Natal dispersal and parental escorting predict relatedness between mates in a passerine bird

Although relatedness between mates is of considerable evolutionary and ecological significance, the way in which the level of relatedness is determined by different behavioural processes remains largely unknown. We investigated the role of behaviour in predicting mate relatedness in great tits using genotypic markers and detailed observations. We studied how mate relatedness is influenced by natal dispersal, inbreeding/outbreeding avoidance after natal dispersal and a behaviour not previously considered that influences membership to social aggregations, namely family escorting behaviour by parents. Among locally born individuals, the level of mate relatedness decreased with natal dispersal distance for females, but not for males. In contrast, mate relatedness was negatively related to the extent of family movements for males, but not for females. However, family movements did not predict dispersal distance for either sex. Local recruits were more related to their mates than immigrants, but this was only significant for females. No evidence was found for inbreeding/outbreeding avoidance after dispersal. Our results suggest that, in highly mobile species, mating options are spatially and/or socially limited, and that parents influence mating options of their offspring before dispersal.     

Evidence for female-biased dispersal in the protandrous hermaphroditic Asian Seabass, Lates calcarifer

Movement of individuals influences individual reproductive success, fitness, genetic diversity and relationships among individuals within populations and gene exchange among populations. Competition between males or females for mating opportunities and/or local resources predicts a female bias in taxa with monogamous mating systems and a male-biased dispersal in polygynous species. In birds and mammals, the patterns of dispersal between sexes are well explored, while dispersal patterns in protandrous hermaphroditic fish species have not been studied. We collected 549 adult individuals of Asian seabass (Lates calcarifer) from four locations in the South China Sea. To assess the difference in patterns of dispersal between sexes, we genotyped all individuals with 18 microsatellites. Significant genetic differentiation was detected among and within sampling locations. The parameters of population structure (F(ST)), relatedness (r) and the mean assignment index (mAIC), in combination with data on tagging-recapture, supplied strong evidences for female-biased dispersal in the Asian seabass. This result contradicts our initial hypothesis of no sex difference in dispersal. We suggest that inbreeding avoidance of females, female mate choice under the condition of low mate competition among males, and male resource competition create a female-biased dispersal. The bigger body size of females may be a cause of the female-biased movement. Studies of dispersal using data from DNA markers and tagging-recapture in hermaphroditic fish species could enhance our understanding of patterns of dispersal in fish.     

Sex-biased natal dispersal and inbreeding avoidance in American black bears as revealed by spatial genetic analyses

We tested the hypothesis that sex-biased natal dispersal reduces close inbreeding in American black bears, a solitary species that exhibits nearly complete male dispersal and female philopatry. Using microsatellite DNA and spatial data from reproductively mature bears (>or= 4 years old), we examined the spatial genetic structure of two distinct populations in New Mexico from 1993 to 2000. As predicted, relatedness (r) and the frequency of close relationships (parent-offspring or full siblings) decreased with distance among female dyads, but little change was observed among male or opposite-sex dyads. Neighbouring females were more closely related than neighbouring males. The potential for inbreeding was low. Most opposite-sex pairs that lived sufficiently close to facilitate mating were unrelated, and few were close relatives. We found no evidence that bears actively avoided inbreeding in their selection of mates from this nearby pool, as mean r and relationship frequencies did not differ between potential and actual mating pairs (determined by parentage analysis). These basic patterns were apparent in both study areas despite a nearly two-fold difference in density. However, the sex bias in dispersal was less pronounced in the lower-density area, based on proportions of bears with male and female relatives residing nearby. This result suggests that male bears may respond to reduced competition by decreasing their rate or distance of dispersal. Evidence supports the hypothesis that inbreeding avoidance is achieved by means of male-biased dispersal but also indicates that competition (for mates or resources) modifies dispersal patterns.     

Re‐mating across years and intralineage polygyny are associated with greater than expected levels of inbreeding in wild red deer

The interaction between philopatry and nonrandom mating has important consequences for the genetic structure of populations, influencing co‐ancestry within social groups but also inbreeding. Here, using genetic paternity data, we describe mating patterns in a wild population of red deer (Cervus elaphus) which are associated with marked consequences for co‐ancestry and inbreeding in the population. Around a fifth of females mate with a male with whom they have mated previously, and further, females frequently mate with a male with whom a female relative has also mated (intralineage polygyny). Both of these phenomena occur more than expected under random mating. Using simulations, we demonstrate that temporal and spatial factors, as well as skew in male breeding success, are important in promoting both re‐mating behaviours and intralineage polygyny. However, the information modelled was not sufficient to explain the extent to which these behaviours occurred. We show that re‐mating and intralineage polygyny are associated with increased pairwise relatedness in the population and a rise in average inbreeding coefficients. In particular, the latter resulted from a correlation between male relatedness and rutting location, with related males being more likely to rut in proximity to one another. These patterns, alongside their consequences for the genetic structure of the population, have rarely been documented in wild polygynous mammals, yet they have important implications for our understanding of genetic structure, inbreeding avoidance and dispersal in such systems.     

Inbreeding and sex-biased gene flow in the ant Formica exsecta

Abstract.— The objective of this study was to assess breeding and dispersal patterns of both males and females in a monogyne (a single queen per colony) population of ants. Monogyny is commonly associated with extensive nuptial flights, presumably leading to considerable gene flow over large areas. Opposite to these expectations we found evidence of both inbreeding and sex-biased gene flow in a monogyne population of Formica exsecta . We found a significant degree of population subdivision at a local scale (within islands) for queens (females heading established colonies) and workers, but not for colony fathers (the males mated to the colony queens). However, we found little evidence of population subdivision at a larger scale (among islands). More conclusive support for sex-biased gene flow comes from the analysis of isolation by distance on the largest island, and from assignment tests revealing differences in female and male philopatry. The genetic similarity between pairs of queens decreased significantly when geographical distance increased, demonstrating limited dispersal and isolation by distance in queens. By contrast, we found no such pattern for colony fathers. Furthermore, a significantly greater fraction of colony queens were assigned as having originated from the population of residence, as compared to colony fathers. Inbreeding coefficients were significantly positive for workers, but not for mother queens. The queen-male relatedness coefficient of 0.23 (regression relatedness) indicates that mating occurs between fairly close relatives. These results suggest that some monogyne species of ants have complex dispersal and mating systems that can result in genetic isolation by distance over small geographical scales. More generally, this study also highlights the importance of identifying the relevant scale in analyses of population structure and dispersal.     

Population density and sex do not influence fine-scale natal dispersal in roe deer

It is commonly assumed that the propensity to disperse and the dispersal distance of mammals should increase with increasing density and be greater among males than among females. However, most empirical evidence, especially on large mammals, has focused on highly polygynous and dimorphic species displaying female-defence mating tactics. We tested these predictions on roe deer, a weakly polygynous species of large herbivore exhibiting a resource-defence mating tactic at a fine spatial scale. Using three long-term studies of populations that were subject to the experimental manipulation of size, we did not find any support for either prediction, whether in terms of dispersal probability or dispersal distance. Our findings of similar dispersal patterns in both sexes of roe deer suggest that the underlying cause of natal dispersal is not related to inbreeding avoidance in this species. The absence of positive density dependence in fine-scale dispersal behaviour suggests that roe deer natal dispersal is a pre-saturation process that is shaped by heterogeneities in habitat quality rather than by density per se.     

Inbreeding Avoidance Drives Consistent Variation of Fine-Scale Genetic Structure Caused by Dispersal in the Seasonal Mating System of Brandt’s Voles

Inbreeding depression is a major evolutionary and ecological force influencing population dynamics and the evolution of inbreeding-avoidance traits such as mating systems and dispersal. Mating systems and dispersal are fundamental determinants of population genetic structure. Resolving the relationships among genetic structure, seasonal breeding-related mating systems and dispersal will facilitate our understanding of the evolution of inbreeding avoidance. The goals of this study were as follows: (i) to determine whether females actively avoided mating with relatives in a group-living rodent species, Brandt’s voles (Lasiopodomys brandtii), by combined analysis of their mating system, dispersal and genetic structure; and (ii) to analyze the relationships among the variation in fine-genetic structure, inbreeding avoidance, season-dependent mating strategies and individual dispersal. Using both individual- and population-level analyses, we found that the majority of Brandt’s vole groups consisted of close relatives. However, both group-specific FISs, an inbreeding coefficient that expresses the expected percentage rate of homozygosity arising from a given breeding system, and relatedness of mates showed no sign of inbreeding. Using group pedigrees and paternity analysis, we show that the mating system of Brandt’s voles consists of a type of polygyny for males and extra-group polyandry for females, which may decrease inbreeding by increasing the frequency of mating among distantly-related individuals. The consistent variation in within-group relatedness, among-group relatedness and fine-scale genetic structures was mostly due to dispersal, which primarily occurred during the breeding season. Biologically relevant variation in the fine-scale genetic structure suggests that dispersal during the mating season may be a strategy to avoid inbreeding and drive the polygynous and extra-group polyandrous mating system of this species.     

Female reproductive strategies, paternity and community structure in wild West African chimpanzees

Although the variability and complexity of chimpanzee behaviour frustrates generalization, it is widely believed that social evolution in this species occurs in the context of the recognizable social group or community. We used a combination of field observations and noninvasive genotyping to study the genetic structure of a habituated community of 55 wild chimpanzees, Pan troglodytes verus, in the Ta? Forest, C?te d'Ivoire. Pedigree relationships in that community show that female mate choice strategies are more variable than previously supposed and that the observed social groups are not the exclusive reproductive units. Genetic evidence based on nuclear microsatellite markers and behavioural obser-vations reveal that females in the Ta? forest actively seek mating partners outside their social unit; noncommunity males accounted for half the paternities over 5 years. This female mating strategy increases male gene flow between communities despite male philopatry, and negates the predicted higher relatedness among community males. Kin selection seems unlikely to explain the frequent cooperation and sharing observed among group males in this population. Similarly, inbreeding avoidance is probably not the sole cause of permanent adolescent female dispersal as a combination of extragroup mating and avoidance of incest with home group males would allow females to avoid inbreeding without the hazards associated with immigration into a new community. Extragroup mating as part of chimpanzee females' reproductive strategy may allow them to choose from a wider variety and number of males, without losing the resources and support provided by their male social group partners. Copyright 1999 The Association for the Study of Animal Behaviour.     

A spatial genetic structure and effects of relatedness on mate choice in a wild bird population

Inbreeding depression, as commonly found in natural populations, should favour the evolution of inbreeding avoidance mechanisms. If natal dispersal, the first and probably most effective mechanism, does not lead to a complete separation of males and females from a common origin, a small-scale genetic population structure may result and other mechanisms to avoid inbreeding may exist. We studied the genetic population structure and individual mating patterns in blue tits (Parus caeruleus). The population showed a local genetic structure in two out of four years: genetic relatedness between individuals (estimated from microsatellite markers) decreased with distance. This pattern was mainly caused by immigrants to the study area; these, if paired with fellow immigrants, were more related than expected by chance. Since blue tits did not avoid inbreeding with their social partner, we examined if individuals preferred less related partners at later stages of the mate choice process. We found no evidence that females or males avoided inbreeding through extra-pair copulations or through mate desertion and postbreeding dispersal. Although the small-scale genetic population structure suggests that blue tits could use a simple rule of thumb to select less related mates, females did not generally prefer more distantly breeding extra-pair partners. However, the proportion of young fathered by an extra-pair male in mixed paternity broods depended on the genetic relatedness with the female. This suggests that there is a fertilization bias towards less related copulation partners and that blue tits are able to reduce the costs of inbreeding through a postcopulatory process.     

Restricted mating dispersal and strong breeding group structure in a mid-sized marsupial mammal (Petrogale penicillata)

Ecological genetic studies have demonstrated that spatial patterns of mating dispersal, the dispersal of gametes through mating behaviour, can facilitate inbreeding avoidance and strongly influence the structure of populations, particularly in highly philopatric species. Elements of breeding group dynamics, such as strong structuring and sex-biased dispersal among groups, can also minimize inbreeding and positively influence levels of genetic diversity within populations. Rock-wallabies are highly philopatric mid-sized mammals whose strong dependence on rocky terrain has resulted in series of discreet, small colonies in the landscape. Populations show no signs of inbreeding and maintain high levels of genetic diversity despite strong patterns of limited gene flow within and among colonies. We used this species to investigate the importance of mating dispersal and breeding group structure to inbreeding avoidance within a 'small' population. We examined the spatial patterns of mating dispersal, the extent of kinship within breeding groups, and the degree of relatedness among brush-tailed rock-wallaby breeding pairs within a colony in southeast Queensland. Parentage data revealed remarkably restricted mating dispersal and strong breeding group structuring for a mid-sized mammal. Breeding groups showed significant levels of female kinship with evidence of male dispersal among groups. We found no evidence for inbreeding avoidance through mate choice; however, anecdotal data suggest the importance of life history traits to inbreeding avoidance between first-degree relatives. We suggest that the restricted pattern of mating dispersal and strong breeding group structuring facilitates inbreeding avoidance within colonies. These results provide insight into the population structure and maintenance of genetic diversity within colonies of the threatened brush-tailed rock-wallaby.     

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.     

Mating patterns and pollen dispersal in a heterodichogamous tree, Juglans mandshurica (Juglandaceae)

Mating patterns in heterodichogamous species are generally considered to be disassortative between flowering morphs, but this hypothesis has hitherto not been vigorously tested. Here, mating patterns and pollen dispersal were studied in Juglans mandshurica, a heterodichogamous wind-pollinated species that is widely distributed in northern and north-eastern China. Paternity analyses carried out on 11 microsatellite loci were used to estimate morph-specific rates of outcrossing and disassortative mating. Pollen dispersal and genetic structure were also investigated in the population under study. The mating pattern of J. mandshurica was highly outcrossing and disassortative. Pairwise values of intramorph relatedness were much higher than those of intermorph relatedness, and a low level of biparental inbreeding was detected. There was no significant difference in outcrossing and disassortative mating rates between the two morphs. The effective pollen dispersal distribution showed an excess of near-neighbor matings, and most offspring of individual trees were sired by one or two nearby trees. These results corroborate the previous suggestion that mating in heterodichogamous plant species is mainly disassortative between morphs, which not only prevents selfing but also effectively reduces intramorph inbreeding.     

Genetic diversity and sex‐bias dispersal of plateau pika in Tibetan plateau

Dispersal is an important aspect in organism's life history which could influence the rate and outcome of evolution of organism. Plateau pika is the keystone species in community of grasslands in Tibetan Plateau. In this study, we combine genetic and field data to character the population genetic pattern and dispersal dynamics in plateau pika (Ochotona curzoniae). Totally, 1,352 individual samples were collected, and 10 microsatellite loci were analyzed. Results revealed that plateau pika possessed high genetic diversity and inbreeding coefficient in a fine‐scale population. Dispersal distance is short and restricted in about 20 m. An effective sex‐biased dispersal strategy is employed by plateau pika: males disperse in breeding period for mating while females do it after reproduction for offspring and resource. Inbreeding avoiding was shown as the common driving force of dispersal, together with the other two factors, environment and resource. In addition, natal dispersal is female biased. More detailed genetic analyzes are needed to confirm the role of inbreeding avoidance and resource competition as ultimate cause of dispersal patterns in plateau pika.     

Colonization and dispersal in a social species, the Bechstein's bat (Myotis bechsteinii)

Metapopulation genetic models consider that colonization and dispersal are distinct behaviours. However, whether colonization and dispersal indeed reflect different biological processes in nature is unclear. One possibility to test this assumption is to assess patterns of autosomal and mitochondrial genetic structure in species with strict female philopatry, such as the communally breeding Bechstein's bat. In this species, mitochondrial DNA can spread only when females establish new colonies, and autosomal DNA is transmitted among colonies only when females mate with solitary males born in foreign colonies. Investigating the genetic structure among 37 colonies, we found that autosomal genes followed an island model on a regional scale and a model of isolation by distance on a larger geographical scale. In contrast, mitochondrial genetic structure revealed no pattern of isolation by distance at a large scale but exhibited an effect of ecological barriers on a regional scale. Our results provide strong empirical evidence that colonization and dispersal do not follow the same behavioural rules in this bat, supporting the assumption of metapopulation genetic models.     

The hidden matrilineal structure of a solitary lemur: implications for primate social evolution

Kin selection affects many aspects of social behaviour, especially in gregarious animals in which relatives are permanently associated. In most group-living primates with complex social behaviour, females are philopatric and organized into matrilines. Models of primate social evolution assume that females in solitary primates are also organized into matrilines. We examined the genetic structure and the mating system of a population of Coquerel's dwarf lemur (Mirza coquereli), a solitary primate from Madagascar, to test this assumption. Our genetic and behavioural analyses revealed that this population of solitary individuals is indeed structured into matrilines, even though this pattern was not predicted by behavioural data. Specifically, females sharing a mitochondrial DNA haplotype were significantly clustered in space and the average genetic and geographical distances among them were negatively correlated. Not all females were philopatric, but there is no evidence for the successful settlement of dispersing females. Although not all adult males dispersed from their natal range, they were not significantly clustered in space and all of them roamed widely in search of oestrous females. As a result, paternity was widely spread among males and mixed paternities existed, indicating that scramble competition polygyny is the mating system of this species. Our data therefore revealed facultative dispersal in both sexes with a strong bias towards female philopatry in this primitive primate. We further conclude that complex kinship structures also exist in non-gregarious species, where their consequences for social behaviour are not obvious.     

Gene dispersal and outbreeding in a philopatric mammal

Extensive mark-recapture data from banner-tailed kangaroo rats, Dipodomys spectabilis, have shown that both males and females are highly philopatric and suggest the possibility of close inbreeding. However, indirect analyses based on genetic structure appear to contradict direct observations, suggesting longer dispersal distances. Using microsatellite genotypes from most members of a banner-tailed kangaroo rat population during five successive breeding seasons, we ask how relatedness is influenced by dispersal and how it in turn influences mating patterns. The data confirm that, because of philopatry, neighbours are often close relatives. However, patterns of parentage also show that the average distance between mates is large relative to natal dispersal distances and larger than the average distance between nearest opposite-sexed neighbours. Females' mates were often not their nearest male neighbour and many were less related than the nearest male neighbour. We detected multiple paternity in some females' litters; both sexes produce offspring with multiple mates within and between breeding seasons. At the population level, heterozygosities were high and estimates of F were low, indicating that levels of inbreeding were low. Using individual inbreeding coefficients of all juveniles to estimate their parents' relatedness, we found that parental relatedness was significantly lower than relatedness between nearest opposite-sexed adult neighbours. Thus in philopatric populations, long breeding forays can cause genes to move further than individuals disperse, and polyandry may serve to reduce relatedness between mates.     

Spatial genetic relationships in a population of the Japanese wood mouse Apodemus argenteus

Space-related relationships between individuals were investigated during the breeding season in a natural population of Apodemus argenteus (Temminck) by using the catch-mark-release method and microsatellite DNA markers. Several overlapping patterns of home ranges in breeding males and females were observed. Although this species is thought to be monogamous, DNA analysis revealed polygynous mating. In adults, relatedness between sexes was generally low and no apparent spatial genetic structure was observed. In juveniles, however, relatedness and geographical distance be-tween individuals were significantly negatively correlated. The relatedness between adult females decreased with distance, whereas there was not such a correlation in males. Long-distance movements were observed in current-year-born males. The differences in spatial genetic structure between adults and juveniles are thought to be produced by male-biased natal dispersal. An erratum to this article can be found at     

Fine‐scale genetic structure reflects sex‐specific dispersal strategies in a population of sociable weavers (Philetairus socius)

Dispersal is a critical driver of gene flow, with important consequences for population genetic structure, social interactions and other biological processes. Limited dispersal may result in kin‐structured populations in which kin selection may operate, but it may also increase the risk of kin competition and inbreeding. Here, we use a combination of long‐term field data and molecular genetics to examine dispersal patterns and their consequences for the population genetics of a highly social bird, the sociable weaver (Philetairus socius), which exhibits cooperation at various levels of sociality from nuclear family groups to its unique communal nests. Using 20 years of data, involving capture of 6508 birds and 3151 recaptures at 48 colonies, we found that both sexes exhibit philopatry and that any dispersal occurs over relatively short distances. Dispersal is female‐biased, with females dispersing earlier, further, and to less closely related destination colonies than males. Genotyping data from 30 colonies showed that this pattern of dispersal is reflected by fine‐scale genetic structure for both sexes, revealed by isolation by distance in terms of genetic relatedness and significant genetic variance among colonies. Both relationships were stronger among males than females. Crucially, significant relatedness extended beyond the level of the colony for both sexes. Such fine‐scale population genetic structure may have played an important role in the evolution of cooperative behaviour in this species, but it may also result in a significant inbreeding risk, against which female‐biased dispersal alone is unlikely to be an effective strategy.     

Microgeographic socio-genetic structure of an African cooperative breeding passerine revealed: integrating behavioural and genetic data

Dispersal can be motivated by multiple factors including sociality. Dispersal behaviour affects population genetic structure that in turn reinforces social organization. We combined observational information with individual-based genetic data in the Karoo scrub-robin, a facultative cooperatively breeding bird, to understand how social bonds within familial groups affect mating patterns, cause sex asymmetry in dispersal behaviour and ultimately influence the evolution of dispersal. Our results revealed that males and females do not have symmetrical roles in structuring the population. Males are extremely philopatric and tend to delay dispersal until they gain a breeding position within a radius of two territories around the natal site. By contrast, females dispersed over larger distances, as soon as they reach independence. This resulted in male neighbourhoods characterized by high genetic relatedness. The long-distance dispersal strategy of females ensured that Karoo scrub-robins do not pair with relatives thereby compensating for male philopatry caused by cooperation. The observed female-biased strategy seems to be the most prominent mechanism to reduce the risk of inbreeding that characterizes social breeding system. This study demonstrates that tying together ecological data, such as breeding status, determining social relationships with genetic data, such as kinship, provides valuable insights into the proximate causes of dispersal, which are central to any evolutionary interpretation.     

Natal dispersal and genetic structure in a population of the European wild rabbit (Oryctolagus cuniculus)

A combination of behavioural observation, DNA fingerprinting, and allozyme analysis were used to examine natal dispersal in a wild rabbit population. Rabbits lived in territorial, warren based social groups. Over a 6-year period, significantly more male than female rabbits moved to a new social group before the start of their first breeding season. This pattern of female philopatry and male dispersal was reflected in the genetic structure of the population. DNA fingerprint band-sharing coefficients were significantly higher for females within the same group than for females between groups, while this was not the case for males. Wrighfs inbreeding coefficients were calculated from fingerprint band-sharing values and compared to those obtained from allozyme data. There was little correlation between the relative magnitudes of the F-statistics calculated using the two techniques for comparisons between different social groups. In contrast, two alternative methods for calculating F_ST from DNA fingerprints gave reasonably concordant values although those based on band-sharing were consistently lower than those calculated by an ‘allele’ frequency approach. A negative F_IS value was obtained from allozyme data. Such excess heterozygosity within social groups is expected even under random mating given the social structure and sex-biased dispersal but it is argued that the possibility of behavioural avoidance of inbreeding should not be discounted in this species. Estimates of genetic differentiation obtained from allozyme and DNA fingerprint data agreed closely with reported estimates for the yellow-bellied marmot, a species with a very similar social structure to the European rabbit.