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.     

No evidence for inbreeding avoidance in a great reed warbler population

Inbreeding depression may drive the evolution of inbreedingavoidance through dispersal and mate choice. In birds, manyspecies show female-biased dispersal, which is an effectiveinbreeding avoidance mechanism. In contrast, there is scarceevidence in birds for kin discriminative mate choice, whichmay, at least partly, reflect difficulties detecting it. First,kin discrimination may be realized as dispersal, and this isdifficult to distinguish from other causes of dispersal. Second,even within small, isolated populations, it is often difficultto determine the potential candidates available to a femalewhen choosing a mate. We sought evidence for inbreeding avoidancevia kin discrimination in a breeding population of great reedwarblers (Acrocephalus arundinaceus) studied over 17 years.Inbreeding depression is strong in the population, suggestingthat it would be adaptive to avoid relatives as mates. Detaileddata on timing of settlement and mate search movements madeit possible to identify candidate mates for each female, andlong-term pedigrees and resolved parentage enabled us to estimaterelatedness between females and their candidate mates. We foundno evidence for kin discrimination: mate choice was random withrespect to relatedness when all mate-choice events were considered,and, after correction for multiple tests, also in all breedingyears. We suggest that dispersal is a sufficient inbreedingavoidance mechanism in most situations, although the lack ofkin discriminative mate choice has negative consequences forsome females, because they end up mating with closely relatedmales that lowers their fitness.     

Female‐biased dispersal in a bat with a female‐defence mating strategy

The ultimate causes for predominant male‐biased dispersal (MBD) in mammals and female‐biased dispersal (FBD) in birds are still subject to much debate. Studying exceptions to general patterns of dispersal, for example, FBD in mammals, provides a valuable opportunity to test the validity of proposed evolutionary pressures. We used long‐term behavioural and genetic data on individually banded Proboscis bats (Rhynchonycteris naso) to show that this species is one of the rare mammalian exceptions with FBD. Our results suggest that all females disperse from their natal colonies prior to first reproduction and that a substantial proportion of males are philopatric and reproduce in their natal colonies, although male immigration has also been detected. The age of females at first conception falls below the tenure of males, suggesting that females disperse to avoid father–daughter inbreeding. Male philopatry in this species is intriguing because Proboscis bats do not share the usual mammalian correlates (i.e. resource‐defence polygyny and/or kin cooperation) of male philopatry. They have a mating strategy based on female defence, where local mate competition between male kin is supposedly severe and should prevent the evolution of male philopatry. However, in contrast to immigrant males, philopatric males may profit from acquaintance with the natal foraging grounds and may be able to attain dominance easier and/or earlier in life. Our results on Proboscis bats lent additional support to the importance of inbreeding avoidance in shaping sex‐biased dispersal patterns and suggest that resource defence by males or kin cooperation cannot fully explain the evolution of male philopatry in mammals.     

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.     

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.     

MHC‐disassortative mate choice and inbreeding avoidance in a solitary primate

Sexual selection theory suggests that choice for partners carrying dissimilar genes at the major histocompatibility complex (MHC) may play a role in maintaining genetic variation in animal populations by limiting inbreeding or improving the immunity of future offspring. However, it is often difficult to establish whether the observed MHC dissimilarity among mates drives mate choice or represents a by‐product of inbreeding avoidance based on MHC‐independent cues. Here, we used 454‐sequencing and a 10‐year study of wild grey mouse lemurs (Microcebus murinus), small, solitary primates from western Madagascar, to compare the relative importance on the mate choice of two MHC class II genes, DRB and DQB, that are equally variable but display contrasting patterns of selection at the molecular level, with DRB under stronger diversifying selection. We further assessed the effect of the genetic relatedness and of the spatial distance among candidate mates on the detection of MHC‐dependent mate choice. Our results reveal inbreeding avoidance, along with disassortative mate choice at DRB, but not at DQB. DRB‐disassortative mate choice remains detectable after excluding all related dyads (characterized by a relatedness coefficient r > 0), but varies slightly with the spatial distance among candidate mates. These findings suggest that the observed deviations from random mate choice at MHC are driven by functionally important MHC genes (like DRB) rather than passively resulting from inbreeding avoidance and further emphasize the need for taking into account the spatial and genetic structure of the population in correlative tests of MHC‐dependent mate choice.     

Inbreeding and disease avoidance in a free‐ranging koala population

Habitat destruction and fragmentation are increasing globally, forcing surviving species into small, isolated populations. Isolated populations typically experience heightened inbreeding risk and associated inbreeding depression and population decline; although individuals in these populations may mitigate these risks through inbreeding avoidance strategies. For koalas, as dietary specialists already under threat in the northern parts of their range, increased habitat fragmentation and associated inbreeding costs are of great conservation concern. Koalas are known to display passive inbreeding avoidance through sex‐biased dispersal, although population isolation will reduce dispersal pathways. We tested whether free‐ranging koalas display active inbreeding avoidance behaviours. We used VHF tracking data, parentage reconstruction, and veterinary examination results to test whether free‐ranging female koalas avoid mating with (a) more closely related males; and (b) males infected with sexually transmitted Chlamydia pecorum. We found no evidence that female koalas avoid mating with relatively more related available mates. In fact, as the relatedness of potential mates increases, so did inbreeding events. We also found no evidence that female koalas can avoid mating with males infected with C. pecorum. The absence of active inbreeding avoidance mechanisms in koalas is concerning from a conservation perspective, as small, isolated populations may be at even higher risk of inbreeding depression than expected. At risk koala populations may require urgent conservation interventions to augment gene flow and reduce inbreeding risks. Similarly, if koalas are not avoiding mating with individuals with chlamydial disease, populations may be at higher risk from disease than anticipated, further impacting population viability.     

Inbreeding and inbreeding avoidance in wild giant pandas

Inbreeding can have negative consequences on population and individual fitness, which could be counteracted by inbreeding avoidance mechanisms. However, the inbreeding risk and inbreeding avoidance mechanisms in endangered species are less studied. The giant panda, a solitary and threatened species, lives in many small populations and suffers from habitat fragmentation, which may aggravate the risk of inbreeding. Here, we performed long‐term observations of reproductive behaviour, sampling of mother–cub pairs and large‐scale genetic analyses on wild giant pandas. Moderate levels of inbreeding were found in 21.1% of mating pairs, 9.1% of parent pairs and 7.7% of panda cubs, but no high‐level inbreeding occurred. More significant levels of inbreeding may be avoided passively by female‐biased natal dispersal rather than by breeding dispersal or active relatedness‐based mate choice mechanisms. The level of inbreeding in giant pandas is greater than expected for a solitary mammal and thus warrants concern for potential inbreeding depression, particularly in small populations isolated by continuing habitat fragmentation, which will reduce female dispersal and increase the risk 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 avoidance in spiders: evidence for rescue effect in fecundity of female spiders with outbreeding opportunity

Selection by inbreeding depression should favour mating biases that reduce the risk of fertilization by related mates. However, equivocal evidence for inbreeding avoidance questions the strength of inbreeding depression as a selective force in the evolution of mating biases. Lack of inbreeding avoidance can be because of low risk of inbreeding, variation in tolerance to inbreeding or high costs of outbreeding. We examined the relationship between inbreeding depression and inbreeding avoidance adaptations under two levels of inbreeding in the spider Oedothorax apicatus, asking whether preference for unrelated sperm via pre- and/or post-copulatory mechanisms could restore female fitness when inbreeding depression increases. Using inbred isofemale lines we provided female spiders with one or two male spiders of different relatedness in five combinations: one male sib; one male nonsib; two male sibs; two male nonsibs; one male sib and one male nonsib. We assessed the effect of mating treatment on fecundity and hatching success of eggs after one and three generations of inbreeding. Inbreeding depression in F1 was not sufficient to detect inbreeding avoidance. In F3, inbreeding depression caused a major decline in fecundity and hatching rates of eggs. This effect was mitigated by complete recovery in fecundity in the sib-nonsib treatment, whereas no rescue effect was detected in the hatching success of eggs. The rescue effect is best explained by post-mating discrimination against kin via differential allocation of resources. The natural history of O. apicatus suggests that the costs of outbreeding may be low which combined with high costs of inbreeding should select for avoidance mechanisms. Direct benefits of post-mating inbreeding avoidance and possibly low costs of female multiple mating can favour polyandry as an inbreeding avoidance mechanism.     

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.     

Phenotype matching and inbreeding avoidance in African elephants

Perhaps the most important 'decision' made by any animal (or plant) is whether to disperse--leave kith and kin, or remain with the familiar and related. The benefits of staying at home are obvious, so dispersal requires an explanation--and the most popular is that dispersal functions to avoid inbreeding depression. Strong support comes from the observation that dispersal is so often sex biased. Simply put, all else being equal members of both sexes should prefer to remain philopatric, but this would lead to inbreeding depression so members of one sex have to disperse. In principle, this link between inbreeding depression and sex-biased dispersal could be broken if individuals recognize close kin and avoid mating with them. Archie et al. (2007) provide one of the most compelling analyses to date of the interaction among inbreeding avoidance, kin recognition and mating strategies in any mammal, clearly showing that elephants recognize even close paternal kin and avoid mating with them. Their important results illuminate the subtleties of elephant inbreeding avoidance as well as illustrate the difficulty of arriving at definitive answers to questions about the evolution of dispersal behaviour.     

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.     

Insects and incest: Sib‐mating tolerance in natural populations of a parasitoid wasp

Sib‐mating avoidance is a pervasive behaviour that is expected to evolve in species subject to inbreeding depression. Although laboratory studies provide elegant demonstrations, small‐scaled bioassays minimize the costs of mate finding and choice, and thus may produce spurious findings. We therefore combined laboratory experiments with field observations to examine the existence of inbreeding avoidance using the parasitoid wasp Venturia canescens. In the laboratory, our approach consisted of mate‐choice experiments to assess kin discrimination in population cages with competitive interactions. A higher mating probability after sib rejections suggested that females could discriminate their sibs; however, in contrast to previous findings, sib‐mating avoidance was not observed. To compare our laboratory results to field data, we captured 241 individuals from two populations. Females laid eggs in the lab, and 226 daughters were obtained. All individuals were genotyped at 18 microsatellite loci, which allowed inference of the genotype of each female's mate and subsequently the relatedness within each mating pair. We found that the observed rate of sib‐mating did not differ from the probability that sibs encountered one another at random in the field, which is consistent with an absence of sib‐mating avoidance. In addition, we detected a weak but significant male‐biased dispersal, which could reduce encounters between sibs. We also found weak fitness costs associated with sib‐mating. As such, the sex‐biased dispersal that we found is probably sufficient to mitigate these costs. These results imply that kin discrimination has probably evolved for purposes other than mate choice, such as superparasitism avoidance.     

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.     

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.     

Sex‐biased dispersal: a review of the theory

Dispersal is ubiquitous throughout the tree of life: factors selecting for dispersal include kin competition, inbreeding avoidance and spatiotemporal variation in resources or habitat suitability. These factors differ in whether they promote male and female dispersal equally strongly, and often selection on dispersal of one sex depends on how much the other disperses. For example, for inbreeding avoidance it can be sufficient that one sex disperses away from the natal site. Attempts to understand sex‐specific dispersal evolution have created a rich body of theoretical literature, which we review here. We highlight an interesting gap between empirical and theoretical literature. The former associates different patterns of sex‐biased dispersal with mating systems, such as female‐biased dispersal in monogamous birds and male‐biased dispersal in polygynous mammals. The predominant explanation is traceable back to Greenwood's ( 1980 ) ideas of how successful philopatric or dispersing individuals are at gaining mates or the resources required to attract them. Theory, however, has developed surprisingly independently of these ideas: models typically track how immigration and emigration change relatedness patterns and alter competition for limiting resources. The limiting resources are often considered sexually distinct, with breeding sites and fertilizable females limiting reproductive success for females and males, respectively. We show that the link between mating system and sex‐biased dispersal is far from resolved: there are studies showing that mating systems matter, but the oft‐stated association between polygyny and male‐biased dispersal is not a straightforward theoretical expectation. Here, an important understudied factor is the extent to which movement is interpretable as an extension of mate‐searching (e.g. are matings possible en route or do they only happen after settling in new habitat – or can females perhaps move with stored sperm). We also point out other new directions for bridging the gap between empirical and theoretical studies: there is a need to build Greenwood's influential yet verbal explanation into formal models, which also includes the possibility that an individual benefits from mobility as it leads to fitness gains in more than one final breeding location (a possibility not present in models with a very rigid deme structure). The order of life‐cycle events is likewise important, as this impacts whether a departing individual leaves behind important resources for its female or male kin, or perhaps both, in the case of partially overlapping resource use.     

Testing alternative captive breeding strategies with the subsequent release into the wild

We used the housefly (Musca domestica L.) as an experimental model to compare two strategies for the captive breeding of an endangered species: a strategy to minimize inbreeding and balance founder contributions (termed “MAI” for “maximum avoidance of inbreeding”) versus a scheme to select against less fit individuals (disregarding relatedness). By balancing the initial founder contributions, the MAI protocol was analogous to methods for minimizing kinship. In both breeding strategies, the population growth rate was limited to a maximum increase of 50% per generation. Five replicate populations, each starting with five male–female pairs, were subjected to five generations of captive breeding. Six generations of simulated “release into the wild” allowed ad lib breeding with less restrictive population growth potential, in either a benign or stressful environment (i.e., constant or variable temperature). Population size, fecundity, and fertility were assayed throughout the experiment, with juvenile‐to‐adult survival assayed in the second phase of the project. Allozyme assays determined the resultant inbreeding coefficients from the captive breeding schemes. The MAI breeding scheme resulted in significantly lower inbreeding coefficients and higher fitness, with qualitatively reduced extinction potential, most notable in the stressful environment. Spontaneous fitness rebounds suggested that the MAI strategy facilitated some form of purging of inbreeding depression effects. Importantly, the advantages of the MAI strategy were difficult to detect during the captive breeding phase, suggesting that the long‐term advantages of the MAI approach could be underestimated in actual breeding programs. We concur with the common recommendation of maximum avoidance of inbreeding at least for systems with low reproductive potential. Zoo Biol 0:1–18, 2005. © 2005 Wiley‐Liss, Inc.     

Inbreeding avoidance mechanisms: dispersal dynamics in cooperatively breeding southern pied babblers

1.?Breeding with kin can reduce individual fitness through the deleterious effects of inbreeding depression. Inbreeding avoidance mechanisms are expected to have developed in most species, and especially in cooperatively breeding species where individuals may delay dispersal until long after sexual maturity. Such potential mechanisms include sex-biased dispersal and avoidance of kin known through associative learning. 2.?The investigation of inbreeding avoidance through dispersal dynamics can be enhanced by combining fine-scale population genetic structure data with detailed behavioural observations of wild populations. 3.?We investigate possible inbreeding avoidance in a wild population of cooperatively breeding southern pied babblers (Turdoides bicolor). A combination of genetic, geographic and observational data is used to examine fine-scale genetic structure, dispersal (including sex-biased dispersal) and inheritance of dominance in cooperatively breeding groups. 4.?Unusually, sex-bias in dispersal distance does not occur. Rather, individuals appear to avoid inbreeding through two routes. First, through dispersal itself: although both males and females disperse locally, they move outside the range within which genetically similar individuals are usually found, going twice as far from natal groups as from non-natal groups. Second, through avoidance of familiar group members as mates: individuals inherit a dominant position in the natal group only when an unrelated breeding partner is present. 5.?This study uses spatial genetic analyses to investigate inbreeding avoidance mechanisms in a cooperative breeder and shows that individuals of both sexes can avoid inbreeding through a dispersal distance mechanism. While it appears that dispersal allows most individuals to move beyond the range of closely related kin, matings may still occur between distant kin. Nevertheless, any costs of breeding with a distant relative may be outweighed by the benefits of local dispersal and the immense fitness gains available from attaining a breeding position.     

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.