Genetic consequences of group living in Mongolian gerbils

Social behavior can shape the local population genetic structure of mammals. Group living can increase pairwise genetic relatedness of mammals at a local level but differentiate the genetic structure at a population level through offspring philopatry and nonrandom mating. Our study aimed to test the hypothesis that social groups of Mongolian gerbils (Meriones unguiculatus) would consist of genetically related individuals due to offspring philopatry and would have distinct genetic structures because of restricted gene flow among social groups and nonrandom mating. We genotyped 327 wild gerbils, live captured from 28 social groups in Inner Mongolia, China, using nine microsatellite loci. The within-group pairwise genetic relatedness coefficient averaged 0.28 ± 0.14 (standard deviation), whereas the average pairwise genetic relatedness coefficient of the whole gerbil population was 0.0 ± 0.2. Additionally, the value of the global F statistic (F(st)) was 0.21, suggesting a substantial genetic differentiation among social groups of Mongolian gerbils. The Bayesian clustering divided the 327 gerbils into 23 distinct genetic clusters. Therefore, our results show that high within-group genetic relatedness and among-group genetic differentiation are the genetic consequences of group living in social mammals because of restricted gene flow, female philopatry, and nonrandom mating within social groups.     

Variation in migratory behavior influences regional genetic diversity and structure among American Kestrel populations (Falco sparverius) in North America

Birds employ numerous strategies to cope with seasonal fluctuations in high-quality habitat availability. Long distance migration is a common tactic; however, partial migration is especially common among broadly distributed species. Under partial migration systems, a portion of a species migrates, whereas the remainder inhabits breeding grounds year round. In this study, we identified effects of migratory behavior variation on genetic structure and diversity of American Kestrels (Falco sparverius), a widespread partial migrant in North America. American Kestrels generally migrate; however, a resident group inhabits the southeastern United States year round. The southeastern group is designated as a separate subspecies (F. s. paulus) from the migratory group (F. s. sparverius). Using mitochondrial DNA and microsatellites from 183 and 211 individuals, respectively, we illustrate that genetic structure is stronger among nonmigratory populations, with differentiation measures ranging from 0.060 to 0.189 depending on genetic marker and analysis approach. In contrast, measures from western North American populations ranged from 0 to 0.032. These findings suggest that seasonal migratory behavior is also associated with natal and breeding dispersal tendencies. We likewise detected significantly lower genetic diversity within nonmigratory populations, reflecting the greater influence of genetic drift in small populations. We identified the signal of population expansion among nonmigratory populations, consistent with the recent establishment of higher latitude breeding locations following Pleistocene glacial retreat. Differentiation of F. s. paulus and F. s. sparverius reflected subtle differences in allele frequencies. Because migratory behavior can evolve quickly, our analyses suggest recent origins of migratory American Kestrel populations in North America.     

Founder events as determinants of within-island and among-island genetic structure of Daphnia metapopulations

The genetic structure of metapopulations offers insights into the genetic consequences of local extinction and recolonization. We studied allozyme variation in rock pool metapopulations of two species of waterfleas (Daphnia) with the aim to understand how these dynamics influence genetic differentiation. We screened 138 populations of D. magna and 65 populations of D. longispina from an area in the archipelago of southern Finland. The pools from which they were sampled are separated by distances between 1.5 and 4710 m and located on a total of 38 islands. The genetic population structure of the two species was strikingly similar, consistent with their similar metapopulation ecology. The mean F(PT) value (differentiation among pools with respect to the total metapopulation) was 0.55 and a hierarchical analysis showed that genetic differentiation was strong (>0.25) among pools within islands as well as among whole islands. Within islands, pairwise genetic differentiation increased with geographic distance, indicating isolation by distance due to spatially limited dispersal. Previous studies have shown strong founder events occurring during colonization in our metapopulation. We suggest that the genetic population structure in the studied metapopulations is largely explained by three consequences of these founder events: (i) strong drift during colonization, (ii) local inbreeding, which results in hybrid vigour and increased effective migration rates after subsequent immigration, and (iii) effects of selection through hitchhiking of neutral genes with linked loci under selection.     

Minisatellite mutational processes reduce Fst estimates

We have used a new method for binning minisatellite alleles (semi-automated allele aggregation) and report the extent of population diversity detectable by eleven minisatellite loci in 2,689 individuals from 19 human populations distributed widely throughout the world. Whereas population relationships are consistent with those found in other studies, our estimate of genetic differentiation (F(st)) between populations is less than 8%, which is lower than comparative estimates of between 10%-15% obtained by using other sources of polymorphism data. We infer that mutational processes are involved in reducing F(st) estimates from minisatellite data because, first, the lowest F(st) estimates are found at loci showing autocorrelated frequencies among alleles of similar size and, second, F(st) declines with heterozygosity but by more than predicted assuming simple models of mutation. These conclusions are consistent with the view that minisatellites are subject to selective or mutational constraints in addition to those expected under simple step-wise mutation models.     

Convergent development of low-relatedness supercolonies in Myrmica ants

Many ant species have independently evolved colony structures with multiple queens and very low relatedness among nestmate workers, but it has remained unclear whether low-relatedness kin structures can repeatedly arise in populations of the same species. Here we report a study of Danish island populations of the red ant Myrmica sulcinodis and show that it is likely that such repeated developments occur. Two microsatellite loci were used to estimate genetic differentiation (F(ST)) among three populations and nestmate relatedness within these populations. The F(ST) values were highly significant due to very different allele frequencies among the three populations with relatively few common alleles and relatively many rare alleles, possibly caused by single queen foundation and rare subsequent immigration. Given the isolation of the islands and the low investment in reproduction, we infer that each of the populations was most likely established by a single queen, even though all three extant populations now have within-colony relatedness 95%), and the genetic differentiation of nests showed a significantly positive correlation with the distance between them. Both male-biased sex-ratio and genetic viscosity are expected characteristics of populations where queens have very local dispersal and where new colonies are initiated through nest-budding. Based on a comparison with other M. sulcinodis populations we hypothesise a distinct succession of population types and suggest that this may be a possible pathway to unicoloniality, ie, development towards a complete lack of colony kin structure and unrelated nestmate workers.     

Microgeographic population structure of brook charr: a comparison of microsatellite and mark-recapture data

Polymorphism at five microsatellite genetic markers (genotyped n  = 496) and mark-recapture tagging data (tagged n  = 9813) were used to define the population structure of brook charr, Salvelinus fontinalis from the Indian Bay watershed, Newfoundland, Canada. Despite the absence of physical barriers to migration among lakes, both genetic and tagging data suggest that brook charr in each lake represent reproductively isolated populations. Exact tests comparing allele frequencies, θ (global value = 0·063), R st (global value = 0·052), individual assignment tests, and Nei's genetic distance provided congruent estimates of population subdivision in agreement with the tagging data (only 2·2% of recaptures were lake-to-lake). The genetic structure of the brook charr populations corresponded with the geographic structure of the drainage basin on a qualitative level, although linear distance over water was not significantly correlated with the tagging data or the genetic distance measures. The agreement between the tagging and the genetic data suggest that microsatellite markers can be useful tools for defining real biological units. The results also suggest that brook charr exhibit microgeographic population structure at the watershed scale, and that this is the scale at which conservation and management of this salmonid might best be implemented.     

Mathematical properties of Fst between admixed populations and their parental source populations

We consider the properties of the F(st) measure of genetic divergence between an admixed population and its parental source populations. Among all possible populations admixed among an arbitrary set of parental populations, we show that the value of F(st) between an admixed population and a specific source population is maximized when the admixed population is simply the most distant of the other source populations. For the case with only two parental populations, as a function of the admixture fraction, we further demonstrate that this F(st) value is monotonic and convex, so that F(st) is informative about the admixture fraction. We illustrate our results using example human population-genetic data, showing how they provide a framework in which to interpret the features of F(st) in admixed populations.     

Microsatellites and the Genetics of Highly Selfing Populations in the Freshwater Snail Bulinus Truncatus

Hermaphrodite tropical freshwater snails provide a good opportunity to study the effects of mating system and genetic drift on population genetic structure because they are self-fertile and they occupy transient patchily distributed habitats (ponds). Up to now the lack of detectable allozyme polymorphism prevented any intrapopulation studies. In this paper, we examine the consequences of selfing and bottlenecks on genetic polymorphism using microsatellite markers in 14 natural populations (under a hierarchical sampling design) of the hermaphrodite freshwater snail Bulinus truncatus. These population genetics data allowed us to discuss the currently available mutation models for microsatellite sequences. Microsatellite markers revealed an unexpectedly high levels of genetic variation with <=41 alleles for one locus and gene diversity of 0.20-0.75 among populations. The values of any estimator of F(is) indicate high selfing rates in all populations. Linkage disequilibria observed at all loci for some populations may also indicate high levels of inbreeding. The large extent of genetic differentiation measured by F(st), R(st) or by a test for homogeneity between genic distributions is explained by both selfing and bottlenecks. Despite a limited gene flow, migration events could be detected when comparing different populations within ponds.     

Genetic relationships of American alligator populations distributed across different ecological and geographic scales

Although much work has been conducted on coastal populations of the American alligator (Alligator mississippiensis), less is known about the population dynamics and genetic structure of populations of alligators confined to inland habitats. DNA microsatellite loci, derived from the American alligator, were used to investigate patterns of genetic variation within and between populations of alligators distributed at coastal and inland localities in Texas. These data were used to evaluate the genetic discreteness of different alligator stocks relative to their basic ecology at these sites. Observed mean heterozygosities across seven loci for both coastal and inland populations ranged from 0.50-0.61, with both inland and coastal populations revealing similar patterns of variation. Measures of F(st) revealed significant population differentiation among all populations; however, analyses of molecular variance (AMOVAs) failed to demonstrate any apparent geographic pattern relative to the population differentiation indicated by F(st) values. Each population contained unique alleles for at least one locus. Additionally, assignment tests based on the distribution of genotypes placed 76% of individuals to their source population. These genetic data suggest considerable subdivision among alligator populations, possibly influenced by demographic and life history differences as well as barriers to dispersal. These results have clear implications for management. Rather than managing alligators in Texas as a single panmictic population, translocation programs and harvest quotas should consider the ecological and genetic distinctiveness of local alligator populations.     

Global analysis of regional differences in craniometric diversity and population substructure.

Estimates of genetic diversity in major geographic regions are frequently made by pooling all individuals into regional aggregates. This method can potentially bias results if there are differences in population substructure within regions, since increased variation among local populations could inflate regional diversity. A preferred method of estimating regional diversity is to compute the mean diversity within local populations. Both methods are applied to a global sample of craniometric data consisting of 57 measurements taken on 1734 crania from 18 local populations in six geographic regions: sub-Saharan Africa, Europe, East Asia, Australasia, Polynesia, and the Americas. Each region is represented by three local populations. Both methods for estimating regional diversity show sub-Saharan Africa to have the highest levels of phenotypic variation, consistent with many genetic studies. Polynesia and the Americas both show high levels of regional diversity when regional aggregates are used, but the lowest mean local population diversity. Regional estimates of F(ST) made using quantitative genetic methods show that both Polynesia and the Americas also have the highest levels of differentiation among local populations, which inflates regional diversity. Regional differences in F(ST) are directly related to the geographic dispersion of samples within each region; higher F(ST) values occur when the local populations are geographically dispersed. These results show that geographic sampling can affect results, and suggest caution in making inferences regarding regional diversity when population substructure is ignored.     

Fine-scale spatial genetic structure and dispersal among spotted salamander (Ambystoma maculatum) breeding populations

We examined fine-scale genetic variation among breeding aggregations of the spotted salamander (Ambystoma maculatum) to quantify dispersal, interpopulation connectivity and population genetic structure. Spotted salamanders rely on temporary ponds or wetlands for aggregate breeding. Adequate breeding sites are relatively isolated from one another and field studies suggest considerable adult site fidelity; therefore, we expected to find population structure and differentiation at small spatial scales. We used microsatellites to estimate population structure and dispersal among 29 breeding aggregations in Tompkins County, New York, USA, an area encompassing 1272 km(2). Bayesian and frequency-based analyses revealed fine-scale genetic structure with two genetically defined demes: the North deme included seven breeding ponds, and the South deme included 13 ponds. Nine ponds showed evidence of admixture between these two genetic pools. Bayesian assignment tests for detection of interpopulation dispersal indicate that immigration among ponds is common within demes, and that certain populations serve as sources of immigrants to neighbouring ponds. Likewise, spatial genetic correlation analyses showed that populations < or = 4.8 km distant from each other show significant genetic correlation that is not evident at higher scales. Within-population levels of relatedness are consistently larger than expected if mating were completely random across ponds, and in the case of a few ponds, within-population processes such as inbreeding or reproductive skew contribute significantly to differentiation from neighbouring ponds. Our data underscore the importance of these within-population processes as a source of genetic diversity across the landscape, despite considerable population connectivity. Our data further suggest that spotted salamander breeding groups behave as metapopulations, with population clusters as functional units, but sufficient migration among demes to allow for potential rescue and recolonization. Amphibian habitats are becoming increasingly fragmented and a clear understanding of dispersal and patterns of population connectivity for taxa with different ecologies and life histories is crucial for their conservation.     

Connectivity and gene flow among Eastern Tiger Salamander (Ambystoma tigrinum) populations in highly modified anthropogenic landscapes

Fragmented landscapes resulting from anthropogenic habitat modification can have significant impacts on dispersal, gene flow, and persistence of wildlife populations. Therefore, quantifying population connectivity across a mosaic of habitats in highly modified landscapes is critical for the development of conservation management plans for threatened populations. Endangered populations of the eastern tiger salamander (Ambystoma tigrinum) in New York and New Jersey are at the northern edge of the species’ range and remaining populations persist in highly developed landscapes in both states. We used landscape genetic approaches to examine regional genetic population structure and potential barriers to migration among remaining populations. Despite the post-glacial demographic processes that have shaped genetic diversity in tiger salamander populations at the northern extent of their range, we found that populations in each state belong to distinct genetic clusters, consistent with the large geographic distance that separates them. We detected overall low genetic diversity and high relatedness within populations, likely due to recent range expansion, isolation, and relatively small population sizes. Nonetheless, landscape connectivity analyses reveal habitat corridors among remaining breeding ponds. Furthermore, molecular estimates of population connectivity among ponds indicate that gene flow still occurs at regional scales. Further fragmentation of remaining habitat will potentially restrict dispersal among breeding ponds, cause the erosion of genetic diversity, and exacerbate already high levels of inbreeding. We recommend the continued management and maintenance of habitat corridors to ensure long-term viability of these endangered populations.     

Dynamics of Fst for the island model

F(st) is a measure of genetic differentiation in a subdivided population. Sewall Wright observed that F(st)=1/1+2Nm in a haploid diallelic infinite island model, where N is the effective population size of each deme and m is the migration rate. In demonstrating this result, Wright relied on the infinite size of the population. Natural populations are not infinite and therefore they change over time due to genetic drift. In a finite population, F(st) becomes a random variable that evolves over time. In this work we ask, given an initial population state, what are the dynamics of the mean and variance of F(st) under the finite island model? In application both of these quantities are critical in the evaluation of F(st) data. We show that after a time of order N generations the mean of F(st) is slightly biased below 1/1+2Nm. Further we show that the variance of F(st) is of order 1/d where d is the number of demes in the population. We introduce several new mathematical techniques to analyze coalescent genealogies in a dynamic setting.     

Marker-inferred relatedness as a tool for detecting heritability in nature

This paper presents a perspective of how inferred relatedness, based on genetic marker data such as microsatellites or amplified fragment length polymorphisms (AFLPs), can be used to demonstrate quantitative genetic variation in natural populations. Variation at two levels is considered: among pairs of individuals within populations, and among pairs of subpopulations within a population. In the former, inferred pairwise relatedness, combined with trait measures, allow estimates of heritability 'in the wild'. In the latter, estimates of QST are obtained, in the absence of known heritabilities, via estimates of pairwise FST. Estimators of relatedness based on the 'Kronecker operator' are given. Both methods require actual variation of relationship, a rarely studied aspect of population structure, and not necessarily present. Some conditions for appropriate population structures in the wild are identified, in part through a review of recent studies.     

Adaptive gradients and isolation-by-distance with postglacial migration in Picea sitchensis

Fossil pollen records suggest rapid migration of tree species in response to Quaternary climate warming. Long-distance dispersal and high gene flow would facilitate rapid migration, but would initially homogenize variation among populations. However, contemporary clinal variation in adaptive traits along environmental gradients shown in many tree species suggests that local adaptation can occur during rapid migration over just a few generations in interglacial periods. In this study, we compared growth performance and pollen genetic structure among populations to investigate how populations of Sitka spruce (Picea sitchensis) have responded to local selection along the historical migration route. The results suggest strong adaptive divergence among populations (average Q(ST)=0.61), corresponding to climatic gradients. The population genetic structure, determined by microsatellite markers (R(ST)=0.09; F(ST)=0.11), was higher than previous estimates from less polymorphic genetic markers. The significant correlation between geographic and pollen haplotype genetic (R(ST)) distances (r=0.73, P<0.01) indicates that the current genetic structure has been shaped by isolation-by-distance, and has developed in relatively few generations. This suggests relatively limited gene flow among populations on a recent timescale. Gene flow from neighboring populations may have provided genetic diversity to founder populations during rapid migration in the early stages of range expansion. Increased genetic diversity subsequently enhanced the efficiency of local selection, limiting gene flow primarily to among similar environments and facilitating the evolution of adaptive clinal variation along environmental gradients.     

Extranuclear differentiation and gene flow in the finite island model

Use of sequence information from extranuclear genomes to examine deme structure in natural populations has been hampered by lack of clear linkage between sequence relatedness and rates of mutation and migration among demes. Here, we approach this problem in two complementary ways. First, we develop a model of extranuclear genomes in a population divided into a finite number of demes. Sex-dependent migration, neutral mutation, unequal genetic contribution of separate sexes and random genetic drift in each deme are incorporated for generality. From this model, we derive the relationship between gene identity probabilities (between and within demes) and migration rate, mutation rate and effective deme size. Second, we show how within- and between-deme identity probabilities may be calculated from restriction maps of mitochondrial (mt) DNA. These results, when coupled with our results on gene flow and genetic differentiation, allow estimation of relative interdeme gene flow when deme sizes are constant and genetic variants are selectively neutral. We illustrate use of our results by reanalyzing published data on mtDNA in mouse populations from around the world and show that their geographic differentiation is consistent with an island model of deme structure.     

Panmixia in Zoarces viviparus: implications for environmental monitoring studies

In this study, the genetic population structure of the eelpout Zoarces viviparus was investigated by using microsatellites. Samples were collected at 10 sites in the Baltic Sea, covering a distance of c. 90 km. Ten newly developed microsatellite loci were used to infer the population structure. No global spatial genetic differentiation was found (global F(ST) = 0·0001; D(est) = -0·0003), indicating strong gene flow at this scale, nor any clear pattern of isolation by distance. The results suggest that gene flow among the studied populations of Z. viviparus is stronger than usually thought, which might be caused by environmental homogeneity. This is important for planning and evaluating monitoring activities in this species and for the interpretation of ecotoxicological studies. Strong migration might lead to wrong conclusions concerning the pollution in a given area. Therefore, reference stations should be placed at a larger distance than presently practiced.     

Spatial isolation and genetic differentiation in naturally fragmented plant populations of the Swiss Alps

Aims The effect of anthropogenic landscape fragmentation on the genetic diversity and adaptive potential of plant populations is a major issue in conservation biology. However, little is known about the partitioning of genetic diversity in alpine species, which occur in naturally fragmented habitats. Here, we investigate molecular patterns of three alpine plants (Epilobium fleischeri, Geum reptans and Campanula thyrsoides) across Switzerland and ask whether spatial isolation has led to high levels of population differentiation, increasing over distance, and a decrease of within-population variability. We further hypothesize that the contrasting potential for long-distance dispersal (LDD) of seed in these species will considerably influence and explain diversity partitioning.Methods For each study species, we sampled 20–23 individuals from each of 20–32 populations across entire Switzerland. We applied Random Amplified Polymorphic Dimorphism markers to assess genetic diversity within (Nei's expected heterozygosity, H e; percentage of polymorphic bands, P p) and among (analysis of molecular variance, Φ st) populations and correlated population size and altitude with within-population diversity. Spatial patterns of genetic relatedness were investigated using Mantel tests and standardized major axis regression as well as unweighted pair group method with arithmetic mean cluster analyses and Monmonier's algorithm. To avoid known biases, we standardized the numbers of populations, individuals and markers using multiple random reductions. We modelled LDD with a high alpine wind data set using the terminal velocity and height of seed release as key parameters. Additionally, we assessed a number of important life-history traits and factors that potentially influence genetic diversity partitioning (e.g. breeding system, longevity and population size).Important findings For all three species, we found a significant isolation-by-distance relationship but only a moderately high differentiation among populations (Φ st : 22.7, 14.8 and 16.8%, for E. fleischeri, G. reptans and C. thyrsoides, respectively). Within-population diversity (H e : 0.19–0.21, P p : 62–75%) was not reduced in comparison to known results from lowland species and even small populations with <50 reproductive individuals contained high levels of genetic diversity. We further found no indication that a high long-distance seed dispersal potential enhances genetic connectivity among populations. Gene flow seems to have a strong stochastic component causing large dissimilarity between population pairs irrespective of the spatial distance. Our results suggest that other life-history traits, especially the breeding system, may play an important role in genetic diversity partitioning. We conclude that spatial isolation in the alpine environment has a strong influence on population relatedness but that a number of factors can considerably influence the strength of this relationship.     

Relative influences of historical and contemporary forces shaping the distribution of genetic variation in the Atlantic killifish, Fundulus heteroclitus

A major goal of population genetics research is to identify the relative influences of historical and contemporary processes that serve to structure genetic variation. Most population genetic models assume that populations exist in a state of migration-drift equilibrium. However, in the past this assumption has rarely been verified, and is likely rarely achieved in natural populations. We assessed the equilibrium status at both local and regional scales of the Atlantic killifish, Fundulus heteroclitus . This species is a model organism for the study of adaptive clinal variation, but has also experienced a complicated history of range expansion and secondary contact following allopatric divergence, potentially obscuring the influence of contemporary evolutionary processes. Presumptively neutral genetic markers (microsatellites) demonstrated zones of secondary intergradation among coastal populations centred around northern New Jersey and the Chesapeake Bay region. Analysis of genetic variation indicated isolation by distance among some populations and provided supporting evidence that the Delaware Bay, but not the Chesapeake Bay, has acted as a barrier to dispersal among coastal populations. Bayesian estimates indicated large effective population sizes and low migration rates, and were in good agreement with empirically derived estimates of population and neighbourhood size from mark–recapture studies. These data indicate that populations are not in migration-drift equilibrium at a regional scale, and suggest that contributing factors include large population size combined with relatively low migration rates. These conditions should be considered when interpreting the evolutionary significance of the distribution of genetic variation among F. heteroclitus populations.     

Spatial genetic structure in populations of the terrestrial orchid Cephalanthera longibracteata (Orchidaceae)

Orchid seeds are unusual for being the smallest among flowering plants. These dust-like seeds are wind-borne and, thus, would seem to have the potential for long-distance dispersal (a common perception); this perception has led to a prediction of near-random spatial genetic structure within orchid populations. Mathematical models (e.g., simple ballistic model) for wind-dispersed seeds and wind-tunnel experiments, in contrast, indicate that most seeds of orchids should fall close to the maternal plant (<6 m), supporting a prediction of significant fine-scale genetic structure within populations. In reality we do not know much about seed dispersion in orchids. To determine which of these two predictions is more appropriate, Wright's F statistics and spatial autocorrelation analysis were used to examine the genetic structure within two adult populations of the terrestrial orchid Cephalanthera longibracteata (Orchidaceae) in southern Korea. In results comparable to those of other self-compatible, mixed-mating plant species, C. longibracteata populations exhibited low levels of genetic diversity (mean H(e) = 0.036) and a significant excess of homozygosity (mean F(IS) = 0.330), consistent with substantial inbreeding via selfing and/or mating among close relatives in a spatially structured population. Spatial autocorrelation analysis revealed significant positive genetic correlations among plants located <10 m, with relatedness at <3 m comparable to that expected for half sibs and first cousins. This genetic structure supports the prediction that the majority of seed dispersal occurs over distances of less than 10 m and is responsible for generating substantial overlap in seed shadows within C. longibracteata populations.