, received lower rates of harassment, as measured by the success rate of subadult male mating attempts. Adult female-adult male parties did not always result in mating between the associating dyad. Female initiation of protective services by adult males is one social tactic that female orangutans employ to reduce sexual harassment. Females therefore receive direct services from adult males, which may be one factor that influences female mate choice in Sumatran orangutans.     

Sperm removal and ejaculate size correlate with chelae asymmetry in a freshwater crayfish species

Asymmetry in traits of sexual relevance may impair copulation behaviour and sexual performance of males, ultimately resulting in a fitness cost. Freshwater crayfish males use chelae, a sexually selected trait, to secure and position the female prior to and during mating. Thus, a relatively large chelae asymmetry, resulting from accidental loss and regeneration of one cheliped after autotomy, could have great consequences for male sexual behaviour. We studied copulatory behaviour and sperm expenditure of males paired to a mated female in Austropotamobius italicus, a freshwater crayfish species where both male and female mate multiply and where last-mating males are able to actively remove previously deposited sperm. We aimed at assessing whether male sperm removal and expenditure varied according to sperm allocated by first-mating males, and according to copulation behaviour and phenotypic traits (carapace length, chelae length and relative chelae asymmetry) of second-mating males. Second-mating males did not adjust their ejaculate size in relation to first-mating male ejaculate, nor to the first-mating male’s sperm removed. Moreover, the amount of sperm removed by second-mating males increased with increasing first-mating males ejaculate size, and first-mating male sperm remaining after removal did not correlate with the original first-mating male ejaculate size. Interestingly, the amount of sperm removed by second-mating males decreased with increasing relative chelae asymmetry, while increasing with male body size. However, second-mating (but not first-mating) asymmetric-clawed males produced larger ejaculates than symmetric-clawed ones. Importantly, the proportion of second-mating male sperm remaining after the two matings did not vary with relative chelae asymmetry nor with body size of second-mating males. Thus, small, asymmetric-clawed crayfish males appear to adopt sperm allocation tactics that allow them to fully compensate for their inferior sperm removal ability.     

Sexual coercion by male chimpanzees shows that female choice may be more apparent than real

The extent to which active female mating preferences influence male reproductive success in mammals is unclear, particularly for promiscuously breeding species like chimpanzees (Pan troglodytes). Previous studies from multiple long-term study sites have shown that female chimpanzees mate more restrictively around ovulation, and this has been taken as evidence for female choice. However, none of these studies rigorously evaluated the alternative hypothesis that restrictive mating results not from unconstrained choice, but in response to coercive mate guarding, in which males use punishment and intimidation to reduce female promiscuity and promote their own mating interests. Nor did they consider evidence for the potential genetic or phenotypic benefits that females might be choosing. Using 11 years of data from the Kanyawara community in Kibale National Park, Uganda, we previously demonstrated that males achieve elevated mating success with those females toward whom they direct high levels of aggression. Here we extend those findings to show that even female copulatory approaches, which have previously been attributed to female choice, are correlated with male aggression. Specifically, individual females at our site initiated periovulatory copulations most frequently with the males who were most aggressive toward them throughout their cycles. Those males showed high rates of aggression toward females throughout estrus, despite achieving high copulation rates, demonstrating a continuing conflict of interest over the exclusivity of mating access. Because sexual coercion is potentially widespread in primates and other mammals, our results stress the importance of considering the influence of male aggression in studies of female choice.     

The effects of male and female genotype on variance in male fertilization success in the red flour beetle (<Emphasis Type="Italic">Tribolium castaneum</Emphasis>)

The number of eggs fertilized by a male at any given copulation (fertilization success) is affected by a large number of factors. Male insemination and sperm competition success and various female structures and/or processes that bias paternity in favor of some males over others (cryptic female choice) are all likely to affect fertilization success. We suggest that more comprehensive measures of male fertilization success can increase our understanding of postcopulatory sexual selection. To improve our understanding of the importance of various sources of variance in male fertilization success, we conducted a series of experiments using flour beetles. Different wild-type strains were used in reciprocal double mating experiments, against a phenotypic marker strain. We assessed the relative effects of female genotype, male genotype and mating order on independent and inclusive measures of male defense ability ( P ₁), male offense ability ( P ₂), and female remating behavior. Female genotype influenced both P ₁ and P ₂, and male genotype interacted strongly with female genotype in its effect on P ₂. We also documented an interaction between female and male genotypes in the effects of mating on female remating behavior, such that females tended to remate most rapidly when mated to males of their own genotype. It is clear from our experiments that cryptic female choice influences the pattern of fertilization success in flour beetles, and we suggest that cryptic female choice may often be an important component of postcopulatory sexual selection. Future investigations would benefit from studying the multiple components of variance in male fertilization success.     

Male remating and female fitness in the wolf spider Pardosa astrigera: the role of male mating history

Although the effects of male mating history on female reproductive output and longevity have been studied in insects, few such studies have been carried out in spiders. In a mating system in which females are monandrous while males are polygynous, females may incur the risk by mating with successful males that have experienced consecutive matings and suffer from the possible depletion of sperm and/or associated ejaculates. Here, we examine the effects of male mating history on male courtship and copulation duration, female reproductive fitness, and female adult longevity of the wolf spider, Pardosa astrigera. Results indicated that male mating frequency had little effect on their subsequent copulation success, and of 35 males tested, about half of the males were able to copulate with five virgin females successively at an interval of 24 h. Male mating history had little effect on their courtship duration. However, male mating history significantly affected male copulation duration, female adult longevity, and reproductive output. Males that mated more frequently copulated longer and more likely failed to cause their mates to produce a clutch, although there was no significant difference in the number of eggs laid and the number of eggs hatched regardless of the first clutch or the second one. Multiple mating of male P. astrigera resulted in significant reduction in female adult longevity. Our results indicate that monandrous females mating with multiple-mated males may incur substantial fitness costs.     

Mate quality,not aggressive spillover,explains sexual cannibalism in a size-dimorphic spider

Sexual cannibalism particularly before mating is costly for the male victim but also for the female aggressor if she risks remaining unmated. The aggressive spillover hypothesis explains the persistence of this behavior as a maladaptive side effect of positive selection on aggressiveness in a foraging context. The hypothesis predicts that the occurrence of sexual cannibalism is explained by female aggressiveness but is not related to male phenotype or behavioral type. An alternative hypothesis invokes sexual selection and makes the opposite prediction namely that sexual cannibalism is an expression of female choice and should hence mainly target males of low quality. We tested the above hypotheses on a sexually dimorphic nephilid spider Nephilengys livida, known for male monopolization of females via genital damage, female genital plugging, and mate guarding, by staging mating trials during which we recorded mating behaviors and occurrences of pre- and postcopulatory cannibalism. We did not restrict assessment of aggressiveness to the mating and foraging context but also included aggression against same sex conspecifics. To assess female personalities, i.e., consistent individual differences in behavior including aggressiveness, we repeatedly tested them for intra-sex aggression, voracity towards prey, locomotory activity, and boldness. Females exhibited consistent differences in intra-sex aggressiveness, latency to attack prey, and boldness. Aggressive females had shorter latencies to attack prey and were more active than non-aggressive ones. In contrast to the predictions of the aggressive spillover hypothesis, females that were aggressive towards prey and towards other females were not more likely to attack a male than non-aggressive females. In support of the mate choice hypothesis, less aggressive males were more likely attacked and cannibalized than more aggressive ones. This hints at sexual selection for aggressiveness in males and raises the question of mechanisms that maintain variation in male aggressiveness.     

Fitness consequences of sexual cannibalism in female<Emphasis Type="Italic"> Argiope bruennichi</Emphasis>

The evolution of sexual cannibalism as the most extreme form of nuptial feeding is still poorly understood. Although increasing evidence suggests that female aggressiveness is related to other aspects of foraging behaviour, it is not clear whether the nutritional value of a male is sufficient to provide an adaptive significance for sexual cannibalism. A widely cited though rarely tested explanation is based on a paternal investment model, and predicts that consumption of a male results in increased female fecundity. The available evidence is either correlational or restricted to species with relatively large and potentially nutritious males, and different studies have come to different conclusions. Here we present a test of the paternal investment hypothesis using the very cannibalistic and highly size-dimorphic spider Argiope bruennichi. After a preset schedule, we had females consume none, one or two males independent of the female's cannibalistic behaviour. Consumption of male bodies did not result in any detectable fitness benefit for the female: neither the number of clutches, nor clutch size or hatching success were affected by consumption of males. The frequency of cannibalism was around 80%, independent of the female mating status. We did not observe male complicity, but cannibalism was associated with prolonged copulation. This suggests a sexually selected benefit of cannibalism for males. We conclude that the paternal investment hypothesis does not explain the existence of sexual cannibalism in A. bruennichi and probably not in other spider species with a pronounced sexual size dimorphism.Communicated by L. Simmons     

Pre-copulatory sexual selection in the cigarette beetle Lasioderma serricorne

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