Translocations maintain genetic diversity and increase connectivity in sea otters,Enhydra lutris

Sea otters, Enhydra lutris, were once abundant along the nearshore areas of the North Pacific. The international maritime fur trade that ended in 1911 left 13 small remnant populations with low genetic diversity. Subsequent translocations into previously occupied habitat resulted in several reintroduced populations along the coast of North America. We sampled sea otters between 2008 and 2011 throughout much of their current range and used 19 nuclear microsatellite markers to evaluate genetic diversity, population structure, and connectivity between remnant and reintroduced populations. Average genetic diversity within populations was similar: observed heterozygosity 0.55 and 0.53, expected heterozygosity 0.56 and 0.52, unbiased expected heterozygosity 0.57 and 0.52, for reintroduced and remnant populations, respectively. Sea otter population structure was greatest between the Northern and Southern sea otters with further structuring in Northern sea otters into Western, Central, and Southeast populations (including the reintroduced populations). Migrant analyses suggest the successful reintroductions and growth of remnant groups have enhanced connectivity and gene flow between populations throughout many of the sampled Northern populations. We recommend that future management actions for the Southern sea otter focus on future reintroductions to fill the gap between the California and Washington populations ultimately restoring gene flow to the isolated California population.     

Divergence genetics analysis reveals historical population genetic processes leading to contrasting phylogeographic patterns in co-distributed species

Coalescent samplers are computational time machines for inferring the historical demographic genetic processes that have given rise to observable patterns of spatial genetic variation among contemporary populations. We have used traditional characterizations of population structure and coalescent‐based inferences about demographic processes to reconstruct the population histories of two co‐distributed marine species, the frilled dog whelk, Nucella lamellosa, and the bat star, Patiria miniata. Analyses of population structure were consistent with previous work in both species except that additional samples of N. lamellosa showed a larger regional genetic break on Vancouver Island (VI) rather than between the southern Alexander Archipelago as in P. miniata. Our understanding of the causes, rather than just the patterns, of spatial genetic variation was dramatically improved by coalescent analyses that emphasized variation in population divergence times. Overall, gene flow was greater in bat stars (planktonic development) than snails (benthic development) but spatially homogeneous within species. In both species, these large phylogeographic breaks corresponded to relatively ancient divergence times between populations rather than regionally restricted gene flow. Although only N. lamellosa shows a large break on VI, population separation times on VI are congruent between species, suggesting a similar response to late Pleistocene ice sheet expansion. The absence of a phylogeographic break in P. miniata on VI can be attributed to greater gene flow and larger effective population size in this species. Such insights put the relative significance of gene flow into a more comprehensive historical biogeographic context and have important implications for conservation and landscape genetic studies that emphasize the role of contemporary gene flow and connectivity in shaping patterns of population differentiation.     

Genetic diversity and population parameters of sea otters, Enhydra lutris, before fur trade extirpation from 1741-1911

All existing sea otter, Enhydra lutris, populations have suffered at least one historic population bottleneck stemming from the fur trade extirpations of the eighteenth and nineteenth centuries. We examined genetic variation, gene flow, and population structure at five microsatellite loci in samples from five pre-fur trade populations throughout the sea otter's historical range: California, Oregon, Washington, Alaska, and Russia. We then compared those values to genetic diversity and population structure found within five modern sea otter populations throughout their current range: California, Prince William Sound, Amchitka Island, Southeast Alaska and Washington. We found twice the genetic diversity in the pre-fur trade populations when compared to modern sea otters, a level of diversity that was similar to levels that are found in other mammal populations that have not experienced population bottlenecks. Even with the significant loss in genetic diversity modern sea otters have retained historical structure. There was greater gene flow before extirpation than that found among modern sea otter populations but the difference was not statistically significant. The most dramatic effect of pre fur trade population extirpation was the loss of genetic diversity. For long term conservation of these populations increasing gene flow and the maintenance of remnant genetic diversity should be encouraged.     

Micro-spatial genetic structure in song sparrows (<Emphasis Type="Italic">Melospiza melodia</Emphasis>)

The spatial genetic structure of populations is strongly influenced by current and historical patterns of gene flow and drift, which in the simplest case, is limited by geographic distance. We examined the microspatial genetic structure within 33 populations of song sparrows (Melospiza melodia) which included eight subspecies located across coastal areas in southern British Columbia (BC) and California. We also examined the effect of water barriers and local density estimates on genetic structuring. Across both regions, positive genetic structure was detectable at distances of less than 10 km. Genetic divergence was highest in Californian subspecies, perhaps due to reduced gene flow across sub-specific contact zones. In BC, populations distributed across islands displayed greater genetic structuring over similar spatial scales than those across mainland sites, supporting the prediction that water barriers reduce gene flow in this species. Our results confirm both the expectation for fine-scale genetic structure in these generally sedentary subspecies, and the role of landscape features in generating geographic variation in genetic structure.     

Genetic diversity and differentiation in a wide ranging anadromous fish,American shad (Alosa sapidissima), is correlated with latitude

Studies that span entire species ranges can provide insight into the relative roles of historical contingency and contemporary factors that influence population structure and can reveal patterns of genetic variation that might otherwise go undetected. American shad is a wide ranging anadromous clupeid fish that exhibits variation in demographic histories and reproductive strategies (both semelparity and iteroparity) and provides a unique perspective on the evolutionary processes that govern the genetic architecture of anadromous fishes. Using 13 microsatellite loci, we examined the magnitude and spatial distribution of genetic variation among 33 populations across the species' range to (i) determine whether signals of historical demography persist among contemporary populations and (ii) assess the effect of different reproductive strategies on population structure. Patterns of genetic diversity and differentiation among populations varied widely and reflect the differential influences of historical demography, microevolutionary processes and anthropogenic factors across the species' range. Sequential reductions of diversity with latitude among formerly glaciated rivers are consistent with stepwise postglacial colonization and successive population founder events. Weak differentiation among U.S. iteroparous populations may be a consequence of human‐mediated gene flow, while weak differentiation among semelparous populations probably reflects natural gene flow. Evidence for an effect of reproductive strategy on population structure suggests an important role for environmental variation and suggests that the factors that are responsible for shaping American shad life history patterns may also influence population genetic structure.     

High genetic diversity in the blue-listed British Columbia population of the purple martin maintained by multiple sources of immigrants

To assess genetic diversity in the blue-listed purple martin (Progne subis) population in British Columbia, we analysed mitochondrial control region sequences of 93 individuals from British Columbia and 121 individuals collected from seven localities of the western and eastern North American subspecies P. s. arboricola and P. s. subis, respectively. Of the 47 haplotypes we detected, 34 were found exclusively in western populations, and 12 were found only in eastern populations. The most common eastern haplotype (25) was also found in three nestlings in British Columbia and one in Washington. Another British Columbia nestling had a haplotype (35) that differed by a C to T transition from haplotype 25. Coalescent analysis indicated that these five nestlings are probably descendents of recent immigrants dispersing from east to the west, because populations were estimated to have diverged about 200,000–400,000 ybp, making ancestral polymorphism a less likely explanation. Maximum likelihood estimates of gene flow among all populations detected asymmetrical gene flow into British Columbia not only of rare migrants from the eastern subspecies in Alberta but also a substantial number of migrants from the adjacent Washington population, and progressively lower numbers from Oregon in an isolation-by distance pattern. The influx of migrants from different populations is consistent with the migrant-pool model of recolonization which has maintained high genetic diversity in the small recovering population in British Columbia. Thus, the risk to this population is not from genetic erosion or inbreeding following a severe population crash, but from demographic stochasticity and extinction in small populations.     

Restricted gene flow in fragmented populations of a wind-pollinated tree

Fragmentation of natural populations can have negative effects at the genetic level, thus threatening their evolutionary potential. Many of the negative genetic impacts of population fragmentation can be ameliorated by gene flow and it has been suggested that in wind-pollinated tree species, high or even increased levels of gene flow are a feature of fragmented populations, although several studies have disputed this. We have used a combination of nuclear microsatellites and allele-specific PCR (AS-PCR) analysis of chloroplast single nucleotide polymorphisms (SNPs) to examine the levels and patterns of genetic diversity and population differentiation in fragmented populations of juniper (Juniperus communis) in Ireland and inform conservation programs for the species. Significant population differentiation was found for both chloroplast and nuclear markers, indicating restricted gene flow, particularly over larger geographic scales. For conservation purposes, the existence of genetically distinct clusters and geographically localised chloroplast haplotypes suggests that the concept of provenance should be taken into account when formulating augmentation or reintroduction strategies. Furthermore, the potential lack of seed dispersal and seedling establishment means that ex-situ approaches to seed and seedling management may have to be considered.     

Silene rothmaleri P. Silva (Caryophyllaceae), a rare, fragmented but genetically diverse species

Silene rothmaleri is an endemic Portuguese species considered extinct until 1992, when it was rediscovered in the wild with a highly fragmented distribution. These rare plants occur along the southwestern Portuguese coast in small populations, which in addition to phenological differences that occur along the north–south gradient could create a pattern of genetic isolation. To evaluate the degree of genetic diversity and estimate the relationship between population fragmentation and genetic variability, we analysed the five known populations of S. rothmaleri using random amplified polymorphic DNA. Degree of polymorphism and Shannon Index of phenotypic diversity revealed high levels of diversity, found mainly within populations. PCo and cluster analysis revealed a distinct north–south cline, which was confirmed by spatial autocorrelation (Mantel) analysis. This indicates the existence of gene flow between small nearby populations and its insufficiency between widely separated populations. Levels of gene flow (Nm) estimated from the Shannon Index reveal a pattern consistent with a larger past distribution that went through a period of contraction and lack of gene flow followed by population differentiation. The central and largest population probably acts as a core of genetic variability inherited as a relict from a larger and more diverse ancestral population.     

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.     

The Pleistocene glacial cycles shaped the historical demography and phylogeography of a pine fungal endophyte

The fungal endophyte Lophodermium nitens is an obligate symbiont of soft pines inhabiting only two pine species in Mexico with a broad distribution of geographically isolated populations. A previous study for the hosts indicated a main east–west subdivision with recurrent gene flow within these regions and demographic expansion of populations. We took these patterns as null hypotheses to test for the demography and phylogeographical patterns of the fungus, given the obligatory relationship of the endophyte to the host and its reduced capacity for long-distance dispersal. For this purpose, we employed two nuclear DNA loci, fragments of the actin and chitin synthase I genes. Both loci showed high genetic variation, consisting of private single-copy alleles, as well as few ones at high frequency that were shared among almost all populations. In order to distinguish between shared polymorphism due to incomplete lineage sorting and gene flow posterior to population divergence, we applied the coalescent-based Isolation–Migration (IM) model. We found patterns of gene flow and isolation similar to those of the hosts as well as signs of population expansion. Mean migration time and divergence time estimates fell within the Pleistocene, previous to Last Glacial Maximum. The results presented here for L. nitens emphasize the potential use of endophytic fungi to deepen the knowledge of historical patterns and processes of their host plants.     

Discordant patterns of evolutionary differentiation in two Neotropical treefrogs

Comparative studies of codistributed taxa test the degree to which historical processes have shaped contemporary population structure. Discordant patterns of lineage divergence among taxa indicate that species differ in their response to common historical processes. The complex geologic landscape of the Isthmus of Central America provides an ideal setting to test the effects of vicariance and other biogeographic factors on population history. We compared divergence patterns between two codistributed Neotropical frogs ( Dendropsophus ebraccatus and Agalychnis callidryas ) that exhibit colour pattern polymorphisms among populations, and found significant differences between them in phenotypic and genetic divergence among populations. Colour pattern in D. ebraccatus did not vary with genetic or geographic distance, while colour pattern co-varied with patterns of gene flow in A. callidryas . In addition, we detected significant species differences in the phylogenetic history of populations, gene flow among them, and the extent to which historical diversification and recent gene flow have been restricted by five biogeographic barriers in Costa Rica and Panama. We inferred that alternate microevolutionary processes explain the unique patterns of diversification in each taxon. Our study underscores how differences in selective regimes and species-typical ecological and life-history traits maintain spatial patterns of diversification.     

EFFECTS OF INTRINSIC AND EXTRINSIC FACTORS ON POPULATION FRAGMENTATION IN THREE SPECIES OF NORTH AMERICAN MINNOWS (TELEOSTEI: CYPRINIDAE)

Geographic patterns of genetic variation (mitochondrial DNA [mtDNA] and allozymes) were used to examine effects of intrinsic characteristics (e.g., vagility, habitat specificity, and reproductive behaviors) and extrinsic factors (e.g., climatic and geological history) on population fragmentation. The three species of cyprinid fishes examined (Tiaroga cobitis, Meda fulgida, and Agosia chrysogaster) occupied similar historical ranges within the lower Colorado River drainage, but differ in intrinsic characteristics conducive to population fragmentation. Relationships among populations were similar across species, reflecting common historical influences, but results indicate the distribution of variation among species is strongly affected by intrinsic characteristics. Variation within two species (T. cobitis and M. fulgida) is subdivided among populations, suggesting little gene flow among rivers. In contrast, similarity of A. chrysogaster populations throughout the Gila River drainage supports the hypothesis that levels of gene flow are high for this species. Levels of mtDNA divergence were much higher than expected for both T. cobitis and A. chrysogaster suggesting long-term isolation of geographic regions. These results indicate that both long-term and short-term extrinsic factors have shaped basic patterns of variation within these fishes; however, the intrinsic characteristics of each species have strongly affected the population genetic structure of these fishes.     

Contrasting Patterns of Genetic Differentiation among Blackcaps (Sylvia atricapilla) with Divergent Migratory Orientations in Europe

Migratory divides are thought to facilitate behavioral, ecological, and genetic divergence among populations with different migratory routes. However, it is currently contentious how much genetic divergence is needed to maintain distinct migratory behavior across migratory divides. Here we investigate patterns of neutral genetic differentiation among Blackcap (Sylvia atricapilla) populations with different migratory strategies across Europe. We compare the level of genetic divergence of populations migrating to southwestern (SW) or southeastern (SE) wintering areas with birds wintering in the British Isles following a recently established northwesterly (NW) migration route. The migratory divide between SW and SE wintering areas can be interpreted as a result of a re-colonization process after the last glaciation. Thus we predicted greater levels of genetic differentiation among the SW/SE populations. However, a lack of genetic differentiation was found between SW and SE populations, suggesting that interbreeding likely occurs among Blackcaps with different migratory orientations across a large area; therefore the SW/SE migratory divide can be seen as diffuse, broad band and is, at best, a weak isolating barrier. Conversely, weak, albeit significant genetic differentiation was evident between NW and SW migrants breeding sympatrically in southern Germany, suggesting a stronger isolating mechanism may be acting in this population. Populations located within/near the SW/SE contact zone were the least genetically divergent from NW migrants, confirming NW migrants likely originated from within the contact zone. Significant isolation-by-distance was found among eastern Blackcap populations (i.e. SE migrants), but not among western populations (i.e. NW and SW migrants), revealing different patterns of genetic divergence among Blackcap populations in Europe. We discuss possible explanations for the genetic structure of European Blackcaps and how gene flow influences the persistence of divergent migratory behaviors.     

Exploring demographic, physical, and historical explanations for the genetic structure of two lineages of Greater Antillean bats

Observed patterns of genetic structure result from the interactions of demographic, physical, and historical influences on gene flow. The particular strength of various factors in governing gene flow, however, may differ between species in biologically relevant ways. We investigated the role of demographic factors (population size and sex-biased dispersal) and physical features (geographic distance, island size and climatological winds) on patterns of genetic structure and gene flow for two lineages of Greater Antillean bats. We used microsatellite genetic data to estimate demographic characteristics, infer population genetic structure, and estimate gene flow among island populations of Erophylla sezekorni/E. bombifrons and Macrotus waterhousii (Chiroptera: Phyllostomidae). Using a landscape genetics approach, we asked if geographic distance, island size, or climatological winds mediate historical gene flow in this system. Samples from 13 islands spanning Erophylla's range clustered into five genetically distinct populations. Samples of M. waterhousii from eight islands represented eight genetically distinct populations. While we found evidence that a majority of historical gene flow between genetic populations was asymmetric for both lineages, we were not able to entirely rule out incomplete lineage sorting in generating this pattern. We found no evidence of contemporary gene flow except between two genetic populations of Erophylla. Both lineages exhibited significant isolation by geographic distance. Patterns of genetic structure and gene flow, however, were not explained by differences in relative effective population sizes, island area, sex-biased dispersal (tested only for Erophylla), or surface-level climatological winds. Gene flow among islands appears to be highly restricted, particularly for M. waterhousii, and we suggest that this species deserves increased taxonomic attention and conservation concern.     

SPECIATION AND POPULATION GENETIC STRUCTURE IN TROPICAL PACIFIC SEA URCHINS

Unlike populations of many terrestrial species, marine populations often are not separated by obvious, permanent barriers to gene flow. When species have high dispersal potential and few barriers to gene flow, allopatric divergence is slow. Nevertheless, many marine species are of recent origin, even in taxa with high dispersal potential. To understand the relationship between genetic structure and recent species formation in high dispersal taxa, we examined population genetic structure among four species of sea urchins in the tropical Indo-West Pacific that have speciated within the past one to three million years. Despite high potential for gene flow, mtDNA sequence variation among 200 individuals of four species in the urchin genus Echinometra shows a signal of strong geographic effects. These effects include (1) substantial population heterogeneity; (2) lower genetic variation in peripheral populations; and (3) isolation by distance. These geographic patterns are especially strong across scales of 5000-10,000 km, and are weaker over scales of 2500-5000 km. As a result, strong geographic patterns would not have been readily visible except over the wide expanse of the tropical Pacific. Surface currents in the Pacific do not explain patterns of gene flow any better than do patterns of simple spatial proximity. Finally, populations of each species tend to group into large mtDNA regions with similar mtDNA haplotypes, but these regional boundaries are not concordant in different species. These results show that all four species have accumulated mtDNA differences over similar spatial and temporal scales but that the precise geographic pattern of genetic differentiation varies for each species. These geographic patterns appear much less deterministic than in other well-known coastal marine systems and may be driven by chance and historical accident.     

Genetic structure of European pine martens (Martes martes), and evidence for introgression with M. americana in England

European pine martens (Martes martes)were once distributed across much ofwestern Europe. A combination of factors, suchas persecution, trapping, and habitat loss haveled to sharp declines in the species' numbersand range and, as such, local populations havebecome more vulnerable to extinction. Toevaluate the influence of these factors on boththe level of genetic variation and populationstructure, we genotyped pine martens fromacross much of their current distribution. Continental M. martes populations werefound to have a higher level of geneticstructure and lower genetic variation thantheir North American sibling species, M.americana, sampled throughout Canada. Thedifferences among mainland populations of thesespecies may lie in greater levels of habitatfragmentation and persecution experienced byEuropean martens, though it is difficult toexclude more ancient processes such as theinfluence of glaciations. Among islandpopulations of the two species, the Scottishpopulation revealed a similar level ofstructure and variation to the M. a.atrata population of Newfoundland, howeverIreland was more differentiated with lessgenetic variation. Our work usingmicrosatellites also extends previous mtDNAevidence for the presence of M. americanahaplotypes in England, raising the possibilityof hybridization with M. martes. Thesefindings may influence current discussions onthe status of English martens and theappropriateness of proposed re-introductions byrevealing that some indigenous martens persistin England, despite the presence of somepotential hybrids in the region.     

Utility of the methylation-sensitive amplified polymorphism (MSAP) marker for detection of DNA methylation polymorphism and epigenetic population structure in a wild barley species (<Emphasis Type="Italic">Hordeum brevisubulatum</Emphasis>)

We report here that by using a modified scoring criterion, the methylation-sensitive amplified polymorphism or MSAP marker can be used effectively to detect polymorphism in DNA methylation patterns within and among populations of a perennial wild barley species, Hordeum brevisubulatum. Twenty-four selected individual genotypes representing four natural populations of H. brevisubulatum distributed in the Songnen Prairie in northeastern China were studied. The utility of MSAP was evidenced by its detection of high levels of polymorphism in DNA methylation patterns between individuals within a given population, and the clear inter-population differentiation in methylation patterns (methylation-based epigenetic population structure) revealed among the four populations. The resolving power of MSAP to detect DNA methylation polymorphism was found to be comparable with that of a retrotransposon-based sequence-specific amplified polymorphism marker, or SSAP, to detect genetic polymorphism in the same set of plants, suggesting that MSAP with a modified scoring criterion can be used efficiently to detect DNA methylation polymorphism and assess epigenetic population structure in natural plant populations. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Spatiotemporal analysis of gene flow in Chesapeake Bay Diamondback Terrapins (Malaclemys terrapin)

There is widespread concern regarding the impacts of anthropogenic activities on connectivity among populations of plants and animals, and understanding how contemporary and historical processes shape metapopulation dynamics is crucial for setting appropriate conservation targets. We used genetic data to identify population clusters and quantify gene flow over historical and contemporary time frames in the Diamondback Terrapin (Malaclemys terrapin). This species has a long and complicated history with humans, including commercial overharvesting and subsequent translocation events during the early twentieth century. Today, terrapins face threats from habitat loss and mortality in fisheries bycatch. To evaluate population structure and gene flow among Diamondback Terrapin populations in the Chesapeake Bay region, we sampled 617 individuals from 15 localities and screened individuals at 12 polymorphic microsatellite loci. Our goals were to demarcate metapopulation structure, quantify genetic diversity, estimate effective population sizes, and document temporal changes in gene flow. We found that terrapins in the Chesapeake Bay region harbour high levels of genetic diversity and form four populations. Effective population sizes were variable. Among most population comparisons, estimates of historical and contemporary terrapin gene flow were generally low (m ≈ 0.01). However, we detected a substantial increase in contemporary gene flow into Chesapeake Bay from populations outside the bay, as well as between two populations within Chesapeake Bay, possibly as a consequence of translocations during the early twentieth century. Our study shows that inferences across multiple time scales are needed to evaluate population connectivity, especially as recent changes may identify threats to population persistence.     

Linking genetic and ecological differentiation in an ungulate with a circumpolar distribution

Genetic differentiation among populations may arise from the disruption of gene flow due to local adaptation to distinct environments and/or neutral accumulation of mutations and genetic drift resulted from geographical isolation. Quantifying the role of these processes in determining the genetic structure of natural populations remains challenging. Here, we analyze the relative contribution of isolation‐by‐resistance (IBR), isolation‐by‐environment (IBE), genetic drift and historical isolation in allopatry during Pleistocene glacial cycles on shaping patterns of genetic differentiation in caribou/reindeer populations Rangifer tarandus across the entire distribution range of the species. Our study integrates analyses at range‐wide and regional scales to partial out the effects of historical and contemporary isolation mechanisms. At the circumpolar scale, our results indicate that genetic differentiation is predominantly explained by IBR and historical isolation. At a regional scale, we found that IBR, IBE and population size significantly explained the spatial distribution of genetic variation among populations belonging to the Euro‐Beringian lineage within North America. In contrast, genetic differentiation among populations within the North American lineage was predominantly explained by IBR and population size, but not IBE. We also found discrepancies between genetic and ecotype designation across the Holarctic species distribution range. Overall, these results indicate that multiple isolating mechanisms have played roles in shaping the spatial distribution of genetic variation across the distribution range of a large mammal with high potential for gene flow. Considering multiple spatial scales and simultaneously testing a comprehensive suite of potential isolating mechanisms, our study contributes to understand the ecological and evolutionary processes underlying organism–landscape interactions.