Rapidly declining fine-scale spatial genetic structure in female red deer

A growing literature now documents the presence of fine-scale genetic structure in wild vertebrate populations. Breeding population size, levels of dispersal and polygyny--all hypothesized to affect population genetic structure--are known to be influenced by ecological conditions experienced by populations. However the possibility of temporal or spatial variation in fine-scale genetic structure as a result of ecological change is rarely considered or explored. Here we investigate temporal variation in fine-scale genetic structure in a red deer population on the Isle or Rum, Scotland. We document extremely fine-scale spatial genetic structure (< 100 m) amongst females but not males across a 24-year study period during which resource competition has intensified and the population has reached habitat carrying capacity. Based on census data, adult deer were allocated to one of three subpopulations in each year of the study. Global F(ST) estimates for females generated using these subpopulations decreased over the study period, indicating a rapid decline in fine-scale genetic structure of the population. Global F(ST) estimates for males were not different from zero across the study period. Using census and genetic data, we illustrate that, as a consequence of a release from culling early in the study period, the number of breeding females has increased while levels of polygyny have decreased in this population. We found little evidence for increasing dispersal between subpopulations over time in either sex. We argue that both increasing female population size and decreasing polygyny could explain the decline in female population genetic structure.     

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.     

Fine-scale population genetic structure in a fission-fusion society

Nonrandom patterns of mating and dispersal create fine-scale genetic structure in natural populations — especially of social mammals — with important evolutionary and conservation genetic consequences. Such structure is well-characterized for typical mammalian societies; that is, societies where social group composition is stable, dispersal is male-biased, and males form permanent breeding associations in just one or a few social groups over the course of their lives. However, genetic structure is not well understood for social mammals that differ from this pattern, including elephants. In elephant societies, social groups fission and fuse, and males never form permanent breeding associations with female groups. Here, we combine 33 years of behavioural observations with genetic information for 545 African elephants ( Loxodonta africana ), to investigate how mating and dispersal behaviours structure genetic variation between social groups and across age classes. We found that, like most social mammals, female matrilocality in elephants creates co-ancestry within core social groups and significant genetic differentiation between groups (Φ_ST = 0.058). However, unlike typical social mammals, male elephants do not bias reproduction towards a limited subset of social groups, and instead breed randomly across the population. As a result, reproductively dominant males mediate gene flow between core groups, which creates cohorts of similar-aged paternal relatives across the population. Because poaching tends to eliminate the oldest elephants from populations, illegal hunting and poaching are likely to erode fine-scale genetic structure. We discuss our results and their evolutionary and conservation genetic implications in the context of other social mammals.     

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.     

Fine-scale social and spatial genetic structure in Sitka black-tailed deer

The spatial extent of Sitka black-tailed deer (Odocoileus hemionus sitkensis) populations below the regional scale is relatively unknown, as is dispersal between populations. Here, we use noninvasive samples to genotype 221 Sitka black-tailed deer in three watersheds on Prince of Wales Island, Alaska, separated by a maximum of 44 km, using traditional and spatial genetic approaches. We find that despite geographic proximity, multiple lines of evidence suggest fine-scale genetic structure among the three study sites. The 2 most geographically distant watersheds differed significantly in genetic composition, suggesting an isolation-by-distance pattern. Within study sites, deer exhibited spatial genetic structure within a radius of 1,000 m. Based on a reduced sample of known-sex individuals, females exhibited positive spatial genetic structure within a radius of 500 m but males showed no structure. Moreover, females were more likely to be related to their 5 nearest female neighbors, regardless of distance, than were males. Evidence indicates dispersal by both sexes although it may be more common, or dispersal distances are greater, in males. Nonetheless, analysis of assignment indices and comparison of sex-specific correlograms found no evidence of sex-biased dispersal between watersheds. Patterns of spatial relatedness and connectivity suggest limited dispersal among Sitka black-tailed deer, creating genetic structure on a fine spatial scale, perhaps as small as the watershed.     

Genetic consequences of human management in an introduced island population of red deer (Cervus elaphus)

We investigated phylogeography and spatial genetic structure in an introduced island population of red deer (Cervus elaphus) on the Isle of Rum, Scotland, experiencing spatial variation in management regime. Five different mitochondrial DNA (mtDNA) haplotypes were present among female red deer on Rum. These comprised two phylogenetically divergent groups, one of which clustered with red deer from Sardinia and North Africa, while the other four grouped with other Western European red deer. Recent and historical red deer management practices explain this result. The Rum population is descended from recent introductions from at least four different UK mainland populations, and translocation of red deer within the UK and across Europe is well documented. We found significant spatial genetic structure across Rum in both mtDNA haplotypes and microsatellite markers. Mitochondrial spatial structure was over an order of magnitude greater than structure in nuclear markers. This extreme difference is explained by the fact that the Rum population was introduced from different source populations, the highly male-biased dispersal patterns of red deer and the much smaller effective population size of mitochondrial compared to nuclear markers. Spatial structure in mtDNA conformed to a pattern of isolation by distance, while nuclear DNA did not. Apparent structure in the nuclear markers was driven by differences between the North Block and the rest of the island. We suggest that recent differences in the management regimes in different parts of the island have led to differences in effective male migration that would account for this observation.     

No evidence of juvenile body mass affecting dispersal in male red deer

Dispersal is an important mechanism in population dynamics with a sparse empirical basis. Environmental causes of dispersal may work directly or indirectly. In a population with documented negative density-dependent male dispersal, we investigated if the effect of density on dispersal was indirectly mediated through body mass. We analysed the probability of dispersal in 170 juvenile red deer males in Snillfjord municipality, Norway, during a 20-year period of rapid population growth (1977–1997). Body mass and dispersal propensity were not related. Thus, changes in population density act directly on dispersal and are not affected by body mass. Body mass-dependent dispersal occurs in species with strong antagonistic interactions and a high cost of dispersal. Our result suggests that the cost of dispersal in male red deer is low in terms of energy expenditure and survival. We conclude that the effect of body mass on dispersal is likely to vary with mating system and cost of dispersal.     

Analysis of spatial genetic structure in an expanding Pinus halepensis population reveals development of fine-scale genetic clustering over time

We analysed the change of spatial genetic structure (SGS) of reproductive individuals over time in an expanding Pinus halepensis population. To our knowledge, this is the first empirical study to analyse the temporal component of SGS by following the dynamics of successive cohorts of the same population over time, rather than analysing different age cohorts at a single time. SGS is influenced by various factors including restricted gene dispersal, microenvironmental selection, mating patterns and the spatial pattern of reproductive individuals. Several factors that affect SGS are expected to vary over time and as adult density increases. Using air photo analysis, tree-ring dating and molecular marker analysis we reconstructed the spread of reproductive individuals over 30 years beginning from five initial individuals. In the early stages, genotypes were distributed randomly in space. Over time and with increasing density, fine-scale (< 20 m) SGS developed and the magnitude of genetic clustering increased. The SGS was strongly affected by the initial spatial distribution and genetic variation of the founding individuals. The development of SGS may be explained by fine-scale environmental heterogeneity and possibly microenvironmental selection. Inbreeding and variation in reproductive success may have enhanced SGS magnitude over time.     

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.     

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.     

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.     

Female-biased dispersal under conditions of low male mating competition in a polygynous mammal

Sex-biased dispersal is a common phenomenon in birds and mammals. Competition for mates has been argued to be an important selective pressure favouring dispersal. Sexual differences in the level of intrasexual competition may produce asymmetries in the costs-benefits balance of dispersal and philopatry for males and females, which may favour male-biased dispersal in polygynous species such as most mammals. This being the case, condition-dependent dispersal predicts that male-bias should decrease if mating competition relaxes. We test this expectation for red deer, where male-biased dispersal is the norm. In southwestern Spain, red deer populations located in nonfenced hunting estates presented altered structures with sex ratio strongly biased to females and high proportion of young males. As a consequence, mate competition in these populations was lower than in other, most typical red deer populations. We found that, under such conditions of altered population structure, dispersal was female-biased rather than male-biased. Additionally, mate competition positively related to male dispersal but negatively to female dispersal. Other factors such as resource competition, age of individuals and sex ratio were not related to male or female dispersal. Males may not disperse if intrasexual competition is low and then females may disperse as a response to male philopatry. We propose hypotheses related to female mate choice to explain female dispersal under male philopatry. The shift of the sex-biased dispersal pattern along the gradient of mate competition highlights its condition-dependence as well as the interaction between male and female dispersal in the evolution of sex-biased dispersal.     

Female philopatry and male-biased dispersal in a direct-developing salamander, Plethodon cinereus

The local resource competition hypothesis and the local mate competition hypothesis were developed based on avian and mammalian systems to explain sex-biased dispersal. Most avian species show a female bias in dispersal, ostensibly due to resource defence, and most mammals show a male bias, ostensibly due to male-male competition. These findings confound phylogeny with mating strategy; little is known about sex-biased dispersal in other taxa. Resource defence and male-male competition are both intense in Plethodon cinereus, a direct-developing salamander, so we tested whether sex-biased dispersal in this amphibian is consistent with the local resource competition hypothesis (female-biased) or the local mate competition hypothesis (male-biased). Using fine-scale genetic spatial autocorrelation analyses, we found that females were philopatric, showing significant positive genetic structure in the shortest distance classes, with stronger patterns apparent when only territorial females were tested. Males showed no spatial genetic structure over the shortest distances. Mark-recapture observations of P. cinereus over 5 years were consistent with the genetic data: males dispersed farther than females during natal dispersal and 44% of females were recaptured within 1 m of their juvenile locations. We conclude that, in this population of a direct-developing amphibian, females are philopatric and dispersal is male-biased, consistent with the local mate competition hypothesis.     

Dispersal is not female biased in a resource-defence mating ungulate, the European roe deer

Dispersal is frequently more prevalent in one sex compared to the other. Greenwood proposed that patterns of sex-biased dispersal among birds and mammals are linked to their mating strategies. For species where males defend resources rather than females, he predicted female-biased dispersal, because males should remain at their birth site where they are familiar with the distribution of the resources that they must defend. Greenwood's hypothesis has been extensively supported among birds, where most species exhibit a resource-defence mating strategy. However, almost no equivalent information is available for mammals as males generally defend mates in this group. An exception is the European roe deer, a resource-defence mating ungulate. We thus tested Greenwood's hypothesis on this atypical mammalian model, looking for female-biased dispersal using sex-specific inter-individual genetic distances. We conclusively show that gene flow is not higher among females compared to males in the studied roe deer population, and hence that dispersal is not female-biased, suggesting that male mating strategy is not the primary selective force driving the evolution of dispersal in roe deer. We discuss the role of female mate choice and intra-sexual competition as possible alternative selective pressures involved.     

Population structure and genetic variation in the endangered Giant Kangaroo Rat (<Emphasis Type="Italic">Dipodomys ingens</Emphasis>)

Populations of the endangered giant kangaroo rat, Dipodomys ingens (Heteromyidae), have suffered increasing fragmentation and isolation over the recent past, and the distribution of this unique rodent has become restricted to 3% of its historical range. Such changes in population structure can significantly affect effective population size and dispersal, and ultimately increase the risk of extinction for endangered species. To assess the fine-scale population structure, gene flow, and genetic diversity of remnant populations of Dipodomys ingens, we examined variation at six microsatellite DNA loci in 95 animals from six populations. Genetic subdivision was significant for both the northern and southern part of the kangaroo rat’s range although there was considerable gene flow among southern populations. While regional gene diversity was relatively high for this endangered species, hierarchical F-statistics of northern populations in Fresno and San Benito counties suggested non-random mating and genetic drift within subpopulations. We conclude that effective dispersal, and therefore genetic distances between populations, is better predicted by ecological conditions and topography of the environment than linear geographic distance between populations. Our results are consistent with and complimentary to previous findings based on mtDNA variation of giant kangaroo rats. We suggest that management plans for this endangered rodent focus on protection of suitable habitat, maintenance of connectivity, and enhancement of effective dispersal between populations either through suitable dispersal corridors or translocations.     

Genetic consequences of natal dispersal in the colonial lesser kestrel

Dispersal is a life-history trait that plays a fundamental role in population dynamics, influencing evolution, species distribution, and the genetics and structure of populations. In spite of the fact that dispersal has been hypothesized to be an efficient behavioural mechanism to avoid inbreeding, the expected relationship between dispersal and mate relatedness still remains controversial. Here, we examine the genetic consequences of natal dispersal, namely the higher chance of obtaining genetically less similar mates as a result of moving from natal to breeding sites, in a lesser kestrel (Falco naumanni) population. Relatedness between individuals tended to decrease with distance between their breeding colonies, indicating that the study population follows an 'isolation-by-distance' pattern of spatial genetic structure. Such a fine-scale genetic structure generates a scenario in which individuals can potentially increase the chance of obtaining genetically less similar mates by dispersing over larger distances from their natal colony. Using dispersal information and genotypic data, we showed that mate relatedness decreased with natal dispersal distance, an effect that remained significant both while including and excluding philopatric individuals from the data set. These results, together with the well known detrimental consequences of reduced genetic diversity in the study population, suggest that dispersal may have evolved, at least in part, to avoid the negative fitness consequences of mating with genetically similar individuals.     

Genetic spatial autocorrelation can readily detect sex-biased dispersal

Sex-biased dispersal is expected to generate differences in the fine-scale genetic structure of males and females. Therefore, spatial analyses of multilocus genotypes may offer a powerful approach for detecting sex-biased dispersal in natural populations. However, the effects of sex-biased dispersal on fine-scale genetic structure have not been explored. We used simulations and multilocus spatial autocorrelation analysis to investigate how sex-biased dispersal influences fine-scale genetic structure. We evaluated three statistical tests for detecting sex-biased dispersal: bootstrap confidence intervals about autocorrelation r values and recently developed heterogeneity tests at the distance class and whole correlogram levels. Even modest sex bias in dispersal resulted in significantly different fine-scale spatial autocorrelation patterns between the sexes. This was particularly evident when dispersal was strongly restricted in the less-dispersing sex (mean distance <200 m), when differences between the sexes were readily detected over short distances. All tests had high power to detect sex-biased dispersal with large sample sizes (n ≥ 250). However, there was variation in type I error rates among the tests, for which we offer specific recommendations. We found congruence between simulation predictions and empirical data from the agile antechinus, a species that exhibits male-biased dispersal, confirming the power of individual-based genetic analysis to provide insights into asymmetries in male and female dispersal. Our key recommendations for using multilocus spatial autocorrelation analyses to test for sex-biased dispersal are: (i) maximize sample size, not locus number; (ii) concentrate sampling within the scale of positive structure; (iii) evaluate several distance class sizes; (iv) use appropriate methods when combining data from multiple populations; (v) compare the appropriate groups of individuals.     

Use of microsatellite markers to assess the spatial genetic structure of a population of sika deerCervus nippon on Kinkazan Island, Japan

To understand the relationship between social behaviour and gene distribution, we used microsatellite markers to resolve the spatial genetic structure of the sika deerCervus nippon Temminck, 1838 population on Kinkazan Island, a small island (9.6 km²) in northern Japan. We obtained 177 samples of deer which correspond to about 30% of the total population on the island. 126 were from a local population where each deer was individually identified, while 51 from other area on the island. Although there were no apparent geographical barriers on the island, the sika deer population showed local differentiation in its genetic composition. By comparing allele-sharing rates between gender and social categories, we demonstrated a higher genetic relatedness within males in a local group. The Assignment Index (AI) of each sex within a local group showed similar distributions. None of our analyses indicated a lower genetic relatedness among males than females, which contradicted our predictions based on the dispersal behaviour of males. Considering other factors, the results suggest that the range of male dispersal is quite limited on this island.     

Fine-scale population genetic structure and sex-biased dispersal in the smooth snake (Coronella austriaca) in southern England

Human-induced alteration of natural habitats has the potential to impact on the genetic structuring of remnant populations at multiple spatial scales. Species from higher trophic levels, such as snakes, are expected to be particularly susceptible to land-use changes. We examined fine-scale population structure and looked for evidence of sex-biased dispersal in smooth snakes (Coronella austriaca), sampled from 10 heathland localities situated within a managed coniferous forest in Dorset, United Kingdom. Despite the limited distances between heathland areas (maximum <6 km), there was a small but significant structuring of populations based on eight microsatellite loci. This followed an isolation-by-distance model using both straight line and 'biological' distances between sampling sites, suggesting C. austriaca's low vagility as the causal factor, rather than closed canopy conifer forest exerting an effect as a barrier to dispersal. Within population comparisons of male and female snakes showed evidence for sex-biased dispersal, with three of four analyses finding significantly higher dispersal in males than in females. We suggest that the fine-scale spatial genetic structuring and sex-biased dispersal have important implications for the conservation of C. austriaca, and highlight the value of heathland areas within commercial conifer plantations with regards to their future management.     

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.