Dispersal, philopatry and intergroup relatedness: fine-scale genetic structure in the white-breasted thrasher, Ramphocinclus brachyurus

Dispersal is a fundamental process influencing evolution, social behaviour, and the long-term persistence of populations. We use both observational and genetic data to investigate dispersal, kin-clustering and intergroup relatedness in the white-breasted thrasher, Ramphocinclus brachyurus, a cooperatively breeding bird that is globally endangered. Mark-resighting data suggested sex-biased dispersal, with females dispersing over greater distances while males remained philopatric. Accordingly, spatial autocorrelation analysis showed highly significant fine-scale genetic structure among males, but not among females. This fine-scale genetic structuring of the male population resulted in very high levels of relatedness between dominant males at neighbouring nests, similar to that seen within cooperative groups in many species where kin selection is cited as a cause of cooperation. By implication, between-group as well as within-group cooperation may be important, potentially creating a feedback loop in which short-distance dispersal by males leads to the formation of male kin clusters that in turn facilitate nepotistic interactions and favour further local recruitment. The strength of spatial autocorrelation, as measured by the autocorrelation coefficient, r, was approximately two to three times greater than that reported in previous studies of animals. Relatively short dispersal distances by both males and females may have a negative impact on the white-breasted thrasher's ability to colonize new areas, and may influence the long-term persistence of isolated populations. This should be taken into account when designating protected areas or selecting sites for habitat restoration.     

Dispersal Patterns of Orang-utans (<Emphasis Type="BoldItalic">Pongo</Emphasis> spp.) in a Bornean Peat-swamp Forest

Knowledge regarding dispersal patterns in great apes may help in understanding the evolution of dispersal patterns and social grouping in early hominoids, as well as in our own species. However, the social structure and dispersal system of orang-utans (Pongo spp.) remains little understood despite past research. We addressed this question by conducting genetic analyses on a wild orang-utan (Pongo pygmaeus wurmbii) population from the Sabangau peat-swamp in Borneo. We estimated pairwise relatedness among 16 adult individuals using 19 polymorphic microsatellite markers. Mean relatedness among females was significantly higher than in males, irrespective of the relatedness estimator used, following the pattern predicted for male dispersal. Our results support field observations that average dispersal distance for females is less than for males, suggesting that female orang-utans are philopatric, whereas males disperse. This contrasts with previous findings from other sites where anthropogenic influences were present. Based on qualitative mitochondrial DNA analyses, it appears that unflanged adult males show some degree of site fidelity compared to flanged males. Thus, male orang-utans may disperse permanently from their natal range once they are fully flanged. Male-biased dispersal and female philopatry in orang-utans differ from those of extant African apes and are more similar to many Old World monkey species. Hence we hypothesize that this system may represent the ancestral state of early hominoids.     

No difference between the sexes in fine-scale spatial genetic structure of roe deer

Background

Data on spatial genetic patterns may provide information about the ecological and behavioural mechanisms underlying population structure. Indeed, social organization and dispersal patterns of species may be reflected by the pattern of genetic structure within a population.

Methodology/Principal Findings

We investigated the fine-scale spatial genetic structure of a roe deer (Capreolus capreolus) population in Trois-Fontaines (France) using 12 microsatellite loci. The roe deer is weakly polygynous and highly sedentary, and can form matrilineal clans. We show that relatedness among individuals was negatively correlated with geographic distance, indicating that spatially proximate individuals are also genetically close. More unusually for a large mammalian herbivore, the link between relatedness and distance did not differ between the sexes, which is consistent with the lack of sex-biased dispersal and the weakly polygynous mating system of roe deer.

Conclusions/Significance

Our results contrast with previous reports on highly polygynous species with male-biased dispersal, such as red deer, where local genetic structure was detected in females only. This divergence between species highlights the importance of socio-spatial organization in determining local genetic structure of vertebrate populations.     

(Not) far from home: No sex bias in dispersal,but limited genetic patch size,in an endangered species,the Spotted Turtle (Clemmys guttata)

Sex-biased dispersal is common in many animals, with male-biased dispersal often found in studies of mammals and reptiles, including interpretations of spatial genetic structure, ostensibly as a result of male–male competition and a lack of male parental care. Few studies of sex-biased dispersal have been conducted in turtles, but a handful of studies, in saltwater turtles and in terrestrial turtles, have detected male-biased dispersal as expected. We tested for sex-biased dispersal in the endangered freshwater turtle, the spotted turtle (Clemmys guttata) by investigating fine-scale genetic spatial structure of males and females. We found significant spatial genetic structure in both sexes, but the patterns mimicked each other. Both males and females typically had higher than expected relatedness at distances <25 km, and in many distance classes greater than 25 km, less than expected relatedness. Similar patterns were apparent whether we used only loci in Hardy–Weinberg equilibrium (n = 7) or also included loci with potential null alleles (n = 5). We conclude that, contrary to expectations, sex-biased dispersal is not occurring in this species, possibly related to the reverse sexual dimorphism in this species, with females having brighter colors. We did, however, detect significant spatial genetic structure in males and females, separate and combined, showing philopatry within a genetic patch size of <25 km in C. guttata, which is concerning for an endangered species whose populations are often separated by distances greater than the genetic patch size.     

Resources, not Kinship, Determine Social Patterning in the Territorial Gunnison's prairie Dog (Cynomys gunnisoni)

In this study, we describe patterns of relatedness in Gunnison's prairie dog ( Cynomys gunnisoni ) social groups. Kin selection is often cited as a mechanism for the evolution and maintenance of social groups, and Gunnison's prairie dog females are occasionally described as being strongly philopatric. Overall, randomization tests revealed that females within territorial groups were not more closely related to each other than expected at random. A similar pattern was found among males and between males and females, indicating that there was no sex-biased dispersal occurring in these populations. Ecological variables measured in this study, such as food abundance and food dispersion, were not correlated with relatedness. In addition, territory size and density/m² did not correlate significantly with relatedness. Although there was variability in the spatial overlap among individuals within groups, there was no indication that relatedness explained this variation. These results suggest that kin selection is not maintaining social groups in these populations, but that competition for access to resources required by both males and females may explain dispersal and social group patterns in these populations.     

No evidence for female kin association,indications for extragroup paternity,and sex‐biased dispersal patterns in wild western gorillas

Characterizing animal dispersal patterns and the rational behind individuals’ transfer choices is a long‐standing question of interest in evolutionary biology. In wild western gorillas (Gorilla gorilla), a one‐male polygynous species, previous genetic findings suggested that, when dispersing, females might favor groups with female kin to promote cooperation, resulting in higher‐than‐expected within‐group female relatedness. The extent of male dispersal remains unclear with studies showing conflicting results. To investigate male and female dispersal patterns and extragroup paternity, we analyzed long‐term field observations, including female spatial proximity data, together with genetic data (10 autosomal microsatellites) on individuals from a unique set of four habituated western gorilla groups, and four additional extragroup males (49 individuals in total). The majority of offspring (25 of 27) were sired by the group male. For two offspring, evidence for extragroup paternity was found. Contrarily to previous findings, adult females were not significantly more related within groups than across groups. Consistently, adult female relatedness within groups did not correlate with their spatial proximity inferred from behavioral data. Adult females were similarly related to adult males from their group than from other groups. Using R _ST statistics, we found significant genetic structure and a pattern of isolation by distance, indicating limited dispersal in this species. Comparing relatedness among females and among males revealed that males disperse farer than females, as expected in a polygamous species. Our study on habituated western gorillas shed light on the dispersal dynamics and reproductive behavior of this polygynous species and challenge some of the previous results based on unhabituated groups.     

The lengths birds will go to avoid incest

Cooperatively breeding species, in which some individuals help others to rear their offspring, face a high risk of inbreeding because of close relatedness within social groups. Many species circumvent this problem via sex-biased dispersal, in which one sex is more likely to disperse (and to disperse further), while the other stays and helps. In the absence of sex-biased dispersal, more complex dispersal patterns can arise, based on kin recognition. However, this can also present challenges when dispersal distances are short, leading to clusters of relatives on neighbouring territories. In this issue, Nelson-Flower et al. (2012) break important new ground by unravelling adaptive incest-avoidance mechanisms in a cooperatively breeding bird without sex-biased dispersal. They provide an elegant demonstration of finely tuned dispersal distances together with cognitively based methods for knowing whom to avoid as mates.     

Population Genetics,Dispersal, and Kinship Among Wild Squirrel Monkeys (Saimiri sciureus macrodon): Preferential Association Between Closely Related Females and Its Implications for Insect Prey Capture Success

Little genetic information is available to evaluate hypotheses concerning the parameters that affect population genetic structure in primate taxa that exhibit interspecific variation in social systems, such as squirrel monkeys (Saimiri). Here, we used genetic data to assess dispersal patterns, kin structure, and preferential association with same-sex kin in a wild population of Saimiri sciureus macrodon. We also analyzed behavioral data to assess whether individuals that maintain shorter interindividual distances show increased insect foraging success. If there was greater male than female dispersal, then we expected mean pairwise relatedness, F _ST values, and intragroup mean corrected assignment indices to be greater among adult females than among adult males. We also expected matrices of pairwise affinity indices (PAIs) for “association” (time spent ≤5 m) and “proximity” (time spent ≤10 m) among female dyads to positively correlate with a matrix of female pairwise relatedness. Not only did we find support for female philopatry, but we also found significant positive relationships between the relatedness matrix and each of the PAI matrices: females were more likely to be associated with (and proximal to) close female relatives than more distant relatives or unrelated individuals. Foraging analyses revealed that females had higher insect capture rates than males, and this sex difference may be related to a smaller mean interindividual distance among closely related female group members. Our result shows how estimates of genetic relatedness are useful for testing predictions regarding the evolution of sex-biased dispersal patterns, as well as potential relationships between kin-biased social behaviors and foraging success.     

Fine-scale spatial genetic correlation analyses reveal strong female philopatry within a brush-tailed rock-wallaby colony in southeast Queensland

We combine spatial data on home ranges of individuals and microsatellite markers to examine patterns of fine-scale spatial genetic structure and dispersal within a brush-tailed rock-wallaby (Petrogale penicillata) colony at Hurdle Creek Valley, Queensland. Brush-tailed rock-wallabies were once abundant and widespread throughout the rocky terrain of southeastern Australia; however, populations are nearly extinct in the south of their range and in decline elsewhere. We use pairwise relatedness measures and a recent multilocus spatial autocorrelation analysis to test the hypotheses that in this species, within-colony dispersal is male-biased and that female philopatry results in spatial clusters of related females within the colony. We provide clear evidence for strong female philopatry and male-biased dispersal within this rock-wallaby colony. There was a strong, significant negative correlation between pairwise relatedness and geographical distance of individual females along only 800 m of cliff line. Spatial genetic autocorrelation analyses showed significant positive correlation for females in close proximity to each other and revealed a genetic neighbourhood size of only 600 m for females. Our study is the first to report on the fine-scale spatial genetic structure within a rock-wallaby colony and we provide the first robust evidence for strong female philopatry and spatial clustering of related females within this taxon. We discuss the ecological and conservation implications of our findings for rock-wallabies, as well as the importance of fine-scale spatial genetic patterns in studies of dispersal behaviour.     

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     

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.     

Sex-related spatial kin structure in a spring population of grey-sided voles Clethrionomys rufocanus as revealed by mitochondrial and microsatellite DNA analyses

Polymerase chain reaction-directed mitochondria (mt) and microsatellite DNA analyses were performed to examine the kin structure in a spring population of grey-sided voles Clethrionomys rufocanus in Hokkaido, Japan. The spatial distribution of 81 voles in a trapping grid (about 1 ha) was estimated by using the catch-mark-release method. DNA samples were extracted from the toes clipped for individual identification. Maternal lineages of voles were unequivocally determined by the mtDNA haplotypes, as identified by nucleotide sequencing of the control region. Relatedness between individuals was estimated based on the genotype and allele frequencies at several microsatellite loci. Although the distribution of voles was uniform within the grid, neighbouring females were frequently from the same maternal lineage. Relatedness values between females correlated negatively with geographical distances. Combination of the two molecular markers revealed four clusters of closely related, matrilineal females in the population, whereas no such cluster was apparent in males. The present study first demonstrated a sex-related spatial kin structure in a natural population of the grey-sided vole.     

Cryptic behaviours, inverse genetic landscapes, and spatial avoidance of inbreeding in the Pacific jumping mouse

Although the behaviour of individuals is known to impact the genetic make-up of a population, observed behavioural patterns do not always correspond to patterns of genetic structure. In particular, philopatric or dispersal-limited species often display lower-than-expected values of relatedness or inbreeding suggestive of the presence of cryptic migration, dispersal, or mating behaviours. I used a combination of microsatellite and mark-recapture data to test for the influence of such behaviours in a dispersal-limited species, the Pacific jumping mouse, within a semi-isolated population over three seasons. Despite short dispersal distances and a low rate of first generation migrants, heterozygosities were high and inbreeding values were low. Dispersal was male-biased; interestingly however, this pattern was only present when dispersal was considered to include movement away from paternal home range. Not unexpectedly, males were polygynous; notably, some females were also found to be polyandrous, selecting multiple neighbouring mates for their single annual litter. Patterns of genetic structure were consistent with these more inconspicuous behavioural patterns. Females were more closely related than males and isolation by distance was present only in females. Furthermore, detailed genetic landscapes revealed the existence of strong, significant negative correlations, with areas of low genetic distance among females overlapping spatially with areas of high genetic distance among males. These results support the hypothesis that the detected cryptic components of dispersal and mating behaviour are reducing the likelihood of inbreeding in this population through paternally driven spatial mixing of male genotypes and polyandry of females.     

Genetic structure in a solitary rodent (Ctenomys talarum): implications for kinship and dispersal

The genetic structure of a population provides critical insights into patterns of kinship and dispersal. Although genetic evidence of kin structure has been obtained for multiple species of social vertebrates, this aspect of population biology has received considerably less attention among solitary taxa in which spatial and social relationships are unlikely to be influenced by kin selection. Nevertheless, significant kin structure may occur in solitary species, particularly if ecological or life history traits limit individual vagility. To explore relationships between genetic structure, kinship, and dispersal in a solitary vertebrate, we compared patterns of genetic variation in two demographically distinct populations of the talar tuco-tuco (Ctenomys talarum), a solitary species of subterranean rodent from Buenos Aires Province, Argentina. Based on previous field studies of C. talarum at Mar de Cobo (MC) and Necochea (NC), we predicted that natal dispersal in these populations is male biased, with dispersal distances for males and females being greater at NC. Analyses of 12 microsatellite loci revealed that in both populations, kin structure was more apparent among females than among males. Between populations, kinship and genetic substructure were more pronounced at MC. Thus, our findings were consistent with predicted patterns of dispersal for these animals. Collectively, these results indicate that populations of this solitary species are characterized by significant kin structure, suggesting that, even in the absence of sociality and kin selection, the spatial distributions and movements of individuals may significantly impact patterns of genetic diversity among conspecifics.     

Male affiliation, cooperation and kinship in wild chimpanzees

Long-term field research has revealed that male chimpanzees, Pan troglodytes, affiliate and cooperate in several contexts. Assuming close genetic relationship among males, affiliative and cooperative behaviour have been hypothesized to evolve through the indirect effects of kin selection. We tested the hypothesis that matrilineal genetic relatedness affects patterns of male social affiliation and cooperation in an unusually large community of chimpanzees at the Ngogo study site, Kibale National Park, Uganda. Field observations indicated that six behavioural measures of affiliation and cooperation among 23 adult males were significantly correlated with each other. Sequences of the first hypervariable portion of the mtDNA genome revealed that three pairs of males and one quintet shared mtDNA haplotypes. Matrix permutation tests using behavioural and genetic data showed that males that affiliated and cooperated with each other were not closely related through the maternal line. These findings add to a growing body of empirical evidence that suggest kinship plays an ancillary role in structuring patterns of wild chimpanzee behaviour within social groups. Copyright 2000 The Association for the Study of Animal Behaviour.     

Mother–offspring distances reflect sex differences in fine‐scale genetic structure of eastern grey kangaroos

Natal dispersal affects life history and population biology and causes gene flow. In mammals, dispersal is usually male‐biased so that females tend to be philopatric and surrounded by matrilineal kin, which may lead to preferential associations among female kin. Here we combine genetic analyses and behavioral observations to investigate spatial genetic structure and sex‐biased dispersal patterns in a high‐density population of mammals showing fission–fusion group dynamics. We studied eastern grey kangaroos (Macropus giganteus) over 2 years at Wilsons Promontory National Park, Australia, and found weak fine‐scale genetic structure among adult females in both years but no structure among adult males. Immature male kangaroos moved away from their mothers at 18–25 months of age, while immature females remained near their mothers until older. A higher proportion of male (34%) than female (6%) subadults and young adults were observed to disperse, although median distances of detected dispersals were similar for both sexes. Adult females had overlapping ranges that were far wider than the maximum extent of spatial genetic structure found. Female kangaroos, although weakly philopatric, mostly encounter nonrelatives in fission–fusion groups at high density, and therefore kinship is unlikely to strongly affect sociality.     

Dispersal,Mating Events and Fine-Scale Genetic Structure in the Lesser Flat-Headed Bats

Population genetic structure has important consequences in evolutionary processes and conservation genetics in animals. Fine-scale population genetic structure depends on the pattern of landscape, the permanent movement of individuals, and the dispersal of their genes during temporary mating events. The lesser flat-headed bat (Tylonycteris pachypus) is a nonmigratory Asian bat species that roosts in small groups within the internodes of bamboo stems and the habitats are fragmented. Our previous parentage analyses revealed considerable extra-group mating in this species. To assess the spatial limits and sex-biased nature of gene flow in the same population, we used 20 microsatellite loci and mtDNA sequencing of the ND2 gene to quantify genetic structure among 54 groups of adult flat-headed bats, at nine localities in South China. AMOVA and F _ST estimates revealed significant genetic differentiation among localities. Alternatively, the pairwise F _ST values among roosting groups appeared to be related to the incidence of associated extra-group breeding, suggesting the impact of mating events on fine-scale genetic structure. Global spatial autocorrelation analyses showed positive genetic correlation for up to 3 km, indicating the role of fragmented habitat and the specialized social organization as a barrier in the movement of individuals among bamboo forests. The male-biased dispersal pattern resulted in weaker spatial genetic structure between localities among males than among females, and fine-scale analyses supported that relatedness levels within internodes were higher among females than among males. Finally, only females were more related to their same sex roost mates than to individuals from neighbouring roosts, suggestive of natal philopatry in females.     

Fine-scale genetic structure and dispersal in cooperatively breeding apostlebirds

In cooperatively breeding species, restricted dispersal of offspring leads to clustering of closely related individuals, increasing the potential both for indirect genetic benefits and inbreeding costs. In apostlebirds (Struthidea cinerea), philopatry by both sexes results in the formation of large (up to 17 birds), predominantly sedentary breeding groups that remain stable throughout the year. We examined patterns of relatedness and fine-scale genetic structure within a population of apostlebirds using six polymorphic microsatellite loci. We found evidence of fine-scale genetic structure within the study population that is consistent with behavioural observations of short-distance dispersal, natal philopatry by both sexes and restricted movement of breeding groups between seasons. Global F(ST) values among breeding groups were significantly positive, and the average level of pairwise relatedness was significantly higher for individuals within groups than between groups. For individuals from different breeding groups, geographical distance was negatively correlated with pairwise relatedness and positively correlated with pairwise F(ST). However, when each sex was examined separately, this pattern was significant only among males, suggesting that females may disperse over longer distances. We discuss the potential for kin selection to influence the evolution and maintenance of cooperative breeding in apostlebirds. Our results demonstrate that spatial genetic structural analysis offers a useful alternative to field observations in examining dispersal patterns of cooperative breeders.     

Sex differences in dispersal and the evolution of helping and harming

In this article, we explore the impact of sex-biased dispersal on local relatedness and on selection for helping and harming behavior among males and females. We show that in a patch-structured population, when there is a marked sex bias in dispersal, selection will almost always favor harming behavior among individuals of the sex more prone to dispersal. This result holds regardless of the effects of mating skew or overlapping generations. Selection may well also favor helping behavior among individuals of the philopatric sex, particularly if there is generational overlap, but this is less likely to occur if individuals of the philopatric sex compete more intensely for fewer breeding opportunities. In this last case, if generational overlap is low and mating skew pronounced, the result may be selection for harming behavior among both males and females. In general, the rate of dispersal and the level of relatedness among individuals of one sex do not reliably predict their level of helping or harming behavior; selection on either males or females depends on the dispersal of both sexes.     

Fine-scale genetic structure of a long-lived reptile reflects recent habitat modification

Anthropogenic habitat fragmentation — ubiquitous in modern ecosystems — has strong impacts on gene flow and genetic population structure. Reptiles may be particularly susceptible to the effects of fragmentation because of their extreme sensitivity to environmental conditions and limited dispersal. We investigate fine-scale spatial genetic structure, individual relatedness, and sex-biased dispersal in a large population of a long-lived reptile (tuatara, Sphenodon punctatus) on a recently fragmented island. We genotyped individuals from remnant forest, regenerating forest, and grassland pasture sites at seven microsatellite loci and found significant genetic structuring (R_ST = 0.012) across small distances (< 500 m). Isolation by distance was not evident, but rather, genetic distance was weakly correlated with habitat similarity. Only individuals in forest fragments were correctly assignable to their site of origin, and individual pairwise relatedness in one fragment was significantly higher than expected. We did not detect sex-biased dispersal, but natural dispersal patterns may be confounded by fragmentation. Assignment tests showed that reforestation appears to have provided refuges for tuatara from disturbed areas. Our results suggest that fine-scale genetic structuring is driven by recent habitat modification and compounded by the sedentary lifestyle of these long-lived reptiles. Extreme longevity, large population size, simple social structure and random dispersal are not strong enough to counteract the genetic structure caused by a sedentary lifestyle. We suspect that fine-scale spatial genetic structuring could occur in any sedentary species with limited dispersal, making them more susceptible to the effects of fragmentation.