Genetic relatedness and female spatial organization in a solitary carnivore,the raccoon,Procyon lotor

Among mammals, some of the most common types of cohesive social groupings originate from natal philopatry through the extended mother family. This retention of females within social groups (i.e. the nonrandom dispersion of female relatives in space) should affect population genetic structure. We examined the relationship between genetic relatedness and female spatial organization in a wild population of the North-American raccoon, Procyon lotor, a solitary carnivore in east Tennessee. Multilocus genetic band-sharing data and 3(1/2) years of radiotelemetry observations were used to study the spatial and genetic relationships among 38 adult females. DNA amplification employing primers of arbitrary sequence (random amplified polymorphic DNA; RAPD) indicated that female philopatry in raccoons led to a greater likelihood of neighbours being more related than expected by chance. Genetic distance based on RAPD band frequency was positively correlated with spatial distance among females (P = 0.0001) and genetic similarity was positively correlated with the extent of home-range overlap (P = 0.0028). Philopatry seemed biased towards females; average female-female similarities were greater than average male-male similarities (P = 0.0001), or average male-female similarities (P = 0.0001). High home-range overlap among some females with low or moderate levels of band sharing indicated that maternal inheritance of space was not a prerequisite for establishing or sharing home ranges. Female philopatry was the most probable explanation for the nonrandom spatial and genetic association of raccoons in east Tennessee.     

Spatial relatedness and brood parasitism in a female-philopatric bird population

The spatial structure of relatedness between individuals ina population can be crucial for social selection and evolution.Here we analyze a female alternative reproductive tactic, conspecificbrood parasitism, in relation to spatial relatedness among femalesin a Baltic Sea population of the common eider Somateria mollissima.The role of relatedness in brood parasitism is debated: somemodels predict parasite avoidance of related hosts, others predicthost–parasite relatedness. We estimate pairwise relatednessfrom protein fingerprinting of egg albumen in 156 nests, withpairwise nest distances ranging from 1 to 6 km. Relatednessincreases significantly from the longest distances to an averageof r 0.09 below 20 m. Brood parasitism is common, and averagepairwise relatedness between host and parasite is estimatedat 0.18–0.21. Parasites thus do not avoid relatives, andcombined with the findings of a similar study in another eiderpopulation, the results show that mean host–parasite relatednessis higher than that among close neighbors. High host–parasiterelatedness is therefore not an effect of natal philopatry alone;some other form of kin bias is also involved. Recognition andassociation between birth nest mates is a candidate mechanismfor further study.     

Introduction history overrides social factors in explaining genetic structure of females in Mediterranean mouflon

Fine‐scale spatial genetic structure of populations results from social and spatial behaviors of individuals such as sex‐biased dispersal and philopatry. However, the demographic history of a given population can override such socio‐spatial factors in shaping genetic variability when bottlenecks or founder events occurred in the population. Here, we investigated whether socio‐spatial organization determines the fine‐scale genetic structure for both sexes in a Mediterranean mouflon (Ovis gmelini musimon × Ovis sp.) population in southern France 60 years after its introduction. Based on multilocus genotypes at 16 loci of microsatellite DNA (n = 230 individuals), we identified three genetic groups for females and two for males, and concurrently defined the same number of socio‐spatial units using both GPS‐collared individuals (n = 121) and visual resightings of marked individuals (n = 378). The socio‐spatial and genetic structures did not match, indicating that the former was not the main driver of the latter for both sexes. Beyond this structural mismatch, we found significant, yet low, genetic differentiation among female socio‐spatial groups, and no genetic differentiation in males, with this suggesting female philopatry and male‐biased gene flow, respectively. Despite spatial disconnection, females from the north of the study area were genetically closer to females from the south, as indicated by the spatial analysis of the genetic variability, and this pattern was in accordance with the common genetic origin of their founders. To conclude, more than 14 generations later, genetic signatures of first introduction are not only still detectable among females, but they also represent the main factor shaping their present‐time genetic structure.     

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.     

Flexible social structure of a desert rodent, Rhombomys opimus: philopatry, kinship, and ecological constraints

We tested hypotheses based on philopatry, kinship, and ecologicalconstraints to explain sociality in a semifossorial desert rodent,the great gerbil, Rhombomys opimus. Data were collected in thefield in Uzbekistan in the spring and fall of 1996 and 1998–2004.Population densities fluctuated dramatically with high turnoverin both males and females to reveal that dispersal and socialstructure were density dependent. Fewer gerbils dispersed athigher densities and members of family groups dispersed together.A majority of females lived in groups at high densities, butas population densities declined, proportionally more femaleswere solitary. DNA analysis revealed that group-living femaleswere genetically similar, whereas solitary females visited bythe same male, as well as adult males and females in the samefamily group, were usually not genetically similar. Reproductivesuccess as measured by the number of emergent pups and survivalof juveniles during the summer drought was not related to groupsize or whether females were philopatric. A majority of femalesin family groups reproduced, and all females engaged in cooperativebehaviors. We accepted three hypotheses to explain fluctuationsin group formation in the great gerbil: variation in food abundanceand distribution, habitat saturation, and kinship. We concludethat great gerbils are facultatively social. Flexible socialbehavior may be adaptive in unpredictable desert conditions.Females live solitarily under conditions of limited food andhigh mortality that disrupt social behavior and group formationand share territories with female kin under favorable conditionsfor survival and reproduction when kin groups can be maintained.Males adjust to the distribution of females.     

Fine‐scale genetic structure and helping decisions in a cooperatively breeding bird

In animal societies, characteristic demographic and dispersal patterns may lead to genetic structuring of populations, generating the potential for kin selection to operate. However, even in genetically structured populations, social interactions may still require kin discrimination for cooperative behaviour to be directed towards relatives. Here, we use molecular genetics and long‐term field data to investigate genetic structure in an adult population of long‐tailed tits Aegithalos caudatus, a cooperative breeder in which helping occurs within extended kin networks, and relate this to patterns of helping with respect to kinship. Spatial autocorrelation analyses reveal fine‐scale genetic structure within our population, such that related adults of either sex are spatially clustered following natal dispersal, with relatedness among nearby males higher than that among nearby females, as predicted by observations of male‐biased philopatry. This kin structure creates opportunities for failed breeders to gain indirect fitness benefits via redirected helping, but crucially, most close neighbours of failed breeders are unrelated and help is directed towards relatives more often than expected by indiscriminate helping. These findings are consistent with the effective kin discrimination mechanism known to exist in long‐tailed tits and support models identifying kin selection as the driver of cooperation.     

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.     

Genetic structure at three spatial scales is consistent with limited philopatry in Ricord's Rock Iguanas (Cyclura ricordii)

Cyclura ricordii is an endemic iguana from Hispaniola Island and is threatened on the IUCN Red List. The main threats are predation by introduced mammals, habitat destruction, and hunting pressure. The present study focused on two nesting sites from Pedernales Province in the Dominican Republic. The hypothesis that natal philopatry influences dispersal and nest‐site selection was tested. Monitoring and sampling took place in 2012 and 2013. Polymorphic markers were used to evaluate whether natal philopatry limits dispersal at multiple spatial scales. Ripley's K revealed that nests were significantly clustered at multiple scales, when both nesting sites were considered and within each nesting site. This suggests a patchy, nonrandom distribution of nests within nest sites. Hierarchical AMOVA revealed that nest‐site aggregations did not explain a significant portion of genetic variation within nesting sites. However, a small but positive correlation between geographic and genetic distance was detected using a Mantel's test. Hence, the relationship between geographic distance and genetic distance among hatchlings within nest sites, while detectable, was not strong enough to have a marked effect on fine‐scale genetic structure. Spatial and genetic data combined determined that the nesting sites included nesting females from multiple locations, and the hypothesis of “natal philopatry” was not supported because females nesting in the same cluster were no more closely related to each other than to other females from the same nesting site. These findings imply that nesting aggregations are more likely associated with cryptic habitat variables contributing to optimal nesting conditions.     

Fine-scale genetic structure of red deer (Cervus elaphus) in a French temperate forest

Despite the classic population genetic view of a population as a network of sub-populations consisting of randomly mating individuals, the mating system and dispersal patterns of social animals affect the distribution of genetic variation on a local scale. The spatially open, forest-dwelling red deer (Cervus elaphus) population at the Petite Pierre National Reserve in north-eastern France is culled annually, with the management aim of maximising the number of adult males in the population, and is a typical example of an exploited red deer population from continental Europe. Through a change in management policy, the number of adult males in the population has increased over time, leading to a reduction in variance of male reproductive success (Bonenfant et al., 2002). In this study, we investigate the fine-scale genetic structure of the population using 14 microsatellite loci and attempt to find evidence for a change in this genetic structure over time. DNA was extracted from bone powder obtained by drilling into antlers and mandibular condyles. DNA was successfully extracted from up to 30-year-old samples, but it was necessary to genotype samples in duplicate to obtain reliable genetic profiles. Our results point towards a pattern of fine-scale spatial structure amongst female red deer in the study area, but not amongst males, as would be expected for a typical mammalian system with male-biased dispersal and female philopatry. In addition, our results hint at a decrease in spatial genetic structure amongst females over time, which might be related to a change in management policy, but small sample size limited the robustness of this conclusion.     

KIN-STRUCTURED COLONIZATION AND SMALL-SCALE GENETIC DIFFERENTIATION IN SILENE DIOICA

We investigated the genetic structure of a single island population of the dioecious plant Silene dioica in the Skeppsvik Archipelago, Umeå, Sweden. The population is less than 10 years old and consists of approximately 700 individuals growing within an area of about 200 m². Despite the small scale of the study, levels of genetic differentiation among contiguous patches are greater than or comparable to what is observed over larger scales in the archipelago. The results suggest that the small-scale structuring occurs during population expansion, soon after island colonization, and that the observed patterns of genetic differentiation can be attributed to the population being substructured into family groups. This family structure results from kin-structured dispersal processes (colonization and migration) as the population expands over the island. As plant densities increase over time, either spatial fusion or temporal fusion of patches reduce the among patch variation. These processes, however, do not completely eradicate the genetic differentiation established by the kin-structured dispersal processes. We discuss some implications of kin structuring for evolution through either kin or interdemic selection.     

Kin in space: social viscosity in a spatially and genetically substructured network

Population substructuring is a fundamental aspect of animal societies. A growing number of theoretical studies recognize that who-meets-whom is not random, but rather determined by spatial relationships or illustrated by social networks. Structural properties of large highly dynamic social systems are notoriously difficult to unravel. Network approaches provide powerful ways to analyse the intricate relationships between social behaviour, dispersal strategies and genetic structure. Applying network analytical tools to a colony of the highly gregarious Galápagos sea lion (Zalophus wollebaeki), we find several genetic clusters that correspond to spatially determined 'network communities'. Overall relatedness was low, and genetic structure in the network can be interpreted as an emergent property of philopatry and seems not to be primarily driven by targeted interactions among highly related individuals in family groups. Nevertheless, social relationships between directly adjacent individuals in the network were stronger among genetically more similar individuals. Taken together, these results suggest that even small differences in the degree of relatedness can influence behavioural decisions. This raises the fascinating prospect that kin selection may also apply to low levels of relatedness within densely packed animal groups where less obvious co-operative interactions such as increased tolerance and stress reduction are important.     

Population genetic insights into the social organization of Guinea baboons (Papio papio): Evidence for female‐biased dispersal

Sex differences in philopatry and dispersal have important consequences on the genetic structure of populations, social groups, and social relationships within groups. Among mammals, male dispersal and female philopatry are most common and closely related taxa typically exhibit similar dispersal patterns. However, among four well‐studied species of baboons, only hamadryas baboons exhibit female dispersal, thus differing from their congenerics, which show female philopatry and close‐knit female social relationships. Until recently, knowledge of the Guinea baboon social system and dispersal pattern remained sparse. Previous observations suggested that the high degree of tolerance observed among male Guinea baboons could be due to kinship. This led us to hypothesize that this species exhibits male philopatry and female dispersal, conforming to the hamadryas pattern. We genotyped 165 individuals from five localities in the Niokolo‐Koba National Park, Senegal, at 14 autosomal microsatellite loci and sequenced a fragment of the mitochondrial hypervariable region I (HVRI) of 55 individuals. We found evidence for higher population structuring in males than in females, as expected if males are the more philopatric sex. A comparison of relatedness between male–male and female–female dyads within and among communities did not yield conclusive results. HVRI diversity within communities was high and did not differ between the sexes, also suggesting female gene flow. Our study is the first comprehensive analysis of the genetic population structure in Guinea baboons and provides evidence for female‐biased dispersal in this species. In conjunction with their multilevel social organization, this finding parallels the observations for human hunter‐gatherers and strengthens baboons as an intriguing model to elucidate the processes that shaped the highly cooperative societies of Homo. Am. J. Primatol. 77:878–889, 2015. © 2015 The Authors. American Journal of Primatology Published by Wiley Periodicals Inc.     

Colonization genetics of an animal-dispersed plant (Vaccinium membranaceum) at Mount St Helens, Washington

Population founding and spatial spread may profoundly influence later population genetic structure, but their effects are difficult to quantify when population history is unknown. We examined the genetic effects of founder group formation in a recently founded population of the animal-dispersed Vaccinium membranaceum (black huckleberry) on new volcanic deposits at Mount St Helens (Washington, USA) 24 years post-eruption. Using amplified fragment length polymorphisms and assignment tests, we determined sources of the newly founded population and characterized genetic variation within new and source populations. Our analyses indicate that while founders were derived from many sources, about half originated from a small number of plants that survived the 1980 eruption in pockets of remnant soil embedded within primary successional areas. We found no evidence of a strong founder effect in the new population; indeed genetic diversity in the newly founded population tended to be higher than in some of the source regions. Similarly, formation of the new population did not increase among-population genetic variance, and there was no evidence of kin-structured dispersal in the new population. These results indicate that high gene flow among sources and long-distance dispersal were important processes shaping the genetic diversity in this young V. membranaceum population. Other species with similar dispersal abilities may also be able to colonize new habitats without significant reduction in genetic diversity or increase in differentiation among populations.     

Female distribution, genetic relatedness, and fostering behaviour in harbour seals, Phoca vitulina

Although harbour seals may not recognize their relatives, relatives could be chosen preferentially for fostering (i.e. kin selection) if harbour seals display natal philopatry coupled with breeding site fidelity, and thus kin are clustered within the colony. We used behavioural and genetic data to investigate population structure within the Sable Island breeding colony and to test whether harbour seals tend to foster related pups. Adult females on Sable Island showed a high level of breeding-colony site fidelity but low levels of within-colony site fidelity both within and between years. Similarly, although lactating females showed a clumped distribution, group composition was highly variable, suggesting that this study colony was not composed of groups of related animals. DNA fingerprint data supported the hypothesis that female distribution within the colony was not correlated with genetic relatedness. Furthermore, the mean DNA band sharing among foster dyads did not differ significantly from that for unrelated animals. These results indicate that among harbour seals, related pups are not usually chosen preferentially for fostering and hence, kin selection is not likely to be influencing the occurrence of this behaviour. Copyright 1999 The Association for the Study of Animal Behaviour.     

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.     

Gene Diversity and Female Philopatry

The effect of female philopatry on the apportionment of gene diversity within a population is evaluated. Even with random mate selection, the apportionment of gene diversity within and among social lineages (groups of related females) is inherently different than in classically defined demic groups. Considerable excess heterozygosity occurs within lineages without substantial changes in total or population heterozygosity. The proportion of genetic variance among lineages within the population was dependent on the lineage size and the number of male breeders per lineage. The greatest genetic differentiation among lineages was evident when there was one polygynous male breeding within a lineage of philopatric females, a common breeding tactic in mammalian social systems. The fixation indices depicting the genetic structure of the population were found to attain constant values after the first few generations despite the continuous loss of gene diversity within the population by genetic drift. Additionally, the change of gene correlations within individuals relative to the change within the population attains a state of dynamic equilibrium, as do the changes of gene correlations within lineages relative to the total and within individuals relative to within lineages. Comparisons of coancestries and fixation indices for philopatric versus randomly dispersing females indicate that philopatry and polygyny have probably not evolved independently and that promotion of gene correlations among adults rather than offspring has been of primary importance.     

Fine-scale genetic structuring in a natural population of European wild rabbits (Oryctolagus cuniculus)

The genetic structure of a free-living tagged population of European wild rabbits (Oryctolagus cuniculus) was investigated for two consecutive years (1990 and 1991) using 10 polymorphic microsatellite loci. A specific social behaviour, the formation of stable breeding groups, influenced the genetic structure of the population. These breeding groups were shown to constitute genetically differentiated units with low levels of gene flow between them. The average relatedness among members of a social group was higher than within the population as a whole. As a result of female philopatry coupled with male-biased natal dispersal, the relatedness of females was higher than that of males, both within social groups and in the whole population. Furthermore, the average relatedness of females within groups was twice the relatedness of females between groups. This study reveals marked fine-scale, intrapopulation genetic structure, which is attributable to the social behaviour of the European wild rabbit.     

Population structure of brush-tailed rock-wallaby (Petrogale penicillata) colonies inferred from analysis of faecal DNA

Genetic data obtained using faecal DNA were used to elucidate the population structure of four brush-tailed rock-wallaby (Petrogale penicillata) colonies located in Wollemi National Park, New South Wales. The results suggested that the four sampled colonies are genetically differentiated and do not form a panmictic unit. Based on assignment tests, approximately 5% of sampled individuals were inferred to be dispersers and both male and female migrants were detected. Multilocus spatial autocorrelation analyses provided evidence for increased philopatry among females compared to males within the largest colony in the valley. Females in close spatial proximity were more genetically similar than expected under a random distribution of females, and females separated by more than 400 m were less genetically similar than expected. In contrast, there was no evidence of a significant clustering of related males. This suggests that within-colony dispersal is male biased. We also investigated the best strategies for conserving genetic diversity in this population. All of the four sampled colonies were found to contain distinct components of the genetic diversity of the Wolgan Valley P. penicillata population and loss of any colony is likely to result in the loss of unique alleles. Conservation and management plans should take into account that these colonies represent genetically differentiated discrete subpopulations. This approach is also the best strategy for maintaining the genetic diversity of the populations in this valley.     

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.     

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.