Kin encounter rate and inbreeding avoidance in canids

Mating with close kin can lead to inbreeding depression through the expression of recessive deleterious alleles and loss of heterozygosity. Mate selection may be affected by kin encounter rate, and inbreeding avoidance may not be uniform but associated with age and social system. Specifically, selection for kin recognition and inbreeding avoidance may be more developed in species that live in family groups or breed cooperatively. To test this hypothesis, we compared kin encounter rate and the proportion of related breeding pairs in noninbred and highly inbred canid populations. The chance of randomly encountering a full sib ranged between 1-8% and 20-22% in noninbred and inbred canid populations, respectively. We show that regardless of encounter rate, outside natal groups mates were selected independent of relatedness. Within natal groups, there was a significant avoidance of mating with a relative. Lack of discrimination against mating with close relatives outside packs suggests that the rate of inbreeding in canids is related to the proximity of close relatives, which could explain the high degree of inbreeding depression observed in some populations. The idea that kin encounter rate and social organization can explain the lack of inbreeding avoidance in some species is intriguing and may have implications for the management of populations at risk.     

The inbreeding strategy of a solitary primate,Microcebus murinus

Inbreeding depression may be common in nature, reflecting either the failure of inbreeding avoidance strategies or inbreeding tolerance when avoidance is costly. The combined assessment of inbreeding risk, avoidance and depression is therefore fundamental to evaluate the inbreeding strategy of a population, that is how individuals respond to the risk of inbreeding. Here, we use the demographic and genetic monitoring of 10 generations of wild grey mouse lemurs (Microcebus murinus), small primates from Madagascar with overlapping generations, to examine their inbreeding strategy. Grey mouse lemurs have retained ancestral mammalian traits, including solitary lifestyle, polygynandry and male‐biased dispersal, and may therefore offer a representative example of the inbreeding strategy of solitary mammals. The occurrence of close kin among candidate mates was frequent in young females (~37%, most often the father) and uncommon in young males (~6%) due to male‐biased dispersal. However, close kin consistently represented a tiny fraction of candidate mates (< 1%) across age and sex categories. Mating biases favouring partners with intermediate relatedness were detectable in yearling females and adult males, possibly partly caused by avoidance of daughter–father matings. Finally, inbreeding depression, assessed as the effect of heterozygosity on survival, was undetectable using a capture–mark–recapture study. Overall, these results indicate that sex‐biased dispersal is a primary inbreeding avoidance mechanism at the population level, and mating biases represent an additional strategy that may mitigate residual inbreeding costs at the individual level. Combined, these mechanisms explain the rarity of inbreeding and the lack of detectable inbreeding depression in this large, genetically diverse population.     

The effect of sex‐biased dispersal on opposite‐sexed spatial genetic structure and inbreeding risk

Natal sex‐biased dispersal has long been thought to reduce the risk of inbreeding by spatially separating opposite‐sexed kin. Yet, comprehensive and quantitative evaluations of this hypothesis are lacking. In this study, we quantified the effectiveness of sex‐biased dispersal as an inbreeding avoidance strategy by combining spatially explicit simulations and empirical data. We quantified the extent of kin clustering by measuring the degree of spatial autocorrelation among opposite‐sexed individuals (FM structure). This allowed us to systematically explore how the extent of sex‐biased dispersal, generational overlap, and mate searching distance, influenced both kin clustering, and the resulting inbreeding in the absence of complementary inbreeding avoidance strategies. Simulations revealed that when sex‐biased dispersal was limited, positive FM genetic structure developed quickly and increased as the mate searching distance decreased or as generational overlap increased. Interestingly, complete long‐range sex‐biased dispersal did not prevent the development of FM genetic structure when generations overlapped. We found a very strong correlation between FM genetic structure and both F_IS under random mating, and pedigree‐based measures of inbreeding. Thus, we show that the detection of FM genetic structure can be a strong indicator of inbreeding risk. Empirical data for two species with different life history strategies yielded patterns congruent with our simulations. Our study illustrates a new application of spatial genetic autocorrelation analysis that offers a framework for quantifying the risk of inbreeding that is easily extendable to other species. Furthermore, our findings provide other researchers with a context for interpreting observed patterns of opposite‐sexed spatial genetic structure.     

Direct Familiarity Does Not Alter Mating Preference for Sisters in Male Pelvicachromis taeniatus (Cichlidae)

In social species, individuals who grew up together are usually relatives. Therefore, direct familiarity is normally a reliable kin recognition mechanism that is used in many species to discriminate kin from non‐kin. It has been shown in animals and in humans that familiar individuals are rejected as mating partners in order to circumvent potential costs of inbreeding. Here, we tested whether direct familiarity also leads to inbreeding avoidance behaviour in male Pelvicachromis taeniatus, a small socially monogamous cichlid with biparental brood care. In mate choice experiments, reproductively active males were given the choice between familiar sisters and unfamiliar, unrelated females. In a previous study, both sexes of P. taeniatus had preferred unfamiliar full‐sibs over unfamiliar unrelated individuals as mating partners. Here, we show that direct familiarity does not alter the male preference for closely related females. This result is in accordance with theoretical predictions, that inbreeding can be advantageous under certain conditions, and confirms previous findings, that active inbreeding is an adaptive strategy in P. taeniatus.     

Lifetime inbreeding depression in a leaf beetle

Ongoing habitat loss and fragmentation result in rapid population size reductions, which can increase the levels of inbreeding. Consequently, many species are threatened by inbreeding depression, a loss of individual fitness following the mating of close relatives. Here, we investigated inbreeding effects on fitness‐related traits throughout the lifetime of the mustard leaf beetle (Phaedon cochleariae) and mechanisms for the avoidance of inbreeding. Previously, we found that these beetles have family‐specific cuticular hydrocarbon profiles, which are likely not used as recognition cue for precopulatory inbreeding avoidance. Thus, we examined whether adult beetles show postcopulatory inbreeding avoidance instead. For this purpose, we determined the larval hatching rate of eggs laid by females mated sequentially with two nonsiblings, two siblings, a nonsibling, and a sibling or vice versa. The beetles suffered from inbreeding depression throughout their entire ontogeny, as evinced by a prolonged larval development, a decreased larval and adult survival and a decreased reproductive output of inbred compared to outbred individuals. The highest larval hatching rates were detected when females were mated with two nonsiblings or first with a sibling and second with a nonsibling. Significantly lower hatching rates were measured in the treatments with a sibling as second male. Thus, the results do not support the existence of postcopulatory inbreeding avoidance in P. cochleariae, but revealed evidence for second male sperm precedence. Consequently, an alternative strategy to avoid inbreeding costs might exist in this beetle, such as a polyandrous mating system, potentially coupled with a specific dispersal behavior.     

Kin discrimination in sticklebacks is mediated by social learning rather than innate recognition

Theory predicts several advantages for animals to recognize kin. These include inbreeding avoidance and an increase in inclusive fitness. In shoaling species, kin recognition may lead to an increased amount of altruism among shoal members. Adult, non‐reproductive three‐spined sticklebacks, Gasterosteus aculeatus, prefer to shoal with kin. This preference was shown for familiar as well as for unfamiliar individuals. However, whether it is based on learned cues of familiar individuals or on innate mechanisms like self‐referent phenotype matching or ‘true’ kin recognition through recognition alleles remains unknown. In our experiments, juvenile fish were given the choice between shoals that differed in relatedness and familiarity. The number of testfish who joined each group indicated that sticklebacks prefer to shoal with familiar kin when the alternative shoal was composed of unfamiliar non‐kin. When one shoal consisted of familiar kin while the second consisted of familiar non‐kin testfish did not show any preference. Kin recognition in sticklebacks is thus most likely mediated by social learning.     

Close‐kin mating,but not inbred parents,reduces hatching rates and offspring quality in a threatened tortoise

Inbreeding depression, the reduction in fitness due to mating of related individuals, is of particular conservation concern in species with small, isolated populations. Although inbreeding depression is widespread in natural populations, long‐lived species may be buffered from its effects during population declines due to long generation times and thus are less likely to have evolved mechanisms of inbreeding avoidance than species with shorter generation times. However, empirical evidence of the consequences of inbreeding in threatened, long‐lived species is limited. In this study, we leverage a well‐studied population of gopher tortoises, Gopherus polyphemus, to examine the role of inbreeding depression and the potential for behavioural inbreeding avoidance in a natural population of a long‐lived species. We tested the hypothesis that increased parental inbreeding leads to reduced hatching rates and offspring quality. Additionally, we tested for evidence of inbreeding avoidance. We found that high parental relatedness results in offspring with lower quality and that high parental relatedness is correlated with reduced hatching success. However, we found that hatching success and offspring quality increase with maternal inbreeding, likely due to highly inbred females mating with more distantly related males. We did not find evidence for inbreeding avoidance in males and outbred females, suggesting sex‐specific evolutionary trade‐offs may have driven the evolution of mating behaviour. Our results demonstrate inbreeding depression in a long‐lived species and that the evolution of inbreeding avoidance is shaped by multiple selective forces.     

Behavioural inbreeding avoidance in wild African elephants

The costs of inbreeding depression, as well as the opportunity costs of inbreeding avoidance, determine whether and which mechanisms of inbreeding avoidance evolve. In African elephants, sex-biased dispersal does not lead to the complete separation of male and female relatives, and so individuals may experience selection to recognize kin and avoid inbreeding. However, because estrous females are rare and male-male competition for mates is intense, the opportunity costs of inbreeding avoidance may be high, particularly for males. Here we combine 28 years of behavioural and demographic data on wild elephants with genotypes from 545 adult females, adult males, and calves in Amboseli National Park, Kenya, to test the hypothesis that elephants engage in sexual behaviour and reproduction with relatives less often than expected by chance. We found support for this hypothesis: males engaged in proportionally fewer sexual behaviours and sired proportionally fewer offspring with females that were natal family members or close genetic relatives (both maternal and paternal) than they did with nonkin. We discuss the relevance of these results for understanding the evolution of inbreeding avoidance and for elephant conservation.     

No Inbreeding Avoidance by Female Burying Beetles Regardless of Whether They Encounter Males Simultaneously or Sequentially

Inbreeding avoidance reduces the probability that an individual will mate with a related partner, thereby lowering the risk that it produces inbred offspring suffering from inbreeding depression. Inbreeding avoidance can occur through several mechanisms, including active mate choice, polyandry and sex‐biased dispersal. Here, we focus on the role of active mate choice as a mechanism for inbreeding avoidance. Recent evidence suggests that the experimental design used in mate choice experiments (i.e. simultaneous versus sequential choice) can have a strong impact on the strength of the reported mating preferences. In this study, we examine whether similar effects of experimental design also apply in the context of inbreeding avoidance. To this end, we designed two experiments on the burying beetle Nicrophorus vespilloides that matched two different contexts under which females encounter potential mates in the wild; that is, when females encounter males simultaneously and sequentially. We found that females were as likely to mate with related and unrelated males regardless of whether they encountered male partners simultaneously or sequentially. Thus, our study provides no evidence for inbreeding avoidance in this species, and suggests that the number of mates present did not influence the degree of inbreeding avoidance. We discuss potential explanations for the lack of inbreeding avoidance through mate choice, including lack of mechanisms for recognizing close relatives, low costs and/or low risks of inbreeding and the presence of other inbreeding avoidance mechanisms, such as sex‐biased dispersal and polyandry coupled with post‐copulatory mate choice.     

Feed‐backs among inbreeding,inbreeding depression in sperm traits,and sperm competition can drive evolution of costly polyandry

Ongoing ambitions are to understand the evolution of costly polyandry and its consequences for species ecology and evolution. Emerging patterns could stem from feed‐back dynamics between the evolving mating system and its genetic environment, defined by interactions among kin including inbreeding. However, such feed‐backs are rarely considered in nonselfing systems. We use a genetically explicit model to demonstrate a mechanism by which inbreeding depression can select for polyandry to mitigate the negative consequences of mating with inbred males, rather than to avoid inbreeding, and to elucidate underlying feed‐backs. Specifically, given inbreeding depression in sperm traits, costly polyandry evolved to ensure female fertility, without requiring explicit inbreeding avoidance. Resulting sperm competition caused evolution of sperm traits and further mitigated the negative effect of inbreeding depression on female fertility. The evolving mating system fed back to decrease population‐wide homozygosity, and hence inbreeding. However, the net overall decrease was small due to compound effects on the variances in sex‐specific reproductive success and paternity skew. Purging of deleterious mutations did not eliminate inbreeding depression in sperm traits or hence selection for polyandry. Overall, our model illustrates that polyandry evolution, both directly and through sperm competition, might facilitate evolutionary rescue for populations experiencing sudden increases in inbreeding.     

Banded mongooses avoid inbreeding when mating with members of the same natal group

Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicating a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard–female relatedness did not affect the guard's probability of gaining reproductive success. However, where mate‐guards are unsuccessful, they lose paternity to males that are less related to the females than themselves. Together, our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited.     

Immigration prevents inbreeding in a growing colony of a long‐lived and philopatric seabird

Mating between close relatives can have deleterious effects on reproductive success or offspring fitness, which should favour the evolution of active or passive inbreeding avoidance mechanisms. In birds, evidence for active inbreeding avoidance by kin‐discriminative mate choice is scarce; many studies describe random mating in relation to kinship and thus support passive inbreeding avoidance by natal dispersal. However, most studies were conducted in island populations of short‐lived passerines with fast alternation of generations. In this study, we present inbreeding estimates based on pedigree data from a 16‐year study in a coastal colony of Common Terns Sterna hirundo, a long‐lived seabird with delayed sexual maturation and low rates of extra‐pair paternity. Incestuous mating was rare (four of 2387 pairs), even if partially accounting for incomplete pedigrees. Although the average relatedness of observed pairs was lower than would be expected from random pairing, the inbreeding coefficient did not differ from random mating. Hence, we found no clear evidence for active inbreeding avoidance by kin‐discriminative mate choice, and the low level of inbreeding seems to be related to the high immigration rate in the colony and thus to be maintained passively by dispersal.     

Has the inbreeding load for a condition‐dependent sexual signalling trait been purged in insular lizard populations?

Sexually selected traits are often condition‐dependent and are expected to be affected by genome‐wide distributed deleterious mutations and inbreeding. However, sexual selection is a powerful selective force that can counteract inbreeding through purging of deleterious mutations. Inbreeding and purging of the inbreeding load for sexually selected traits has rarely been studied across natural populations with different degrees of inbreeding. Here we investigate inbreeding effects (measured as marker‐based heterozygosity) on condition‐dependent sexually selected signalling trait and other morphological traits across islet‐ and mainland populations (n = 15) of an endemic lizard species (Podarcis gaigeae). Our data suggest inbreeding depression on a condition‐dependent sexually selected signalling character among mainland subpopulations with low or intermediate levels of inbreeding, but no sign of inbreeding depression among small and isolated islet populations despite their higher overall inbreeding levels. In contrast, there was no such pattern among ten other morphological traits which are primarily naturally selected and presumably not involved in sexual signalling. These results are in line with purging of recessive deleterious alleles, or purging in combination with stochastic fixation of alleles by genetic drift, for a sexual signalling character in the islet environment, which is characterized by low population sizes and strong sexual selection. Higher clutch sizes in islet populations also raise interesting questions regarding the possibility of antagonistic pleiotropy. Purging and other non‐exclusive explanations of our results are discussed.     

Consequences of genetic incompatibility on fitness and mate choice: the male point of view

Hymenopterans under single‐locus complementary sex determination (sl‐CSD) face inbreeding costs due to this sex determination mode. Under sl‐CSD, homozygote eggs at the sl‐CSD locus usually develop into unviable or sterile diploid males. Production of such costly males increases when sib‐mating happens because related individuals share half of their genome. In the hymenopteran Venturia canescens (a solitary parasitoid wasp), diploid males are sterile, leading to fitness costs through genetic incompatibility between parents. Whereas the costs of producing diploid males and behavioural strategies that would reduce such costs have been studied in females, the potential fitness costs faced by males have not. Here, we aimed to investigate fitness costs that males endure after a single sib‐mating and tested whether they have the ability to avoid sib‐mating through kin recognition. Our results show that males have a reduced fitness (i.e. they produce fewer daughters) when mating with their sibs. We also show that males have the ability to distinguish between non‐sib and sib females (i.e. kin). They use chemical marks emitted by the females to discriminate kin from non‐kin. We discuss the evolution of kin recognition in males in the context of mate choice for genetic compatibility. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 279–286.     

Kin discrimination and female mate choice in the naked mole-rat Heterocephalus glaber

Naked mole-rats are fossorial, eusocial rodents that naturally exhibit high levels of inbreeding. Persistent inbreeding in animals often results in a substantial decline in fitness and, thus, dispersal and avoidance of kin as mates are two common inbreeding avoidance mechanisms. In the naked mole-rat evidence for the former has recently been found. Here we address the latter mechanism by investigating kin recognition and female mate choice using a series of choice tests in which the odour, social and mate preferences of females were determined. Discrimination by females appears to be dependent on their reproductive status. Reproductively active females prefer to associate with unfamiliar males, whereas reproductively inactive females do not discriminate. Females do not discriminate between kin and non-kin suggesting that the criterion for recognition is familiarity, not detection of genetic similarity per se. In the wild, naked mole-rats occupy discrete burrow systems and dispersal and mixing with non-kin is thought to be comparatively rare. Thus, recognition by familiarity may function as a highly efficient kin recognition mechanism in the naked mole-rat. A preference by reproductively active females for unfamiliar males is interpreted as inbreeding avoidance. These findings suggest that, despite an evolutionary history of close inbreeding, naked mole-rats may not be exempt from the effects of inbreeding depression and will attempt to outbreed should the opportunity arise.     

Premating Avoidance of Inbreeding Absent in Female Guppies (Poecilia reticulata)

The recognition and avoidance of kin during mating can be an important means of reducing the potential for inbreeding depression in offspring. We report here that premating mechanisms to avoid inbreeding, either innate or learnt through juvenile experience, are at best weak in female guppies (Poecilia reticulata). Guppies are small, ovoviviparous, neo‐tropical freshwater fish, with a polygamous mating system where males actively court females and females are selective of their mates. In a series of mate‐choice experiments, naïve, virgin females of the Quare River population in Trinidad were given a choice between a brother and a non‐sib male from the same population. Initially, females were only provided olfactory cues upon which to base their choice and then subsequently both olfactory and visual cues. Despite the females displaying mate choice, we found no evidence of them discriminating between the male types in either experiment. There was thus no indication of inbreeding avoidance, suggesting that experiences after maturation or with mature males (e.g. rare male preference), dispersal and/or post‐mating mechanisms may be evolutionarily more important avoidance mechanisms.     

Female‐biased dispersal alone can reduce the occurrence of inbreeding in black grouse (Tetrao tetrix)

Although inbreeding depression and mechanisms for kin recognition have been described in natural bird populations, inbreeding avoidance through mate choice has rarely been reported suggesting that sex‐biased dispersal is the main mechanism reducing the risks of inbreeding. However, a full understanding of the effect of dispersal on the occurrence of inbred matings requires estimating the inbreeding risks prior to dispersal. Combining pairwise relatedness measures and kinship assignments, we investigated in black grouse whether the observed occurrence of inbred matings was explained by active kin discrimination or by female‐biased dispersal. In this large continuous population, copulations between close relatives were rare. As female mate choice was random for relatedness, females with more relatives in the local flock tended to mate with genetically more similar males. To quantify the initial risks of inbreeding, we measured the relatedness to the males of females captured in their parental flock and virtually translocated female hatchlings in their parental and to more distant flocks. These tests indicated that dispersal decreased the likelihood of mating with relatives and that philopatric females had higher inbreeding risks than the actual breeding females. As females do not discriminate against relatives, the few inbred matings were probably due to the variance in female dispersal propensity and dispersal distance. Our results support the view that kin discrimination mate choice is of little value if dispersal effectively reduces the risks of inbreeding.     

The genetic basis of inbreeding avoidance in house mice

Animals might be able to use highly polymorphic genetic markers to recognize very close relatives and avoid inbreeding. The major histocompatibility complex (MHC) is thought to provide such a marker because it influences individual scent in a broad range of vertebrates. However, direct evidence is very limited. In house mice (Mus musculus domesticus), the major urinary protein (MUP) gene cluster provides another highly polymorphic scent signal of genetic identity that could underlie kin recognition. We demonstrate that wild mice breeding freely in seminatural enclosures show no avoidance of mates with the same MHC genotype when genome-wide similarity is controlled. Instead, inbreeding avoidance is fully explained by a strong deficit in successful matings between mice sharing both MUP haplotypes. Single haplotype sharing is not a good guide to the identification of full sibs, and there was no evidence of behavioral imprinting on maternal MHC or MUP haplotypes. This study, the first to examine wild animals with normal variation in MHC, MUP, and genetic background, demonstrates that mice use self-referent matching of a species-specific polymorphic signal to avoid inbreeding. Recognition of close kin as unsuitable mates might be more variable across species than a generic vertebrate-wide ability to avoid inbreeding based on MHC.     

Evolution of precopulatory and post‐copulatory strategies of inbreeding avoidance and associated polyandry

Inbreeding depression is widely hypothesized to drive adaptive evolution of precopulatory and post‐copulatory mechanisms of inbreeding avoidance, which in turn are hypothesized to affect evolution of polyandry (i.e. female multiple mating). However, surprisingly little theory or modelling critically examines selection for precopulatory or post‐copulatory inbreeding avoidance, or both strategies, given evolutionary constraints and direct costs, or examines how evolution of inbreeding avoidance strategies might feed back to affect evolution of polyandry. Selection for post‐copulatory inbreeding avoidance, but not for precopulatory inbreeding avoidance, requires polyandry, whereas interactions between precopulatory and post‐copulatory inbreeding avoidance might cause functional redundancy (i.e. ‘degeneracy’) potentially generating complex evolutionary dynamics among inbreeding strategies and polyandry. We used individual‐based modelling to quantify evolution of interacting precopulatory and post‐copulatory inbreeding avoidance and associated polyandry given strong inbreeding depression and different evolutionary constraints and direct costs. We found that evolution of post‐copulatory inbreeding avoidance increased selection for initially rare polyandry and that evolution of a costly inbreeding avoidance strategy became negligible over time given a lower‐cost alternative strategy. Further, fixed precopulatory inbreeding avoidance often completely precluded evolution of polyandry and hence post‐copulatory inbreeding avoidance, but fixed post‐copulatory inbreeding avoidance did not preclude evolution of precopulatory inbreeding avoidance. Evolution of inbreeding avoidance phenotypes and associated polyandry is therefore affected by evolutionary feedbacks and degeneracy. All else being equal, evolution of precopulatory inbreeding avoidance and resulting low polyandry is more likely when post‐copulatory inbreeding avoidance is precluded or costly, and evolution of post‐copulatory inbreeding avoidance greatly facilitates evolution of costly polyandry.     

Consequences of a One-male Harem Reproductive System and Inbreeding in a Captive Group of <Emphasis Type="BoldItalic">Cercopithecus solatus</Emphasis>

In closed captive populations, where dispersal is not possible, kin recognition and behavioral avoidance are the only mechanisms by which closely related individuals can avoid inbreeding. In the absence of avoidance, a loss of genetic diversity is inevitable in successive generations.In the 1980s, the CIRMF in Gabon established a small breeding group of sun-tailed monkeys (Cercopithecus solatus) with 4 individuals, and subsequently 17 births have been registered. We aimed to describe via microsatellite genotyping the reproductive system in the colony of Cercopithecus solatus, to evaluate the loss of genetic diversity with succeeding generations, and to evaluate consequences of inbreeding depression on a measure of the lifespan reproductive success of females giving birth to inbred vs. noninbred offspring. During the 11-yr period for which data are available, only alpha males sired offspring, confirming a one-male social organization. They reproduced only during their period of tenure. Two of the 3 alpha males were responsible for all the infants born. Genetic diversity decreased and inbreeding coefficients increased with successive generations. Interbirth interval was increased following the birth of an inbred infant, indicating possible increased maternal costs of rearing inbred infants. Loss of genetic variability in this captive group of sun-tailed monkeys has led to significant inbreeding depression and demonstrates the importance of male-mediated gene flow in restricted one-male harem breeding groups.