When dispersal fails: unexpected genetic separation in Gibraltar macaques (Macaca sylvanus)

Barbary macaques (Macaca sylvanus), now restricted in the wild to a few isolated forested areas of Morocco and Algeria, are present in a free‐ranging colony on Gibraltar. For many decades, the Gibraltar colony was exposed to multiple bottlenecks due to highly nonrandom removal of animals, followed by repeated introductions of animals from North Africa. Moreover, because of complete isolation, Gibraltar's several social groups of macaques provide an ideal system to study the genetic consequences of dispersal in cercopithecines in situ. Predictions of genetic consequences due to male‐biased dispersal in cercopithecines will be different for autosomal and maternally inherited genetic markers, such as the control region of the mitochondrial DNA. We used a panel of 14 highly polymorphic microsatellite loci and part of the hypervariable region I of the mitochondrial control region to estimate genetic structure between five social groups in Gibraltar. Surprisingly, for autosomal markers, both classical summary statistics and an individual‐based method using a Bayesian framework detected significant genetic structure between social groups in Gibraltar, despite much closer proximity than wild Algerian and Moroccan populations. Mitochondrial data support this finding, as a very substantial portion of the total genetic variation (70.2%) was found between social groups. Using two Bayesian approaches, we likewise identified not only a small number of male first‐generation immigrants (albeit less than expected for cercopithecines) but also unexpectedly a few females. We hypothesize that the culling of males that are more likely to disperse might slow down genetic homogenization among neighbouring groups, but may also and more perversely produce selection on certain behavioural traits. This may have important repercussions for conservation, as it could lead to evolutionary changes that are not due to inbreeding or genetic drift.     

Microsatellite data show evidence for male-biased dispersal in the Caribbean lizard Anolis roquet

Dispersal is a key component of an organism's life history and differences in dispersal between sexes appear to be widespread in vertebrates. However, most predictions of sex-biased dispersal have been based on observations of social structure in birds and mammals and more data are needed on other taxa to test whether these predictions apply in other organisms. Caribbean anole lizards are important model organisms in various biological disciplines, including evolutionary biology. However, very little is known about their dispersal strategies despite the importance of dispersal for population structure and dynamics. Here we use nine microsatellite markers to assess signatures of sex-biased dispersal on two spatial sampling scales in Anolis roquet, an anole endemic to the island of Martinique. Significantly higher gene diversity (H(S)) and lower mean assignment value (mAIC) was found in males on the larger spatial sampling scale. Significant heterozygote deficit (F(IS)), lower population differentiation (F(ST)), mAIC and variance of assignment index (vAIC) was found in males on the smaller spatial scale. The observation of male biased dispersal conform with expectations based on the polygynous mating system of Anolis roquet, and contributes to an explanation of the contrasting patterns of genetic structure between maternal and biparental markers that have been reported previously in this, and other anoline, species.     

Genetic evidence for male-biased dispersal in the Siberian jay (Perisoreus infaustus) based on autosomal and Z-chromosomal markers

Sex-bias in natal dispersal patterns can have important genetic and evolutionary consequences; however, reliable information about sex-biased dispersal can be difficult to obtain with observational methods. We analysed the sex-specific patterns of genetic differentiation among three Siberian jay (Perisoreus infaustus) populations, using 11 autosomal and six Z-chromosomal microsatellite markers. Irrespective of marker-type and indices used (viz. F(ST), average pairwise relatedness and effective number of immigrants), all analyses provided strong evidence for male-biased dispersal. Population structuring at autosomal loci (F(ST) =0.046, P<0.05) exceeded that at Z-chromosomal loci (F(ST) =0.033, P<0.05), and levels of introgression were inferred to be significantly higher for Z-chromosomal when compared to autosomal loci. Of the three populations studied, levels of genetic variability were the lowest in the southernmost fringe population, despite the fact that it harboured a group of divergent Z-chromosomal haplotypes that were not found in the other two populations. In general, the results provide strong genetic evidence for male-biased dispersal in Siberian jays, where observational data have previously suggested male philopatry. The results also highlight the utility of Z-chromosomal markers for gaining insights into the genetic diversity and structuring of populations.     

Characterizing dispersal patterns in a threatened seabird with limited genetic structure

Genetic assignment methods provide an appealing approach for characterizing dispersal patterns on ecological time scales, but require sufficient genetic differentiation to accurately identify migrants and a large enough sample size of migrants to, for example, compare dispersal between sexes or age classes. We demonstrate that assignment methods can be rigorously used to characterize dispersal patterns in a marbled murrelet (Brachyramphus marmoratus) population from central California that numbers approximately 600 individuals and is only moderately differentiated (F_ST～ 0.03) from larger populations to the north. We used coalescent simulations to select a significance level that resulted in a low and approximately equal expected number of type I and II errors and then used this significance level to identify a population of origin for 589 individuals genotyped at 13 microsatellite loci. The proportion of migrants in central California was greatest during winter when 83% of individuals were classified as migrants compared to lower proportions during the breeding (6%) and post‐breeding (8%) seasons. Dispersal was also biased toward young and female individuals, as is typical in birds. Migrants were rarely members of parent‐offspring pairs, suggesting that they contributed few young to the central California population. A greater number of migrants than expected under equilibrium conditions, a lack of individuals with mixed ancestry, and a small number of potential source populations (two), likely allowed us to use assignment methods to rigorously characterize dispersal patterns for a population that was larger and less differentiated than typically thought required for the identification of migrants.     

Temporal increase in mtDNA diversity in a declining population

In small and declining populations levels of genetic variability are expected to be reduced due to effects of inbreeding and random genetic drift. As a result, both individual fitness and populations’ adaptability can be compromised, and the probability of extinction increased. Therefore, maintenance of genetic variability is a crucial goal in conservation biology. Here we show that although the level of genetic variability in mtDNA of the endangered Fennoscandian lesser white‐fronted goose Anser erythropus population is currently lower than in the neigbouring populations, it has increased six‐fold during the past 140 years despite the precipitously declining population. The explanation for increased genetic diversity in Fennoscandia appears to be recent spontaneous increase in male immigration rate equalling 0.56 per generation. This inference is supported by data on nuclear microsatellite markers, the latter of which show that the current and the historical Fennoscandian populations are significantly differentiated (F_ST = 0.046, P = 0) due to changes in allele frequencies. The effect of male‐mediated gene flow is potentially dichotomous. On the one hand it may rescue the Fennoscandian lesser white‐fronted goose from loss of genetic variability, but on the other hand, it eradicates the original genetic characteristics of this population.     

How far is too close? restricted,sex‐biased dispersal in black‐capped vireos

Understanding the interplay of dispersal and how it translates into gene flow is key to understanding population processes, and especially so for endangered species occupying fragmented habitats. In migratory songbirds, there is evidence that long‐distance movement capabilities do not translate well into observed dispersal. Our objectives were to (i) define the fine‐scale spatial genetic structure in endangered black‐capped vireos to characterize dispersal patterns and (ii) to correlate dispersal dynamics to overall population genetic structure using a simulation approach. We sampled 160 individuals over 2 years to (i) describe the fine‐scale genetic structuring and (ii) used this information to model scenarios to compare with actual data on change in population structuring over a 100‐year interval. We found that black‐capped vireos exhibit male philopatry and restricted dispersal distances, relative to females. Our simulations also support a sex‐biased dispersal model. Additionally, we find that fragmentation related changes in rates of dispersal might be a likely cause for increasing levels of population structure over a 100‐year period. We show that restricted sex‐biased dispersal can explain population structuring in this species and that changes in dispersal rates due to fragmentation may be a continuing threat to genetic viability in this species.     

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.     

Identifying Y-chromosomal diversity by long-template PCR

Comparing Y-chromosomal and mitochondrial haplotype variation is a promising approach to independently investigate paternal and maternal evolutionary histories in wild mammal populations. However, the difficulty of developing male-specific genetic markers, because of its distinctive genetic architecture and the general low level of polymorphisms observed on the Y chromosome, hampers usually an effective application of this approach. Here, we present a further method of the established Y chromosome conserved anchored tagged sequences strategy to develop Y-chromosomal markers by screening introns of male-specific region (MSY) genes for sequence polymorphisms. By applying long-template PCR using target species-specific primers, adequate sequence information of several kb in size can be obtained. We applied this method in the snow vole (Chionomys nivalis) and obtained 12.4 kb of male-specific sequence data for nine males representing four populations in the Swiss Alps. A total of 28 single nucleotide polymorphisms, four indels (> 1 bp) and one polymorphic microsatellite were identified in introns of the SMCY and DBY genes. Based on this information, we developed a Y-chromosomal genotyping assay and identified four different paternal lineages within one local snow vole population. The method we present is straightforward and as such will probably be suitable to detect adequate Y-chromosomal diversity in a wide range of mammalian species.