No evidence for inbreeding avoidance in a natural population of song sparrows (Melospiza melodia)

We studied mate choice and inbreeding avoidance a natural population of song sparrows (Melospiza melodia) on Mandarte Island, Canada. Inbreeding occurred regularly: 59% all matings were between known relatives. We tested for inbreeding avoidance by comparing the observed levels of inbreeding to those expected if mate choice had been random with respect to relatedness. Independent of our assumptions about the availability of mates in the random mating model, we found that the expected and observed distributions of inbreeding coefficients were similar, as was the expected and observed frequency of close (f >/= 0.125) inbreeding. Furthermore, there was no difference in relatedness observed pairs and those that would have resulted had birds mated instead with their nearest neighbors. The only evidence to suggest any inbreeding avoidance was a reduced rate of parent-offspring matings as compared to one random mating model but not the other. Hence, despite substantial inbreeding depression in this population, we found little evidence for inbreeding avoidance through mate choice. We present a simple model to suggest that variation in inbreeding avoidance behaviors in birds may arise from differences in survival rates: in species with low survival rates, the costs of forfeiting matings to avoid inbreeding may exceed the costs of inbreeding.     

Inbreeding avoidance through kin recognition: choosy females boost male dispersal

Inbreeding avoidance is predicted to induce sex biases in dispersal. But which sex should disperse? In polygynous species, females pay higher costs to inbreeding and thus might be expected to disperse more, but empirical evidence consistently reveals male biases. Here, we show that theoretical expectations change drastically if females are allowed to avoid inbreeding via kin recognition. At high inbreeding loads, females should prefer immigrants over residents, thereby boosting male dispersal. At lower inbreeding loads, by contrast, inclusive fitness benefits should induce females to prefer relatives, thereby promoting male philopatry. This result points to disruptive effects of sexual selection. The inbreeding load that females are ready to accept is surprisingly high. In absence of search costs, females should prefer related partners as long as delta相似文献   

Mate choice by lineage in three captive groups of rhesus macaques (Macaca mulatta)

The hypothesis that the matrilineal affiliation of 410 infants born in three captive groups of rhesus macaques is independent of the patrilineal affiliation of these infants was tested. Preferential mating with particular patrilines was observed for matrilineal members. We conclude that lineage affiliation does influence mate choice of rhesus macaques, at least when a large number of matrilines and relatively few patrilines which include natal males are represented in the group. Such nonrandom mating might explain high levels of genetic heterogeneity reported among matrilines within rhesus groups, despite high rates of male emigration, and is consistent with the maintenance of high levels of within-matriline kinship which might promote cooperative behavior among matriline members.     

Role of male‐biased dispersal in inbreeding avoidance in the grey‐sided vole (Myodes rufocanus)

Effects of male‐biased dispersal on inbreeding avoidance were investigated in a semi‐natural population of Myodes (formerly Clethrionomys) rufocanus using a large outdoor enclosure (3 ha). Parentage of 918 voles weaned from 215 litters and relatedness of mates were analysed using microsatellite loci, and dispersal distances were obtained from mark–recapture live‐trapping data. Natal and breeding male‐biased dispersal was observed. There remained, however, chances that incestuous mating could occur, because not all males dispersed from their natal site, and 51 matings occurred between relatives (relatedness r > 0). The number of weaned juveniles from inbred litters was significantly smaller than that from non‐inbred litters. Fourteen incestuous matings occurred between close relatives (r ≥ 0.25), most of which were those between non‐littermate maternal half siblings (four cases) and those between paternal half siblings (seven cases). When comparing the observed frequencies to the expected ones generated by combining every oestrous female with a male randomly chosen from her surroundings, the observed values for inbreeding of r ≥ 0.25 were significantly smaller than the expectations, while no difference was observed for inbreeding of 0 < r < 0.25. These results suggest that male‐biased dispersal is partly effective to avoid incestuous mating, but it does not provide complete separation of male and female close relatives. Additional mechanisms such as kin discrimination based on familiarity may work in inbreeding avoidance of the vole.     

雌性黄山短尾猴回避近亲交配

本研究分别在交配期(2006年9月-2006年12月)和产仔期(2007年1月-2007年4月)对黄山短尾猴鱼鳞坑YA1群中5只雄猴和5只雌猴成年个体采用目标动物法、随机取样法和连续记录法记录行为参数。研究期间记录交配行为336例:母子交配0例;母系兄妹交配7例(占2.1%),其中强行交配4例;非亲缘关系交配329例(占97.9%),非亲缘关系交配频次显著高于亲缘关系。在交配期,雄猴对亲缘雌猴跟随、性检查频次均低于非亲缘雌猴,接近指数(PMI)在亲缘和非亲缘雌猴间无显著性差异;雌猴对亲缘雄猴交配拒绝率显著高于非亲缘雄猴,接近指数在交配期显著低于非亲缘雄猴,产仔期接近指数在亲缘和非亲缘雄猴间无显著性差异。尽管雄猴在交配选择上趋于避免与亲缘雌猴交配,但某些雄猴仍会主动对有亲缘关系的雌猴邀配或强行交配,雌猴则主动回避。这些结果表明:黄山短尾猴母系亲属间可以通过行为倾向抑制近亲交配发生,且雌猴更主动回避交配,支持了近交回避的双亲投资理论。     

PROBLEMS WITH TESTING INBREEDING AVOIDANCE: THE CASE OF THE COLLARED FLYCATCHER

Four year's data on collared flycatchers, Ficedula albicollis, breeding in a nestbox plot on the island of Gotland, Sweden, was used to investigate whether individuals avoid mating with close kin (i.e., parents or sibs). Only one case of close inbreeding (0.5% of all pairs) was observed during the years of study. The observed frequency of close inbreeding was compared to expected frequencies based on two different null models. Assuming no inbreeding avoidance behaviors (e.g., dispersal or kin recognition), but taking into account the fact that mortality, and different arrival and pairing times of individuals reduce the probability of mating with close kin, the expected frequency of close inbreeding is 10% and 15% for female and male recruits (i.e., born in the study plot), respectively. However, assuming mating to be random within the study plot reduced the expected frequency of close inbreeding to 1% or less for both males and females. Consequently, conclusions drawn concerning inbreeding avoidance depend on the null model used. Contrasting estimated costs of tolerating close inbreeding with those of avoiding it (by dispersal to other plots), however, suggests that the costs of avoiding close inbreeding are substantially greater than those of tolerating it. Therefore, although inbreeding avoidance cannot be rejected as a cause of dispersal of this species, it is not the primary cause, and particularly not for sex-biased dispersal. The general problems of investigating inbreeding avoidance are discussed. It is argued that all previous null models based on random mating in finite populations produce expected frequencies of close inbreeding that in fact include inbreeding avoidance, since they implicitly assume random dispersal within a finite population. Thus, comparisons between observed and expected frequencies of close inbreeding based on random mating are inadequate. The most promising method of investigating inbreeding avoidance is to experimentally study individual movements and mating preferences in the presence and absence of close kin.     

Lack of behavioural evidence for kin avoidance in mate choice in a hymenopteran parasitoid (Hymenoptera: Braconidae)

Mechanisms for inbreeding avoidance should be prevalent in insects that reproduce by arrhenotokous haplodiploidy because of the higher potential production of unviable diploid males in inbred matings. Few studies have focused on mating strategies in insect parasitoids and even less on kinship relationships during mate choice. In this study we tested avoidance of kin as mate in the parasitic wasp Aphidius matricariae (Hymenoptera: Braconidae) using an ethological approach. Key mating parameters, such as male wing fanning, latent period before genitalia contact and duration of copulation were measured. No evidence for kin avoidance in mate choice in both A. matricariae males and females was observed in our behaviour (no choice or choice tests) tests. This lack of ethological sib mating avoidance could be due to different factors such as sex determination rule different than the single locus complementary sex determination, making lower the proportion of diploid males in case of sib matings and thus its negative consequence. The existence of other inbreeding avoidance strategies and mechanisms that reduce the probability of 2 receptive relatives meeting in nature may be common, for example, inbred mating may be rare through differential dispersal, delayed maturation, or protandry.     

How Pronghorn Females Avoid Inbreeding Depression

After a bottleneck in a closed population of pronghorn (Antilocapra americana), some inbred matings occurred, and we detected significant inbreeding depression. But inbred matings occurred less frequently than would be expected by chance. Pronghorn females chose mates after a sampling period and had complete control of the mating decision. Therefore, to discover the behavioral mechanism by which females avoided mating with close kin, we studied female movements and courtship sequences. When females moved from one harem to another in the sampling process, they did not shift to harem males of lower coancestry as they approached estrus. Rather, females progressed more slowly through the later courtship stages when the harem male was related vs. unrelated. Also, the rates of male courtship acts were higher within unrelated vs. related pairs. Some females appeared to use multiple mating as an inbreeding avoidance strategy. Our results suggested that inbreeding avoidance by female pronghorn occurred primarily by reactions to the late stages of male courtship, rather than by spatial avoidance of related males.     

Inbreeding Avoidance in Male Primates: A Response to Female Mate Choice?

Inbreeding often has negative fitness consequences for primates, which have led to the evolution of inbreeding avoidance strategies in a number of species. In polygynous primates, females may suffer a higher fitness cost from inbreeding than males and are thus expected to exhibit a lower tolerance for inbreeding. Nevertheless, it is apparent that inbreeding avoidance behaviours are common in both female and male polygynous primates. In this perspectives article, I review the evidence that female mate choice can lead to male inbreeding avoidance behaviours in polygynous primates. I conclude that male inbreeding avoidance may be strongly driven by female mate choice at both proximate and ultimate levels. To better understand the extent to which this pattern applies across the primate order, studies are needed on the separate effects of participating in inbred matings and producing inbred offspring on male and female lifetime reproductive success . It would also be useful to examine how inbreeding avoidance strategies vary across primate mating systems. Finally, measuring the covariance between female choice and male inbreeding avoidance behaviour, and between male inbreeding avoidance behaviour and male fitness, would help to clarify the role of female mate choice in the evolution of male inbreeding avoidance.     

Genetic implications of mating structure in a Caribbean isolate.

Mating patterns in the population of St. Barthélémy, French West Indies, are examined to evaluate the expected genetic consequences of consanguinity avoidance and of failure to mate due to celibacy and emigration. Nearly 60% of all individuals reaching mating age on "St. Bart" never contribute to the gene pool of succeeding generations. This greatly reduces the effective population size and, therefore, increases genetic drift or random inbreeding. The consequent loss of heterozygosity is partially countered by the fact that the individuals who fail to reproduce within the population tend to be more closely related to the population than are those who do reproduce. This nonrandom failure to mate results in nonrandom inbreeding, which reduces total pedigree inbreeding. Total inbreeding is also reduced by consanguinity avoidance. However, the effect of avoiding close consanguineous matings is, to some extent, reversed by an apparent preference for more distant relationships, especially with second cousins. Generally similar results are found for the related Northside French population of St. Thomas. U.S. Virgin Islands. A recently developed mathematical model predicts the expected effect on heterozygosity of partial or complete avoidance of, or preference for, any combination of consanguineous matings, and also takes into account nonrandom failure to mate. Application of this model to these two populations suggests that under some circumstances nonrandomness in celibacy and emigration may have a greater influence on genotype distributions than does consanguinity avoidance.     

Inbreeding in three captive groups of rhesus monkeys

Using electrophoretic and serological genetic markers each of 17 potentially inbred matings in three groups of rhesus monkeys could be classified as either inbred or noninbred matings. Although nine of these 17 matings involved either father-daughter or paternal half-sib matings, only 7.4 were expected by chance alone. At least two, and possibly as many as three, of the nine cases of inbreeding involved father-daughter matings. Thus, no evidence of avoidance of inbreeding was observed in the closed captive groups of rhesus monkeys studied. Colony management policies must be developed to minimize the opportunity for or the deleterious effects of both father-daughter and half-sib matings. Furthermore, kin selection theory should consider why kin recognition, if it occurs, does not lead to avoidance of inbreeding.     

Apparent inbreeding preference despite inbreeding depression in the American crow

Although matings between relatives can have negative effects on offspring fitness, apparent inbreeding preference has been reported in a growing number of systems, including those with documented inbreeding depression. Here, we examined evidence for inbreeding depression and inbreeding preference in two populations (Clinton, New York, and Davis, California, USA) of the cooperatively breeding American crow (Corvus brachyrhynchos). We then compared observed inbreeding strategies with theoretical expectations for optimal, adaptive levels of inbreeding, given the inclusive fitness benefits and population‐specific magnitude of inbreeding depression. We found that low heterozygosity at a panel of 33 microsatellite markers was associated with low survival probability (fledging success) and low white blood cell counts among offspring in both populations. Despite these costs, our data were more consistent with inbreeding preference than avoidance: The observed heterozygosity among 396 sampled crow offspring was significantly lower than expected if local adults were mating by random chance. This pattern was consistent across a range of spatial scales in both populations. Adaptive levels of inbreeding, given the magnitude of inbreeding depression, were predicted to be very low in the California population, whereas complete disassortative mating was predicted in the New York population. Sexual conflict might have contributed to the apparent absence of inbreeding avoidance in crows. These data add to an increasing number of examples of an “inbreeding paradox,” where inbreeding appears to be preferred despite inbreeding depression.     

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.     

Inbreeding and promiscuity in the endangered grand skink

The inbreeding avoidance hypothesis predicts that organisms that often encounter relatives as potential mates should evolve behaviours to avoid incestuous matings. Avoidance behaviours have practical importance for small populations because deleterious genetic processes may be less imminent than otherwise expected from genetic models that assume random mating. I used genetic techniques to investigate the extent of inbreeding and inbreeding avoidance behaviours in rare lizards from southern New Zealand. Grand skinks, Oligosoma grande, live in small patchily distributed groups, and have low rates of inter-group dispersal (ca. 3–20% disperse). I used data from 15 microsatellite loci to test the hypothesis that adults are likely to encounter kin as potential mates and will inbreed. These data showed that adult skinks usually inhabited rock outcrops with adult relatives of the opposite sex – up to 35% of potential mates were of equivalent relatedness as half-sibs and 17% were equivalent to full sibs. However, skinks did not preferentially breed with less related mates, and 18.2% of matings were between individuals of equivalent relatedness as full-sibs. Instead, skinks mated with partners of all levels of relatedness, and were promiscuous – almost half of adult females and nearly three quarters of adult males reproduced with multiple partners. In addition, inbreeding had no effect on survival of offspring in their first year. Two other putative mechanisms of inbreeding avoidance, sex-biased and natal dispersal, were not pronounced in this species. This study adds to a growing list of species that inbreed despite the risks.     

The transition to social inbred mating systems in spiders: role of inbreeding tolerance in a subsocial predecessor

The social spiders are unusual among cooperatively breeding animals in being highly inbred. In contrast, most other social organisms are outbred owing to inbreeding avoidance mechanisms. The social spiders appear to originate from solitary subsocial ancestors, implying a transition from outbreeding to inbreeding mating systems. Such a transition may be constrained by inbreeding avoidance tactics or fitness loss due to inbreeding depression. We examined whether the mating system of a subsocial spider, in a genus with three social congeners, is likely to facilitate or hinder the transition to inbreeding social systems. Populations of subsocial Stegodyphus lineatus are substructured and spiders occur in patches, which may consist of kin groups. We investigated whether male mating dispersal prevents matings within kin groups in natural populations. Approximately half of the marked males that were recovered made short moves (< 5m) and mated within their natal patch. This potential for inbreeding was counterbalanced by a relatively high proportion of immigrant males. In mating experiments, we tested whether inbreeding actually results in lower offspring fitness. Two levels of inbreeding were tested: full sibling versus non-sib matings and matings of individuals within and between naturally occurring patches of spiders. Neither full siblings nor patch mates were discriminated against as mates. Sibling matings had no effect on direct fitness traits such as fecundity, hatching success, time to hatching and survival of the offspring, but negatively affected offspring growth rates and adult body size of both males and females. Neither direct nor indirect fitness measures differed significantly between within patch and between-patch pairs. We tested the relatedness between patch mates and nonpatch mates using DNA fingerprinting (TE-AFLP). Kinship explained 30% of the genetic variation among patches, confirming that patches are often composed of kin. Overall, we found limited male dispersal, lack of kin discrimination, and tolerance to low levels of inbreeding. These results suggest a history of inbreeding which may reduce the frequency of deleterious recessive alleles in the population and promote the evolution of inbreeding tolerance. It is likely that the lack of inbreeding avoidance in subsocial predecessors has facilitated the transition to regular inbreeding social systems.     

Inbreeding avoidance behaviors

Inbreeding is defined as mating between individuals related by common ancestry. Thus, the degree to which a particular mating is inbred depends on how far back in a pedigree one begins counting common ancestors. In general practice, the term inbreeding is used to describe mating between close relatives (first cousins or closer). Animal breeders have known for centuries that inbreeding causes a loss of constitutional vigor and fertility in domestic livestock. A growing literature now demonstrates that the offspring of matings between close relatives in species of undomesticated birds and mammals are less fit than outbred offspring. The deleterious consequences of inbreeding suggest the possibility that many species have evolved behaviors that lower the frequency of inbreeding.     

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.     

Inbreeding Depression and Inbreeding Avoidance in a Natural Population of Guppies (Poecilia reticulata)

Maintenance of genetic variation in the face of strong natural selection is a long‐standing problem in evolutionary biology. One of the most extreme examples of within‐population variation is the polymorphic, genetically determined color pattern of male Trinidad guppies (Poecilia reticulata). Female mating preference for rare or novel patterns has been implicated as a factor in maintaining this variation. The origin of this preference is not understood, although inbreeding avoidance has been proposed as a mechanism. Inbreeding avoidance is advantageous when populations exhibit inbreeding depression and the opportunity for mating between relatives exists. To determine whether these conditions are met in a natural guppy population, we assessed mating and reproductive patterns using polymorphic molecular markers. Females produced more offspring with less‐related males than with more‐related ones. In addition, females were more likely to have mated with less‐related males, but this trend was only marginally significant. Male heterozygosity was positively correlated with mating success and with the number of offspring sired, consistent with strong inbreeding depression for adult male fitness. These results provide substantial insight into mating patterns of a wild guppy population: strong inbreeding depression occurs, and individuals tend to avoid mating with relatives.     

Kin Recognition and Inbreeding Avoidance in a Butterfly

Owing to the risk of inbreeding depression, the evolution of inbreeding avoidance by means of kin recognition is expected for many biological systems. Nevertheless, an ability to distinguish among relatives and non‐relatives has been only rarely demonstrated, especially so in non‐social organisms. We here show that, in the non‐social tropical butterfly Bicyclus anynana, females discriminate against relatives by preferentially mating with non‐relatives. Inbreeding avoidance was more pronounced in inbred as compared with outbred butterflies, suggesting that it is partly condition dependent. We argue that, in our system, the evolution of inbreeding avoidance is related to carrying a high genetic load and thus to being particularly sensitive to inbreeding depression. We suggest that kin recognition might be more widespread than currently thought and that future studies may possibly benefit from considering condition dependence, especially by paying attention to and/or manipulating population history, genetic load, and the risk of inbreeding depression. We further suggest that kin recognition in B. anynana might be based on cuticular hydrocarbons used for self‐referencing.     

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.