Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator)

Reproductive skew in multimale groups may be determined by the need for alpha males to offer reproductive opportunities as staying incentives to subordinate males (concessions), by the relative fighting ability of the alpha male (tug‐of‐war) or by how easily females can be monopolized (priority‐of‐access). These models have rarely been investigated in species with exceptionally long male tenures, such as white‐faced capuchins, where female mate choice for novel unrelated males may be important in shaping reproductive skew. We investigated reproductive skew in white‐faced capuchins at Sector Santa Rosa, Costa Rica, using 20 years of demographic, behavioural and genetic data. Infant survival and alpha male reproductive success were highest in small multimale groups, which suggests that the presence of subordinate males can be beneficial to the alpha male, in line with the concession model's assumptions. None of the skew models predicted the observed degree of reproductive sharing, and the probability of an alpha male producing offspring was not affected by his relatedness to subordinate males, whether he resided with older subordinate males, whether he was prime aged, the number of males or females in the group or the number of infants conceived within the same month. Instead, the alpha male's probability of producing offspring decreased when he was the sire of the mother, was weak and lacked a well‐established position and had a longer tenure. Because our data best supported the inbreeding avoidance hypothesis and female choice for strong novel mates, these hypotheses should be taken into account in future skew models.     

Paternity in wild ring‐tailed lemurs (Lemur catta): Implications for male mating strategies

In group‐living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single‐male monopolization of paternity in groups. Ring‐tailed lemurs (Lemur catta) are seasonally breeding primates that live in multi‐male, multi‐female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra‐group males—posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wild L. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80–95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra‐troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in different L. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra‐group mating is a viable strategy that can result in extra‐group paternity for L. catta males.     

Paternity analysis of alternative male reproductive routes among the langurs (Semnopithecus entellus) of Ramnagar

Because primate males usually invest very little in offspring, male reproductive success will mainly be determined by access to fertile females with differences in access leading to differential male reproductive success. To determine the outcome of alternative male reproductive routes, we investigated a wild population of Hanuman langurs at Ramnagar, South Nepal, where groups were either one-male or multimale. Paternity was established by DNA analysis from faeces for 42 infants in five groups. In one-male groups all infants were sired by the only resident male in the group. In multimale groups the alpha male fathered significantly more infants (57%) than all other resident males. Nonresident males sired at least 21% of all infants born into multimale groups. Because of the lower mean number of infants sired by alpha males during their whole tenure as alpha compared with males in one-male groups (2.3 versus 6.8) and the higher maximum value (8.9 versus 6.0), the alpha male route is considered the riskier option. Based on demographic data we suggest that the considerable variance in short-term reproductive success might not translate to the same degree into differences in long-term reproductive success. Copyright 2001 The Association for the Study of Animal Behaviour.     

Sperm transfer and paternity in the scorpionfly <Emphasis Type="Italic">Panorpa cognata</Emphasis>: large variance in traits favoured by post-copulatory episodes of sexual selection

Post-copulatory episodes of sexual selection can be a powerful selective force influencing the reproductive success of males. In order to understand variation in male fertilisation success, we first need to consider the pattern of sperm utilisation by females following matings with more than one male. Second, we need to study those traits responsible for male success in sperm competition. Here we study both male sperm transfer characteristics as well as offspring paternity of females mated to two males in the scorpionfly Panorpa cognata. By repeatedly mating males to virgin females and interrupting copulation at defined time points, we found for all males that sperm transfer set off after approximately 40 min. During the remaining copulation, sperm transfer of individual males was continuous and with constant rate. Yet the rate of sperm transfer differed between individual males from about one sperm per minute to more than eight sperm per minute for the most successful males. In addition, we measured the fertilisation success in sperm competition of males with known sperm transfer capability. The relative number of sperm transferred by males during copulation, estimated from copulation duration and the males’ individual sperm transfer rate, explained a large proportion of variation in offspring paternity. The mode of sperm competition in this species, thus, conforms largely to a fair raffle following complete mixing of sperm prior to fertilisation. Hence, male differences in both the ability to copulate for long and of rapid sperm transfer will translate directly into differences in reproductive success.     

Male reproductive strategy and the importance of maternal status in the Antarctic fur seal Arctocephalus gazella

Abstract. Although mammalian mating systems are classically characterized in terms of male competition and polygyny, it is becoming increasingly apparent that alternative male strategies and female choice may play important roles. For example, females who mate with males from a dominant dynasty risk producing inbred offspring. Many pinnipeds are highly polygynous, but in some species alternative male strategies such as aquatic mating appear to be important, even when behavioral observations suggest strong polygyny. Here, we analyze male reproductive success in the Antarctic fur seal Arctocephalus gazella , an otariid described behaviorally as being highly polygynous, by combining a microsatellite paternity analysis spanning seven consecutive breeding seasons with detailed behavioral data on both sexes. Territorial males fathered 59% of 660 pups analyzed from our study colony. Male reproductive skew was considerable, with a quarter of all paternities assigned to just 12 top individuals on a beach where mean annual pup production was 635. Most males were successful for only a single season, but those able to return over successive years enjoyed rapidly increasing success with each additional season of tenure. We found no evidence of alternative male reproductive tactics such as aquatic or sneaky terrestrial mating. However, paternity was strongly influenced by maternal status. Females observed on the beach without a pup were significantly less likely to conceive to a sampled territorial male than equivalent females that did pup. In addition, their pups carried combinations of paternal alleles that were less likely to be found on the study beach and exhibited lower levels of shared paternity. Thus, from a territorial male's perspective, not all females offer equal opportunities for fertilization.     

Old‐male paternity advantage is a function of accumulating sperm and last‐male precedence in a butterfly

Old‐male mating advantage has been convincingly demonstrated in Bicyclus anynana butterflies. This intriguing pattern may be explained by two alternative hypotheses: (i) an increased aggressiveness and persistence of older males during courtship, being caused by the older males' low residual reproductive value; and (ii) an active preference of females towards older males what reflects a good genes hypothesis. Against this background, we here investigate postcopulatory sexual selection by double‐mating Bicyclus anynana females to older and younger males, thus allowing for sperm competition and cryptic mate choice, and by genotyping the resulting offspring. Virgin females were mated with a younger virgin (2–3 days old) and afterwards an older virgin male (12–13 days old) or vice versa. Older males had a higher paternity success than younger ones, but only when being the second (=last) mating partner, while paternity success was equal among older and younger males when older males were the first mating partner. Older males produced larger spermatophores with much higher numbers of fertile sperm than younger males. Thus, we found no evidence for cryptic female mate choice. Rather, the findings reported here seem to result from a combination of last‐male precedence and the number of sperm transferred upon mating, both increasing paternity success.     

Relatedness in wild chimpanzees: influence of paternity, male philopatry, and demographic factors

In chimpanzees (Pan troglodytes), high-ranking males are expected to have high reproductive success and females typically emigrate upon reaching maturity. Although high average relatedness among males in the same social groups has been assumed, previous reports have indicated that relatedness among males is not necessarily significantly higher than that among females. The paternity of 11 offspring and the relatedness of 50 individuals in the M group of chimpanzees at Mahale Mountains National Park, Tanzania, were investigated using DNA analyses. We determined the fathers of 10 offspring. Two different alpha males sired a total of five offspring, whereas the other males had low reproductive success. The proportion of paternal half-sibling pairs among the 10 offspring was 15.6%. The average relatedness among mature males was significantly higher than that among mature females. The existence of an old male and the long tenure of one alpha male may have contributed to this significant difference. The average dyadic relatedness among mature natal individuals was significantly higher than that in natal-immigrant pairs in which the individuals came from different groups. The average relatedness among immigrant females was similar to that in pairs of natal and immigrant females, suggesting that the immigrants came from various groups. Thus, female transfer acts to maintain low average relatedness within the group. A comparison of our results to those from other study sites suggests that although the average relatedness among adult males does not reach the level of half-siblings, under some circumstances it can exceed the relatedness of females.     

Male reproductive competition in spawning aggregations of cod (Gadus morhua, L.)

Reproductive competition may lead to a large skew in reproductive success among individuals. Very few studies have analysed the paternity contribution of individual males in spawning aggregations of fish species with huge census population sizes. We quantified the variance in male reproductive success in spawning aggregations of cod under experimental conditions over an entire spawning season. Male reproductive success was estimated by microsatellite-based parentage analysis of offspring produced in six separate groups of spawning cod. In total, 1340 offspring and 102 spawnings distributed across a spawning season were analysed. Our results show that multiple males contributed sperm to most spawnings but that paternity frequencies were highly skewed among males, with larger males on average siring higher proportions of offspring. It was further indicated that male reproductive success was dependent on the magnitude of the size difference between a female and a male. We discuss our results in relation to the cod mating system. Finally, we suggest that the highly skewed distribution of paternity success observed in cod may be a factor contributing to the low effective population size/census population size ratios observed in many marine organisms.     

Male size composition affects male reproductive variance in Atlantic cod Gadus morhua L. spawning aggregations

Estimates of Atlantic cod Gadus morhua reproductive success, determined using experimental spawning groups and genetic paternity assignment of offspring, showed that within-group variance in male size correlated positively with the degree of male mating skew, predicting a decrease in male reproductive skew with decreasing size variation among males under natural conditions.     

Male competition and paternity in wild chimpanzees of the Taï forest

In social animals, competition among males for mates affects individual reproductive success. The priority‐of‐access model attempts to account for the influence of demographic conditions within groups upon male reproductive success, but empirical data for testing this model are scarce. Our long‐term study of chimpanzees in the Taï National Park, Côte d'Ivoire, encompasses a period of steady decrease in community size and fluctuating numbers of competing males and sexually receptive females. These demographic changes, in combination with genetic assessment of paternity for 48 offspring from three communities, allowed us to quantify the effects of varying levels of competition upon male reproductive success. On average, the highest‐ranking male sired 50% of all analyzed offspring during a 14‐year period from 1987–2000. Competition among males strongly decreased the relative reproductive success of the alpha male, such that the alpha male's rate of success decreased from 67% with few competitors to only 38% with four or more competitors. The increasing number of synchronously receptive females in large groups also reduced the proportion of paternities by the alpha male. Thus, patterns of paternity in Taï chimpanzees fit well the predictions of the priority‐of‐access model. We also found that despite the inability of dominants to monopolize reproduction, they achieved a higher reproductive rate in large multimale groups, because these have more females and a higher infant survival rate. Varied levels of male competition within communities seem to explain differences in the reproductive success of alpha males observed in different chimpanzee populations, and in other primate species. Am J Phys Anthropol, 2006. © 2005 Wiley‐Liss, Inc.     

It takes two to tango: reproductive skew and social correlates of male mating success in a lek-breeding bird

Variance in reproductive success among individuals is a defining characteristic of many social vertebrates. Yet, our understanding of which male attributes contribute to reproductive success is still fragmentary in most cases. Male–male reproductive coalitions, where males jointly display to attract females, are of particular interest to evolutionary biologists because one male appears to forego reproduction to assist the social partner. By examining the relationship between social behaviour and reproductive success, we can elucidate the proximate function of coalitions in the context of mate choice. Here, we use data from a 4-year study of wire-tailed manakins (Pipra filicauda) to provide molecular estimates of reproductive skew and to test the hypothesis that male–male social interactions, in the context of coordinated displays, positively influence a male''s reproductive success. More specifically, we quantify male–male social interactions using network metrics and predict that greater connectivity will result in higher relative reproductive success. Our data show that four out of six leks studied had significant reproductive skew, with success apportioned to very few individuals in each lek. Metrics of male social affiliations derived from our network analysis, especially male connectivity, measured as the number of males with whom the focal male has extended interactions, were strong predictors of the number of offspring sired. Thus, network connectivity is associated with male fitness in wire-tailed manakins. This pattern may be the result of shared cues used by both sexes to assess male quality, or the result of strict female choice for coordinated display behaviour.     

Multiple paternity in an aggregate breeding amphibian: the effect of reproductive skew on estimates of male reproductive success

Aggregate, or explosive, breeding is widespread among vertebrates and likely increases the probability of multiple paternity. We assessed paternity in seven field-collected clutches of the explosively breeding spotted salamander (Ambystoma maculatum) using 10 microsatellite loci to determine the frequency of multiple paternity and the number of males contributing to a female's clutch. Using the Minimum Method of allele counts, multiple paternity was evident in 70% of these egg masses. Simple allele counts underestimate the number of contributing males because this method cannot distinguish multiple fathers with common or similar alleles. Therefore, we used computer simulations to estimate from the offspring genotypes the most likely number of contributing fathers given the distributions of allele frequencies in this population. We determined that two to eight males may contribute to A. maculatum clutches; therefore, multiple paternity is a common strategy in this aggregate breeding species. In aggregate mating systems competition for mates can be intense, thus differential reproductive success (reproductive skew) among males contributing to a female's clutch could be a probable outcome. We use our data to evaluate the potential effect of reproductive skew on estimates of the number of contributing males. We simulated varying scenarios of differential male reproductive success, ranging from equal contribution to high reproductive skew among contributing sires in multiply sired clutches. Our data suggest that even intermediate levels of reproductive skew decrease confidence substantially in estimates of the number of contributing sires when parental genotypes are unknown.     

Genetic analysis of the mating system and opportunity for sexual selection in northern water snakes (Nerodia sipedon)

We used data collected over 3 years at two study sites to quantifythe rates and consequences of multiple paternity and to determinethe opportunity for selection on male and female northern watersnakes (Nerodia sipedon). We sampled litters from 45 femalesthat gave birth to 811 offspring. Using eight microsatelliteDNA loci (probability of exclusion of nonparental males >0.99), we assigned paternity to 93% of neonates from one studypopulation and 69% of neonates from the other population. Observationsof participation in mating aggregations predicted individual reproductive success poorly for two reasons. First, males regularlycourted nonreproductive females. Second, more than half ofall sexually mature males obtained no reproductive successeach year, despite the fact that many of them participatedin mating aggregations. The number of sires per litter ranged from one to five, with 58% of all litters sired by more thanone male. Multiple paternity increased with female size, apparentlyboth because bigger females mated with more males and becausethe larger litters of big females provide paternity opportunitiesto more males. Multiple paternity was also more prevalent inyears with shorter mating seasons. We detected no advantage to multiple paternity in reducing either the number of unfertilizedovules or stillborn young. Despite the majority of males siringno young each year, some males fathered young with as manyas three different females in one year. Male reproductive successincreased by more than 10 offspring for each additional mate,whereas female success increased by fewer than 2 offspring foreach additional mate. The opportunity for sexual selectionwas more than five times higher in males than females.     

Reproductive strategies of rhesus macaques

Reproductive strategies incorporate a multitude of mechanisms that have evolved to promote the reproductive success of individuals. Evolutionary perspectives tend to emphasize the advantages of male-male competition and female choice as mediators of differential reproduction. Male rhesus macaques have not been observed to fight for access to sexually receptive females, although they suffer more wounds during the mating season. An increased likelihood of attacks appears to coincide with male troop entry. Males who spend more time in consort and mate with more females tend to sire more offspring. Genetic analysis of paternity has pinpointed age and endurance rivalry, rather than agonistic competition, as key variables associated with variation in progeny production. Female rhesus macaques often copulate with multiple males during their ovulatory period, and tend to conceive on the first cycle of the mating season. Female reproductive success is more likely to be a function of offspring survivorship than the identity of particular male partners. The role of female choice as a direct mediator of male reproductive success is unresolved, but female mate selection seems to indirectly affect male reproductive success because female preference for mating with novel males seems to foster male dispersal. Evaluating whether mating preferences for particular male phenotypes affectsfemale reproductive success is a task for the future. A common denominator to the reproductive strategies of both female and male rhesus macaques is that feeding patterns affect body condition which influences reproductive output and regulates relative reproductive success.     

Mate-Guarding as a Male Reproductive Tactic in <Emphasis Type="Italic">Propithecus verreauxi</Emphasis>

Sexual selection theory predicts that in group-living mammals, male reproductive tactics can lead to high reproductive skew in favor of dominant individuals. In sifakas (Propithecus verreauxi), a group-living primate with extremely seasonal reproduction, male reproductive success is highly skewed because dominant males sire almost all offspring despite a tendency toward an even adult group sex ratio. To understand the underlying behavioral mechanism resulting in this rank-related reproductive skew in male sifakas, we studied mate-guarding as a potential reproductive tactic. Behavioral observations of dominant males and adult females in combination with hormonal determination of timing of female receptivity in 9 groups at Kirindy Forest revealed that dominant males spent more time in proximity to females when they were receptive and were responsible for the maintenance of this proximity. Results also indicated that monopolization of receptive females was facilitated by both estrous asynchrony within groups and by the ability of dominant males to obtain olfactory cues as to the timing of female receptivity. Although dominant males engaging in mate-guarding are expected to experience various costs, there was no evidence for decreased foraging behavior and only a trend toward increased aggression between dominant and subordinate non-natal males within groups. Our results are in accordance with the hypothesis that dominant males use mate-guarding to monopolize receptive females and that it is one proximate mechanism that contributes to the high reproductive skew observed within the population of male sifakas at Kirindy.     

Paternity analyses in wild‐caught and laboratory‐reared Caribbean cricket females reveal the influence of mating environment on post‐copulatory sexual selection

Polyandry is ubiquitous in insects and provides the conditions necessary for male‐ and female‐driven forms of post‐copulatory sexual selection to arise. Populations of Amphiacusta sanctaecrucis exhibit significant divergence in portions of the male genitalia that are inserted directly into the female reproductive tract, suggesting that males may exercise some post‐copulatory control over fertilization success. We examine the potential for male–male and male–female post‐copulatory interactions to influence paternity in wild‐caught females of A. sanctaecrucis and contrast our findings with those obtained from females reared in a high‐density laboratory environment. We find that female A. sanctaecrucis exercise control by mating multiple times (females mount males), but that male–male post‐copulatory interactions may influence paternity success. Moreover, post‐copulatory interactions that affect reproductive success of males are not independent of mating environment: clutches of wild‐caught females exhibit higher sire diversity and lower paternity skew than clutches of laboratory‐reared females. There was no strong evidence for last male precedence in either case. Most attempts at disentangling the contributions of male–male and male–female interactions towards post‐copulatory sexual selection have been undertaken in a laboratory setting and may not capture the full context in which they take place – such as the relationship between premating and post‐mating interactions. Our results reinforce the importance of designing studies that can capture the multifaceted nature of sexual selection for elucidating the role of post‐copulatory sexual selection in driving the evolution of male and female reproductive traits, especially when different components (e.g. precopulatory and post‐copulatory interactions) do not exert independent effects on reproductive outcomes.     

Female control of the distribution of paternity in cooperative breeders

Models of reproductive skew have shed light on why animal societies vary in the partitioning of reproduction among group members. However, their application to cooperative vertebrate societies remains controversial. A particular problem is that previous models assume that skew in paternity is determined by interactions among males and males only. This conflicts with observations from many species that indicate that females exert control over the distribution of paternity. Here we address this shortfall in the current theory by developing two models to explore the expected patterns of skew in three member groups in which a female controls the allocation of paternity among two males. The first "staying incentive" model extends previous "transactional" (or "concession") models to examine the conditions where females will be willing to share reproduction among a dominant and a subordinate male to retain the subordinate in the group. The second "work incentive" model explores patterns of skew where females allocate paternity in order to maximize the amount of care their offspring receive. The models make contrasting predictions about the nature of male-female conflict over reproduction and also about the relationships between skew and relatedness, ecological constraints, the relative quality of the subordinate male, and the relative cost of care for the two males. These divergent predictions provide a schema by which the evolutionary causes of variation in skew among males can be evaluated.     

Benefits of polyandry: Molecular evidence from field‐caught dung beetles

When females mate with multiple males, they set the stage for postcopulatory sexual selection via sperm competition and/or cryptic female choice. Surprisingly little is known about the rates of multiple mating by females in the wild, despite the importance of this information in understanding the potential for postcopulatory sexual selection to drive the evolution of reproductive behaviour, morphology and physiology. Dung beetles in the genus Onthophagus have become a laboratory model for studying pre‐ and postcopulatory sexual selection, yet we still lack information about the reproductive behaviour of female dung beetles in natural populations. Here, we develop microsatellite markers for Onthophagus taurus and use them to genotype the offspring of wild‐caught females and to estimate natural rates of multiple mating and patterns of sperm utilization. We found that O. taurus females are highly polyandrous: 88% of females produced clutches sired by at least two males, and 5% produced clutches with as many as five sires. Several females (23%) produced clutches with significant paternity skew, indicating the potential for strong postcopulatory sexual selection in natural populations. There were also strong positive correlations between the number of offspring produced and both number of fathers and paternity skew, which suggests that females benefit from mating polyandrously by inciting postcopulatory mechanisms that bias paternity towards males that can sire more viable offspring. This study evaluates the fitness consequences of polyandry for an insect in the wild and provides strong evidence that female dung beetles benefit from multiple mating under natural conditions.     

Male dominance rank and reproductive success in an enclosed group of Japanese macaques: with special reference to post-conception mating

The mating behaviour and reproductive success of male Japanese macaques (Macaca fuscata) were studied in relation to the female sexual cycles, which were monitored from the plasma profiles of gonadotropins and ovarian hormones. Based on observations of the mating behaviour during four successive mating seasons and paternity identification by DNA fingerprinting in 35 out of 37 offspring born in the subsequent birth seasons, the correlations between (1) male dominance rank and timing of mating, and (2) male dominance rank and reproductive success were examined. The results may be summarized as follows. (1) The number of copulations with ejaculation by any male was positively correlated with the male dominance rank, but not with the identified numbers of offspring fathered by each male. (2) Males could not choose ovulatory females as mating partners: the number of copulations with ejaculation with females during ovulatory weeks was not related to the male's rank. Monopolized copulations in consortship were mostly observed between high-ranking males and non-lactating parous females after conception. (3) Paternity testing showed that the male copulating most frequently with a female was not the identified father in 11 out of 15 cases. Prediction of the fathers of offspring was difficult even from the number of copulations occurring at around the estimated time of ovulation. An adaptive explanation of these correlations is discussed.