Widespread gene flow and high genetic variability in populations of water voles Arvicola terrestris in patchy habitats (original) (raw)

Genetic structure of the cyclic fossorial water vole (Arvicola terrestris): landscape and demographic influences

Molecular Ecology, 2005

Genetic structure can be strongly affected by landscape features and variation through time and space of demographic parameters such as population size and migration rate. The fossorial water vole ( Arvicola terrestris ) is a cyclic species characterized by large demographic fluctuations over short periods of time. The outbreaks do not occur everywhere at the same time but spread as a wave at a regional scale. This leads to a pattern of large areas (i.e. some hundreds of km 2 ), each with different vole abundances, at any given time. Here, we describe the abundance and genetic structures in populations of the fossorial water vole. We use the data to try to understand how landscape and demographic features act to shape the genetic structure. The spatial variability of vole abundance was assessed from surface indices, collected in spring 2002 (April) in eastern central France. Genetic variability was analysed using eight microsatellite loci at 23 localities sampled between October 2001 and April 2002. We found some congruence between abundance and genetic structures. At a regional scale, the genetic disruptions were associated with both sharp relief and transition between an area of low abundance and another of high abundance. At a local scale, we observed a variation of the isolation-by-distance pattern according to the abundance level of vole populations. From these results we suggest that the dispersal pattern in cyclic rodent populations varies throughout the demographic cycle.

Fine-scale genetic structure and dispersal in the common vole (Microtus arvalis)

Molecular ecology, 2007

The genetic structure and demography of local populations is tightly linked to the rate and scale of dispersal. Dispersal parameters are notoriously difficult to determine in the field, and remain often completely unknown for smaller organisms. In this study, we investigate spatial and temporal genetic structure in relation to dispersal patterns among local populations of the probably most abundant European mammals, the common vole (Microtus arvalis). Voles were studied in six natural populations at distances of 0.4–2.5 km in three different seasons (fall, spring, summer) corresponding to different life-history stages. Field observations provided no direct evidence for movements of individuals between populations. The analysis of 10 microsatellite markers revealed a persistent overall genetic structure among populations of 2.9%, 2.5% and 3%FST in the respective season. Pairwise comparisons showed that even the closest populations were significantly differentiated from each other in each season, but there was no evidence for temporal differentiation within populations or isolation by distance among populations. Despite significant genetic structure, assignment analyses identified a relatively high proportion of individuals as being immigrants for the population where they were captured. The immigration rate was not significantly lower for females than for males. We suggest that a generally low and sex-dependent effective dispersal rate as the consequence of only few immigrants reproducing successfully in the new populations together with the social structure within populations may explain the maintenance of genetic differentiation among populations despite migration.

Temporally stable genetic variability and dynamic kinship structure in a fluctuating population of the root vole Microtus oeconomus

Molecular Ecology, 2010

Genetic variability, kin structure and demography of a population are mutually dependent. Population genetic theory predicts that under demographically stable conditions, neutral genetic variability reaches equilibrium between gene flow and drift. However, density fluctuations and non-random mating, resulting e.g. from kin clustering, may lead to changes in genetic composition over time. Theoretical models also predict that changes in kin structure may affect aggression level and recruitment, leading to density fluctuations. These predictions have been rarely tested in natural populations. The aim of this study was to analyse changes in genetic variability and kin structure in a local population of the root vole (Microtus oeconomus) that underwent a fourfold change in mean density over a 6-year period. Intensive live-trapping resulted in sampling 88% of individuals present in the study area, as estimated from mark-recapture data. Based on 642 individual genotypes at 20 microsatellite loci, we compared genetic variability and kin structure of this population between consecutive years. We found that immigration was negatively correlated with density, while the number of kin groups was positively correlated with density. This is consistent with theoretical predictions that changes in kin structure play an important role in population fluctuations. Despite the changes in density and kin structure, there was no genetic differentiation between years. Population-level genetic diversity measures did not significantly vary in time and remained relatively high (H E range: 0.72-0.78). These results show that a population that undergoes significant demographic and social changes may maintain high genetic variability and stable genetic composition.

The spatial genetic structure of bank vole (Myodes glareolus) and yellow-necked mouse (Apodemus flavicollis) populations: The effect of distance and habitat barriers

Animal Biology, 2009

Habitat barriers are considered to be an important factor causing the local reduction of genetic diversity by dividing a population into smaller sections and preventing gene fl ow between them. However, the "barrier eff ect" might be diff erent in the case of diff erent species. Th e eff ect of geographic distance and water barriers on the genetic structure of populations of two common rodent species -the yellownecked mouse ( Apodemus fl avicollis ) and the bank vole ( Myodes glareolus ) living in the area of a lake (on its islands and on two opposite shores) was investigated with the use of microsatellite fragment analysis. Th e two studied species are characterised by similar habitat requirements, but diff er with regard to the socio-spatial structure of the population, individual mobility, capability to cross environmental barriers, and other factors. Trapping was performed for two years in spring and autumn in north-eastern Poland (21 o E, 53 o N). A total of 160 yellow-necked mouse individuals (7 microsatellite loci) and 346 bank vole individuals (9 microsatellite loci) were analysed. Th e results of the diff erentiation analyses (F ST and R ST ) have shown that both the barrier which is formed by a ca. 300 m wide belt of water (between the island and the mainland) and the actual distance of approximately 10 km in continuous populations are suffi cient to create genetic diff erentiation within both species. Th e diff erences between local populations living on opposite lake shores are the smallest; diff erences between any one of them and the island populations are more distinct. All of the genetic diversity indices (the mean number of alleles, mean allelic richness, as well as the observed and expected heterozygosity) of the local populations from the lakeshores were signifi cantly higher than of the small island populations of these two species separated by the water barrier. Th e more profound "isolation eff ect" in the case of the island populations of the bank vole, in comparison to the yellow-necked mouse populations, seems to result not only from the lower mobility of the bank vole species, but may also be attributed to other diff erences in the animals' behaviour.

Demographic and genetic structure of fossorial water voles (Arvicola terrestris) on Scottish islands

Journal of Zoology, 2003

The distribution of fossorial water voles Arvicola terrestris on 15 small islands in the Sound of Jura, Argyll, Scotland, was established and populations were characterized in terms of size, structure and genetic composition (12 microsatellites). The results are compared with similar data from four metapopulations of riparian water voles in mainland Scotland. Water voles occurred on six islands, one of which was occupied in 1994, but not on two islands occupied during the 1960s. Probability of occupancy was signi®cantly associated with proximity to the nearest occupied island. Unlike voles on the mainland, which occupy fragmented patches of exclusively riparian habitat, voles on islands were fossorial and occupied large areas of continuous habitat. Spring population sizes were c. 10 times higher on the islands than colonies of mainland metapopulations. Individuals from three islands were genotyped and these populations had 50% lower levels of microsatellite polymorphism than the mainland metapopulations. Rates of inferred contemporary dispersal among islands separated by 1 km or more of sea were very low, according to large differences among islands in genetic composition, proportions of coat colour types and incidence of skin infection. None the less, the long-term persistence of the island populations is likely to depend on such dispersal. Comparisons between island populations and mainland metapopulations indicate that in both fragmented systems the level of dispersal is the primary factor in¯uencing genetic structure. The low genetic variability in the island populations may re¯ect either past historical events (founder effect and genetic drift) or present ecology (lack of immigration in closed and temporally¯uctuating populations).

Fine-scale spatial patterns of genetic relatedness among resident adult prairie voles

Journal of Mammalogy, 2015

Characterizing the spatial arrangement of related individuals within populations can convey information about opportunities for the evolution of kin-selected social behaviors, the potential for inbreeding, and the geographic distribution of genetic variation. Prairie voles (Microtus ochrogaster) are socially monogamous rodents that sometimes breed cooperatively. Individuals of both sexes are highly philopatric, and among natal dispersers, the average dispersal distance is about 30 m. Such limited natal dispersal can result in the spatial clustering of kin and we used microsatellite data to estimate genetic relatedness among resident adult prairie voles in 2 natural populations to test the hypothesis that limited natal dispersal of male and female prairie voles results in the spatial clustering of kin. Spatial autocorrelation analyses of nest residency and microsatellite data indicated that proximate same-sex adult residents of both sexes were significantly more related than more spatially distant resident samesex adults in Kansas. In Indiana, adult female voles residing less than 20 m apart were also significantly more related than more spatially distant resident adult females but spatial clustering of kin was not detected among resident adult males. The spatial clustering of kin indicates that opportunities for kin-selected behaviors exist in both populations, especially among females. Differences in the patterns of spatial genetic structure among resident males between the Kansas and Indiana populations may be due to population differences in factors such as demography and mating system, as well as in the extent of natal philopatry.

Role of genetic factors in landscape-geographic variation of the water vole ( Arvicola terrestris L.)

Russian Journal of …, 2006

The geographic variation of the water vole Arvicola terrestris L. has been analyzed with respect to two linear combinations of craniometric characters with the highest additive heritability (h 2 = 0.59 and h 2 = 0.52). The greatest differences have been revealed between the territorially close montane and piedmont populations. The lowland and montane populations have proved to differ to the smallest extent, despite their spatial and altitudinal separation. Selection under extreme conditions that leads to similar phenotypic results may be based on the common genetic background of these populations, irrespective of considerable distances between them and different environmental conditions in their habitats.

Migration and recovery of the genetic diversity during the increasing density phase in cyclic vole populations

Molecular Ecology, 2006

In cyclic populations, high genetic diversity is currently reported despite the periodic low numbers experienced by the populations during the low phases. Here, we report spatiotemporal monitoring at a very fine scale of cyclic populations of the fossorial water vole ( Arvicola terrestris ) during the increasing density phase. This phase marks the transition from a patchy structure (demes) during low density to a continuous population in high density. We found that the genetic diversity was effectively high but also that it displayed a local increase within demes over the increasing phase. The genetic diversity remained relatively constant when considering all demes together. The increase in vole abundance was also correlated with a decrease of genetic differentiation among demes. Such results suggest that at the end of the low phase, demes are affected by genetic drift as the result of being small and geographically isolated. This leads to a loss of local genetic diversity and a spatial differentiation among demes. This situation is counterbalanced during the increasing phase by the spatial expansion of demes and the increase of the effective migration among differentiated demes. We provide evidences that in cyclic populations of the fossorial water voles, the relative influence of drift operating during low density populations and migration occurring principally while population size increases interacts closely to maintain high genetic diversity.

Genetic variability and structure of the water vole Arvicola amphibius across four metapopulations in northern Norway

Ecology and Evolution, 2013

Water vole Arvicola amphibius populations have recently experienced severe decline in several European countries as a consequence of both reduction in suitable habitat and the establishment of the alien predator American mink Neovison vison. We used DNA microsatellite markers to describe the genetic structure of 14 island populations of water vole off the coast of northern Norway. We looked at intra-and inter-population levels of genetic variation and examined the effect of distance among pairs of populations on genetic differentiation (isolation by distance). We found a high level of genetic differentiation (measured by F ST ) among populations overall as well as between all pairs of populations. The genetic differentiation between populations was positively correlated with geographic distance between them. A clustering analysis grouped individuals into 7 distinct clusters and showed the presence of 3 immigrants among them. Our results suggest a small geographic scale for evolutionary and population dynamic processes in our water vole populations.

Parentage assignment detects frequent and large-scale dispersal in water voles

Molecular Ecology, 2003

Estimating the rate and scale of dispersal is essential for predicting the dynamics of fragmented populations, yet empirical estimates are typically imprecise and often negatively biased. We maximized detection of dispersal events between small, subdivided populations of water voles (Arvicola terrestris) using a novel method that combined direct capture–mark–recapture with microsatellite genotyping to identify parents and offspring in different populations and hence infer dispersal. We validated the method using individuals known from trapping data to have dispersed between populations. Local populations were linked by high rates of juvenile dispersal but much lower levels of adult dispersal. In the spring breeding population, 19% of females and 33% of males had left their natal population of the previous year. The average interpopulation dispersal distance was 1.8 km (range 0.3–5.2 km). Overall, patterns of dispersal fitted a negative exponential function. Information from genotyping increased the estimated rate and scale of dispersal by three- and twofold, respectively, and hence represents a powerful tool to provide more realistic estimates of dispersal parameters.