Genetic diversity,population structure and sex‐biased dispersal in three co‐evolving species

Genetic diversity and spatial structure of populations are important for antagonistic coevolution. We investigated genetic variation and population structure of three closely related European ant species: the social parasite Harpagoxenus sublaevis and its two host species Leptothorax acervorum and Leptothorax muscorum. We sampled populations in 12 countries and analysed eight microsatellite loci and an mtDNA sequence. We found high levels of genetic variation in all three species, only slightly less variation in the host L. muscorum. Using a newly introduced measure of differentiation (Jost’s D_est ), we detected strong population structuring in all species and less male‐biased dispersal than previously thought. We found no phylogeographic patterns that could give information on post‐glacial colonization routes – northern populations are as variable as more southern populations. We conclude that conditions for Thompson’s geographic mosaic of coevolution are ideal in this system: all three species show ample genetic variation and strong population structure.     

Variable extent of sex‐biased dispersal in a strongly polygynous mammal

For mammals with a polygynous mating system, dispersal is expected to be male‐biased. However, with the increase in empirical studies, discrepancies are arising between the expected and observed direction/extent of the bias in dispersal. In this study, we assessed sex‐biased dispersal in red deer (Cervus elaphus) on 13 estates from the Scottish Highlands. A total of 568 adult individuals were genotyped at 21 microsatellite markers and sequenced for 821 bp of the mitochondrial control region. Estimates of population structure with mitochondrial sequences were eight times larger than that obtained with microsatellite data (F_{st′‐mt DNA} = 0.831; F_{st′‐micros} = 0.096) indicating overall male‐biased dispersal in the study area. Comparisons of microsatellite data between the sexes indicated a predominance of male‐biased dispersal in the study area but values of F_ST and relatedness were only slighter larger for females. Individual‐based spatial autocorrelation analysis generated a similar pattern of relatedness across geographical distances for both sexes, with differences only significant at two distance intervals (25–30 and 70–112 km). Patterns of relatedness differed between estates, male biased‐dispersal was detected in eight estates but no sex‐biased dispersal was found in the remaining five. Neither population density nor landscape cover was found to be associated with the patterns of relatedness found across the estates. Differences in management strategies that could influence age structure, sex ratio and dispersal behaviour are proposed as potential factors influencing the relatedness patterns observed. This study provides new insights on dispersal of a strongly polygynous mammal at geographical scales relevant for management and conservation.     

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.     

Topographic effects on fine‐scale spatial genetic structure in Castanopsis chinensis Hance (Fagaceae)

Ecological study plots are usually treated as if they are flat. This does not hold for many situations such as mountains where topography is complex. In areas with complex topography individual relationships are not only determined by projection distance, but also by surface distance. To demonstrate this we compared projection and surface distances by analyzing spatial genetic autocorrelation for Castanopsis chinensis in two subplots (A and B) in the Dinghushan (DHS) national nature reserve in subtropical South China. We observed that the two types of distances generally result in similar fine‐scale spatial genetic structure (SGS) patterning for the spatially less structured subplot B, but not for the highly structured subplot A. The present study shows clearly that accounting for plot architecture in plant species on topographically complex areas enables a more accurate picture of the underlying spatial genetic structure to emerge.     

Pollen dispersal and genetic structure of the tropical tree Dipteryx panamensis in a fragmented Costa Rican landscape

In the face of widespread deforestation, the conservation of rainforest trees relies increasingly on their ability to maintain reproductive processes in fragmented landscapes. Here, we analysed nine microsatellite loci for 218 adults and 325 progeny of the tree Dipteryx panamensis in Costa Rica. Pollen dispersal distances, genetic diversity, genetic structure and spatial autocorrelation were determined for populations in four habitats: continuous forest, forest fragments, pastures adjacent to fragments and isolated pastures. We predicted longer but less frequent pollen movements among increasingly isolated trees. This pattern would lead to lower outcrossing rates for pasture trees, as well as lower genetic diversity and increased structure and spatial autocorrelation among their progeny. Results generally followed these expectations, with the shortest pollen dispersal among continuous forest trees (240 m), moderate distances for fragment (343 m) and adjacent pasture (317 m) populations, and distances of up to 2.3 km in isolated pastures (mean: 557 m). Variance around pollen dispersal estimates also increased with fragmentation, suggesting altered pollination conditions. Outcrossing rates were lower for pasture trees and we found greater spatial autocorrelation and genetic structure among their progeny, as well as a trend towards lower heterozygosity. Paternal reproductive dominance, the pollen contributions from individual fathers, did not vary among habitats, but we did document asymmetric pollen flow between pasture and adjacent fragment populations. We conclude that long-distance pollen dispersal helps maintain gene flow for D. panamensis in this fragmented landscape, but pasture and isolated pasture populations are still at risk of long-term genetic erosion.     

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.     

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.     

Low genetic variability, female-biased dispersal and high movement rates in an urban population of Eurasian badgers Meles meles

1. Urban and rural populations of animals can differ in their behaviour, both in order to meet their ecological requirements and due to the constraints imposed by different environments. The study of urban populations can therefore offer useful insights into the behavioural flexibility of a species as a whole, as well as indicating how the species in question adapts to a specifically urban environment. 2. The genetic structure of a population can provide information about social structure and movement patterns that is difficult to obtain by other means. Using non-invasively collected hair samples, we estimated the population size of Eurasian badgers Meles meles in the city of Brighton, England, and calculated population-specific parameters of genetic variability and sex-specific rates of outbreeding and dispersal. 3. Population density was high in the context of badger densities reported throughout their range. This was due to a high density of social groups rather than large numbers of individuals per group. 4. The allelic richness of the population was low compared with other British populations. However, the rate of extra-group paternity and the relatively frequent (mainly temporary) intergroup movements suggest that, on a local scale, the population was outbred. Although members of both sexes visited other groups, there was a trend for more females to make intergroup movements. 5. The results reveal that urban badgers can achieve high densities and suggest that while some population parameters are similar between urban and rural populations, the frequency of intergroup movements is higher among urban badgers. In a wider context, these results demonstrate the ability of non-invasive genetic sampling to provide information about the population density, social structure and behaviour of urban wildlife.     

Fine scale relationships between sex, life history, and dispersal of masu salmon

Identifying the patterns and processes driving dispersal is critical for understanding population structure and dynamics. In many organisms, sex-biased dispersal is related to the type of mating system. Considerably, less is known about the influence of life-history variability on dispersal. Here we investigated patterns of dispersal in masu salmon (Oncorhynchus masou) to evaluate influences of sex and life history on dispersal. As expected, assignment tests and isolation by distance analysis revealed that dispersal of marine-migratory masu salmon was male-biased. However, dispersal of resident and migratory males did not follow our expectation and marine-migratory individuals dispersed more than residents. This may be because direct competition between marine-migratory and resident males is weak or that the cost of dispersal is smaller for marine-migratory individuals. This study revealed that both sex and migratory life-history influence patterns of dispersal at a local scale in masu salmon.     

Fine‐scale genetic structure and inferences on population biology in the threatened Mediterranean red coral,Corallium rubrum

Identifying microevolutionary processes acting in populations of marine species with larval dispersal is a challenging but crucial task because of its conservation implications. In this context, recent improvements in the study of spatial genetic structure (SGS) are particularly promising because they allow accurate insights into the demographic and evolutionary processes at stake. Using an exhaustive sampling and a combination of image processing and population genetics, we highlighted significant SGS between colonies of Corallium rubrum over an area of half a square metre, which sheds light on a number of aspects of its population biology. Based on this SGS, we found the mean dispersal range within sites to be between 22.6 and 32.1 cm, suggesting that the surveyed area approximately corresponded to a breeding unit. We then conducted a kinship analysis, which revealed a complex half‐sib family structure and allowed us to quantify the level of self‐recruitment and to characterize aspects of the mating system of this species. Furthermore, significant temporal variations in allele frequencies were observed, suggesting low genetic drift. These results have important conservation implications for the red coral and further our understanding of the microevolutionary processes acting within populations of sessile marine species with a larval phase.     

Genetic evidence that culling increases badger movement: implications for the spread of bovine tuberculosis

The Eurasian badger (Meles meles) has been implicated in the transmission of bovine tuberculosis (TB, caused by Mycobacterium bovis) to cattle. However, evidence suggests that attempts to reduce the spread of TB among cattle in Britain by culling badgers have mixed effects. A large-scale field experiment (the randomized badger culling trial, RBCT) showed that widespread proactive badger culling reduced the incidence of TB in cattle within culled areas but that TB incidence increased in adjoining areas. Additionally, localized reactive badger culling increased the incidence of TB in cattle. It has been suggested that culling-induced perturbation of badger social structure may increase individual movements and elevate the risk of disease transmission between badgers and cattle. Field studies support this hypothesis, by demonstrating increases in badger group ranges and the prevalence of TB infection in badgers following culling. However, more evidence on the effect of culling on badger movements is needed in order to predict the epidemiological consequences of this control strategy. Here, analysis of the genetic signatures of badger populations in the RBCT revealed increased dispersal following culling. While standard tests provided evidence for greater dispersal after culling, a novel method indicated that this was due to medium- and long-distance dispersal, in addition to previously reported increases in home-range size. Our results also indicated that, on average, badgers infected with M. bovis moved significantly farther than did uninfected badgers. A disease control strategy that included culling would need to take account of the potentially negative epidemiological consequences of increased badger dispersal.     

Population genetic structure and long-distance dispersal among seabird populations: implications for colony persistence

Dramatic local population decline brought about by anthropogenic-driven change is an increasingly common threat to biodiversity. Seabird life history traits make them particularly vulnerable to such change; therefore, understanding population connectivity and dispersal dynamics is vital for successful management. Our study used a 357-base pair mitochondrial control region locus sequenced for 103 individuals and 18 nuclear microsatellite loci genotyped for 245 individuals to investigate population structure in the Atlantic and Pacific populations of the pelagic seabird, Leach's storm-petrel Oceanodroma leucorhoa leucorhoa. This species is under intense predation pressure at one regionally important colony on St Kilda, Scotland, where a disparity between population decline and predation rates hints at immigration from other large colonies. AMOVA, F(ST), Φ(ST) and Bayesian cluster analyses revealed no genetic structure among Atlantic colonies (Global Φ(ST) = -0.02 P > 0.05, Global F(ST) = 0.003, P > 0.05, STRUCTURE K = 1), consistent with either contemporary gene flow or strong historical association within the ocean basin. The Pacific and Atlantic populations are genetically distinct (Global Φ(ST) = 0.32 P < 0.0001, Global F(ST) = 0.04, P < 0.0001, STRUCTURE K = 2), but evidence for interocean exchange was found with individual exclusion/assignment and population coalescent analyses. These findings highlight the importance of conserving multiple colonies at a number of different sites and suggest that management of this seabird may be best viewed at an oceanic scale. Moreover, our study provides an illustration of how long-distance movement may ameliorate the potentially deleterious impacts of localized environmental change, although direct measures of dispersal are still required to better understand this process.     

No genetic evidence of sex-biased dispersal in a lekking bird, the capercaillie (Tetrao urogallus)

Sex-biased dispersal is often connected to the mating behaviour of the species. Even if patterns of natal dispersal are reasonably well documented for monogamous birds, only a few data are available for polygynous and especially lekking species. We investigated the dispersal of the capercaillie (Tetrao urogallus) by examining sex-specific gene flow among the leks. Genetic information was extracted using nuclear and mitochondrial molecular markers for sexed faecal samples and analysed by novel Bayesian statistical methods. Contrary to the traditional view that the males are highly philopatric and female is the dispersing sex, we found roughly equivalent gross and effective dispersal of the sexes. The level of polygamy has a strong influence on the effective population size and on the effective dispersal. The results do not support the theories that dispersal evolves solely as a result of resource competition or other advantages to males obtained through kin selection in lekking species.     

A sex‐linked SCAR marker in Bryonia dioica (Cucurbitaceae), a dioecious species with XY sex‐determination and homomorphic sex chromosomes

Genetic crosses between the dioecious Bryonia dioica (Cucurbitaceae) and the monoecious B. alba in 1903 provided the first clear evidence for Mendelian inheritance of dioecy and made B. dioica the first organism for which XY sex‐determination was experimentally proven. Applying molecular tools to this system, we developed a sex‐linked sequence‐characterized amplified region (SCAR) marker for B. dioica and sequenced it for individuals representing the full geographic range of the species from Scotland to North Africa. For comparison, we also sequenced this marker for representatives of the dioecious B. cretica, B. multiflora and B. syriaca, and monoecious B. alba. In no case did any individual, male or female, yield more than two haplotypes. In northern Europe, we found strong linkage between our marker and sex, with all Y‐sequences being identical to each other. In southern Europe, however, the linkage between our marker and sex was weak, with recombination detected within both the X‐ and the Y‐homologues. Population genetic analyses suggest that the SCAR marker experienced different evolutionary pressures in northern and southern Europe. These findings fit with phylogenetic evidence that the XY system in Bryonia is labile and suggest that the genus may be a good system in which to study the early steps of sex chromosome evolution.     

Effects of fine‐scale genetic structure on male mating success in gynodioecious Beta vulgaris ssp. maritima

Plant mating systems are known to influence population genetic structure because pollen and seed dispersal are often spatially restricted. However, the reciprocal outcomes of population structure on the dynamics of polymorphic mating systems have received little attention. In gynodioecious sea beet (Beta vulgaris ssp. maritima), three sexual types co‐occur: females carrying a cytoplasmic male sterility (CMS) gene, hermaphrodites carrying a non‐CMS cytoplasm and restored hermaphrodites that carry CMS genes and nuclear restorer alleles. This study investigated the effects of fine‐scale genetic structure on male reproductive success of the two hermaphroditic forms. Our study population was strongly structured and characterized by contrasting local sex‐ratios. Pollen flow was constrained over short distances and depended on local plant density. Interestingly, restored hermaphrodites sired significantly more seedlings than non‐CMS hermaphrodites, despite the previous observation that the former produce pollen of lower quality than the latter. This result was explained by the higher frequency of females in the local vicinity of restored (CMS) hermaphrodites as compared to non‐CMS hermaphrodites. Population structure thus strongly influences individual fitness and may locally counteract the expected effects of selection, suggesting that understanding fine scale population processes is central to predicting the evolution of gender polymorphism in angiosperms.     

Detection and visualization of spatial genetic structure in continuous Eucalyptus globulus forest

Visualizing the pattern of variation using microsatellites within a Eucalyptus globulus forest on the island of Tasmania provided surprising insights into the complex nature of the fine-scale spatial genetic structure that resides in these forests. We used spatial autocorrelation and principal coordinate analysis to compare fine-scale genetic structure between juvenile and mature cohorts in a study area, 140 m in diameter, located within a typical, continuous E. globulus forest. In total, 115 juvenile and 168 mature individuals were genotyped with eight highly polymorphic microsatellite loci. There was no significant difference in the level of genetic diversity between cohorts. However, there were differences in the spatial distribution of the genetic variation. Autocorrelation analysis provided clear evidence for significant spatial genetic structure in the mature cohort and significant, but weaker, structure in the juvenile cohort. The spatial interpolation of principal coordinate axes, derived from ordination of the genetic distance matrix between individuals, revealed a spatially coherent family group which was evident in both cohorts. Direct comparison of the genetic structure within each cohort allowed visualization of a shift in the spatial distribution of genetic variation within the population of approximately 10 m. As the shift coincided with the direction of prevailing winds, it is hypothesized that this phenomenon is due to downwind dispersal of seeds and is indicative of the important role of prevailing winds in forcing eastward gene flow in these high-latitude forests.     

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.     

Evidence that disease-induced population decline changes genetic structure and alters dispersal patterns in the Tasmanian devil

Infectious disease has been shown to be a major cause of population declines in wild animals. However, there remains little empirical evidence on the genetic consequences of disease-mediated population declines, or how such perturbations might affect demographic processes such as dispersal. Devil facial tumour disease (DFTD) has resulted in the rapid decline of the Tasmanian devil, Sarcophilus harrisii, and threatens to cause extinction. Using 10 microsatellite DNA markers, we compared genetic diversity and structure before and after DFTD outbreaks in three Tasmanian devil populations to assess the genetic consequences of disease-induced population decline. We also used both genetic and demographic data to investigate dispersal patterns in Tasmanian devils along the east coast of Tasmania. We observed a significant increase in inbreeding (F_IS pre/post-disease −0.030/0.012, P<0.05; relatedness pre/post-disease 0.011/0.038, P=0.06) in devil populations after just 2–3 generations of disease arrival, but no detectable change in genetic diversity. Furthermore, although there was no subdivision apparent among pre-disease populations (θ=0.005, 95% confidence interval (CI) −0.003 to 0.017), we found significant genetic differentiation among populations post-disease (θ=0.020, 0.010–0.027), apparently driven by a combination of selection and altered dispersal patterns of females in disease-affected populations. We also show that dispersal is male-biased in devils and that dispersal distances follow a typical leptokurtic distribution. Our results show that disease can result in genetic and demographic changes in host populations over few generations and short time scales. Ongoing management of Tasmanian devils must now attempt to maintain genetic variability in this species through actions designed to reverse the detrimental effects of inbreeding and subdivision in disease-affected populations.