Reconstructing the evolutionary history of an endangered subspecies across the changing landscape of the Great Central Valley of California

Identifying historic patterns of population genetic diversity and connectivity is a primary challenge in efforts to re‐establish the processes that have generated and maintained genetic variation across natural landscapes. The challenge of reconstructing pattern and process is even greater in highly altered landscapes where population extinctions and dramatic demographic fluctuations in remnant populations may have substantially altered, if not eliminated, historic patterns. Here, we seek to reconstruct historic patterns of diversity and connectivity in an endangered subspecies of woodrat that now occupies only 1–2 remnant locations within the highly altered landscape of the Great Central Valley of California. We examine patterns of diversity and connectivity using 14 microsatellite loci and sequence data from a mitochondrial locus and a nuclear intron. We reconstruct temporal change in habitat availability to establish several historical scenarios that could have led to contemporary patterns of diversity, and use an approximate Bayesian computation approach to test which of these scenarios is most consistent with our observed data. We find that the Central Valley populations harbour unique genetic variation coupled with a history of admixture between two well‐differentiated species of woodrats that are currently restricted to the woodlands flanking the Valley. Our simulations also show that certain commonly used analytical approaches may fail to recover a history of admixture when populations experience severe bottlenecks subsequent to hybridization. Overall our study shows the strength of combining empirical and simulation analyses to recover the history of populations occupying highly altered landscapes.     

A strong genetic footprint of the re‐introduction history of Alpine ibex (Capra ibex ibex)

A population’s neutral genetic variation is a composite of its size, degree of isolation and demographic history. Bottlenecks and founder events increase genetic drift, leading to the loss of genetic variation and increased genetic differentiation among populations. Gene flow has the opposite effects. Thus, gene flow can override the genetic patterns caused by founder events. Using 37 microsatellite loci, we investigated the effects of serial bottlenecks on genetic variation and differentiation among 42 Alpine ibex populations in Switzerland with known re‐introduction histories. We detected a strong footprint of re‐introduction events on contemporary genetic structure, with re‐introduction history explaining a substantial part of the genetic differentiation among populations. As a result of the translocation of a considerable number of individuals from the sole formerly surviving population in northern Italy, most of the genetic variation of the ancestral population is now present in the combined re‐introduced Swiss populations. However, re‐introductions split up the genetic variation among populations, such that each contemporary Swiss population showed lower genetic variation than the ancestral population. As expected, serial bottlenecks had different effects on the expected heterozygosity (He) and standardized number of alleles (sNa). While loss of sNa was higher in the first bottlenecks than in subsequent ones, He declined to a similar degree with each bottleneck. Thus, genetic drift was detected with each bottleneck, even when no loss of sNa was observed. Overall, more than a hundred years after the beginning of this successful re‐introduction programme, re‐introduction history was the main determinant of today’s genetic structure.     

MHC variation reflects the bottleneck histories of New Zealand passerines

Most empirical evidence suggests that balancing selection does not counter the effects of genetic drift in shaping postbottleneck major histocompatibility complex (MHC) genetic diversity when population declines are severe or prolonged. However, few studies have been able to include data from historical specimens, or to compare populations/species with different bottleneck histories. In this study, we examined MHC class II B and microsatellite diversity in four New Zealand passerine (songbird) species that experienced moderate to very severe declines. We compared diversity from historical samples (collected c. 1884–1938) to present‐day populations. Using a Bayesian framework, we found that the change in genetic diversity from historical to contemporary samples was affected by three main factors: (i) whether the data were based on MHC or microsatellite markers, (ii) species (as a surrogate for bottleneck severity) and (iii) whether the comparison between historical and contemporary samples was made using historical samples originating from the mainland, or using historical samples originating from islands. The greatest losses in genetic diversity occurred for the most severely bottlenecked species, particularly between historical mainland and contemporary samples. Additionally, where loss of diversity occurred, the change was greater for MHC genes compared to microsatellite loci.     

Stocking activities for the Arctic charr in Lake Geneva: Genetic effects in space and time

Artificial stocking practices are widely used by resource managers worldwide, in order to sustain fish populations exploited by both recreational and commercial activities, but their benefits are controversial. Former practices involved exotic strains, although current programs rather consider artificial breeding of local fishes (supportive breeding). Understanding the complex genetic effects of these management strategies is an important challenge with economic and conservation implications, especially in the context of population declines. In this study, we focus on the declining Arctic charr (Salvelinus alpinus) population from Lake Geneva (Switzerland and France), which has initially been restocked with allochtonous fishes in the early eighties, followed by supportive breeding. In this context, we conducted a genetic survey to document the evolution of the genetic diversity and structure throughout the last 50 years, before and after the initiation of hatchery supplementation, using contemporary and historical samples. We show that the introduction of exotic fishes was associated with a genetic bottleneck in the 1980–1990s, a break of Hardy–Weinberg Equilibrium (HWE), a reduction in genetic diversity, an increase in genetic structure among spawning sites, and a change in their genetic composition. Together with better environmental conditions, three decades of subsequent supportive breeding using local fishes allowed to re‐establish HWE and the initial levels of genetic variation. However, current spawning sites have not fully recovered their original genetic composition and were extensively homogenized across the lake. Our study demonstrates the drastic genetic consequences of different restocking tactics in a comprehensive spatiotemporal framework and suggests that genetic alteration by nonlocal stocking may be partly reversible through supportive breeding. We recommend that conservation‐based programs consider local diversity and implement adequate protocols to limit the genetic homogenization of this Arctic charr population.     

Genetic diagnosis of a rare myrmecochorous species,Plagiorhegma dubium (Berberidaceae): Historical genetic bottlenecks and strong spatial structures among populations

Distribution of genetic variation over time and space is relevant to demographic histories and tightly linked to ecological disturbances as well as evolutionary potential of an organism. Therefore, understanding the pattern of genetic diversity is a primary step in conservation and management projects for rare and threatened plant species. We used eight microsatellite markers to examine the level of genetic diversity, spatial structure, and demographic history of Plagiorhegma dubium, a rare myrmecochorous herb, populations sampled across northeast Asia and Siberia. We found low within‐population genetic variation associated with historical bottlenecks. Although pairwise F_ST values were not much higher than the ones found in similar life form species, STRUCTURE and PCoA revealed a clear broadscale spatial pattern of genetic structure. Bayesian clustering (best K = 6) and PCoA identified three populations that are distinctive from neighboring populations in the Korean peninsula, which suggests potential units for conservation and management plans in Korea. MIGRATE‐N and BAYESASS showed that both contemporary (0.003–0.045) and historical migration rates (2 × e^?5?4.6 × e^?4) were low. Our findings provide a good example, where genetic considerations should be integrated for conservation and management plans of rare and threatened species.     

Genetic signature of a range expansion and leap‐frog event after the recent invasion of Europe by the grapevine downy mildew pathogen Plasmopara viticola

Biologic invasions can have important ecological, economic and social consequences, particularly when they involve the introduction and spread of plant invasive pathogens, as they can threaten natural ecosystems and jeopardize the production of human food. Examples include the grapevine downy mildew, caused by the oomycete Plasmopara viticola, an invasive species native to North America, introduced into Europe in the 1870s. We investigated the introduction and spread of this invasive pathogen, by analysing its genetic structure and diversity in a large sample from European vineyards. Populations of P. viticola across Europe displayed little genetic diversity, consistent with the occurrence of a bottleneck at the time of introduction. Bayesian coalescent analyses revealed a clear population expansion signal in the genetic data. We detected a weak, but significant, continental‐wide population structure, with two geographically and genetically distinct clusters in Western and Eastern European vineyards. Approximate Bayesian computation, analyses of clines of genetic diversity and of isolation‐by‐distance patterns provided evidence for a wave of colonization moving in an easterly direction across Europe. This is consistent with historical reports, first mentioning the introduction of the disease in Bordeaux vineyards (France) and sub‐sequently documenting its rapid spread across Europe. This initial introduction in the west was probably followed by a ‘leap‐frog’ event into Eastern Europe, leading to the formation of the two genetic clusters we detected. This study shows that recent population genetics methods within the Bayesian and coalescence frameworks are extremely powerful for increasing our understanding of pathogen population dynamics and invasion histories.     

Genomic signatures of population bottleneck and recovery in Northwest Atlantic pinnipeds

Population increases over the past several decades provide natural settings in which to study the evolutionary processes that occur during bottleneck, growth, and spatial expansion. We used parallel natural experiments of historical decline and subsequent recovery in two sympatric pinniped species in the Northwest Atlantic, the gray seal (Halichoerus grypus atlantica) and harbor seal (Phoca vitulina vitulina), to study the impact of recent demographic change in genomic diversity. Using restriction site‐associated DNA sequencing, we assessed genomic diversity at over 8,700 polymorphic gray seal loci and 3,700 polymorphic harbor seal loci in samples from multiple cohorts collected throughout recovery over the past half‐century. Despite significant differences in the degree of genetic diversity assessed in the two species, we found signatures of historical bottlenecks in the contemporary genomes of both gray and harbor seals. We evaluated temporal trends in diversity across cohorts, as well as compared samples from sites at both the center and edge of a recent gray seal range expansion, but found no significant change in genomewide diversity following recovery. We did, however, find that the variance and degree of allele frequency change measured over the past several decades were significantly different from neutral expectations of drift under population growth. These two cases of well‐described demographic history provide opportunities for critical evaluation of current approaches to simulating and understanding the genetic effects of historical demographic change in natural populations.     

Spatial and temporal genetic dynamics of the grasshopper Oedaleus decorus revealed by museum genomics

Analyzing genetic variation through time and space is important to identify key evolutionary and ecological processes in populations. However, using contemporary genetic data to infer the dynamics of genetic diversity may be at risk of a bias, as inferences are performed from a set of extant populations, setting aside unavailable, rare, or now extinct lineages. Here, we took advantage of new developments in next‐generation sequencing to analyze the spatial and temporal genetic dynamics of the grasshopper Oedaleus decorus, a steppic Southwestern‐Palearctic species. We applied a recently developed hybridization capture (hyRAD) protocol that allows retrieving orthologous sequences even from degraded DNA characteristic of museum specimens. We identified single nucleotide polymorphisms in 68 historical and 51 modern samples in order to (i) unravel the spatial genetic structure across part of the species distribution and (ii) assess the loss of genetic diversity over the past century in Swiss populations. Our results revealed (i) the presence of three potential glacial refugia spread across the European continent and converging spatially in the Alpine area. In addition, and despite a limited population sample size, our results indicate (ii) a loss of allelic richness in contemporary Swiss populations compared to historical populations, whereas levels of expected heterozygosities were not significantly different. This observation is compatible with an increase in the bottleneck magnitude experienced by central European populations of O. decorus following human‐mediated land‐use change impacting steppic habitats. Our results confirm that application of hyRAD to museum samples produces valuable information to study genetic processes across time and space.     

Evidence of population bottleneck in Astragalus michauxii (Fabaceae), a narrow endemic of the southeastern United States

Genetic factors such as decreased genetic diversity and increased homozygosity can have detrimental effects on rare species, and may ultimately limit potential adaptation and exacerbate population declines. The Gulf and Atlantic Coastal Plain physiographic region has the second highest level of endemism in the continental USA, but habitat fragmentation and land use changes have resulted in catastrophic population declines for many species. Astragalus michauxii (Fabaceae) is an herbaceous plant endemic to the region that is considered vulnerable to extinction, with populations generally consisting of fewer than 20 individuals. We developed eight polymorphic microsatellites and genotyped 355 individuals from 24 populations. We characterized the population genetic diversity and structure, tested for evidence of past bottlenecks, and identified evidence of contemporary gene flow between populations. The mean ratios of the number of alleles to the allelic range (M ratio) across loci for A. michauxii populations were well below the threshold of 0.68 identified as indicative of a past genetic bottleneck. Genetic diversity estimates were similar across regions and populations, and comparable to other long-lived perennial species. Within-population genetic variation accounted for 92 % of the total genetic variation found in the species. Finally, there is evidence for contemporary gene flow among the populations in North Carolina. Although genetic factors can threaten rare species, maintaining habitats through prescribed burning, in concert with other interventions such as population augmentation or (re)introduction, are likely most critical to the long term survival of A. michauxii.     

Genetic Effects of a Persistent Bottleneck on a Natural Population of Ornate Box Turtles (Terrapene ornata)

Human activities in the past few hundred years have caused enormous impacts on many ecosystems, greatly accelerating the rate of population decline and extinction. In addition to habitat alteration and destruction, the loss of genetic diversity due to reduced population size has become a major conservation issue for many imperiled species. However, the genetic effects of persistent population bottlenecks can be very different for long-lived and short-lived species when considering the time scale of centuries. To investigate the genetic effects of persistent population bottlenecks on long-lived species, we use microsatellite markers to assess the level of genetic diversity of a small ornate box turtle population that has experienced a persistent bottleneck in the past century, and compare it to a large relatively undisturbed population. The genetic signature of a recent bottleneck is detected by examining the deviation from mutation-drift equilibrium in the small population, but the bottleneck had little effect on its level of genetic diversity. Computer simulations combined with information on population structure suggest that an effective population size of 300, which results in a census population size of 700, would be required for the small population to maintain 90% of the average number of alleles per locus in the next 200 years. The life history of long-lived species could mask the accelerated rate of genetic drift, making population recovery a relatively slow process. Statistical analysis of genetic data and empirical-based computer simulations can be important tools to facilitate conservation planning.     

Conservation genetics of two critically endangered island dwarf carnivores

Genetic diversity is crucial for conservation biology and for understanding evolutionary processes. Oceanic islands harbor a unique biota and high endemism, with populations frequently facing detrimental genetic processes (e.g. drift, bottlenecks). Human activities like habitat transformation further increase extinction risk of insular biota. Mammals comprise the most endangered group among insular fauna. Our aim was to evaluate the genetic and evolutionary patterns of two critically endangered dwarf carnivores from Cozumel Island, the pygmy raccoon (Procyon pygmaeus) and the dwarf coati (Nasua nelsoni), at both historical and contemporary evolutionary scales. We also reviewed their genetic relationships with their mainland counterparts (P. lotor, N. narica), not intended to describe their phylogeny but to ascertain their endemism. Our mitochondrial results support that both Cozumel carnivores are divergent from continental populations, strengthening their endemic status. Both species showed moderate levels of nuclear genetic diversity that were, as expected for island populations, lower in comparison with their mainland congeneric species; they also exhibited significantly low population sizes. We documented historical and contemporary bottleneck signals for P. pygmaeus, whereas N. nelsoni may be suffering the initial stages of a bottleneck not yet fully manifested. The pygmy raccoon is structured into two isolated genetic clusters likely due to interactions with humans on the north of the island, where most potential for disease transmission and health problems exist. We also add evidence about the introduction of the mainland species into the island, risking genetic introgression and hybridization. We discuss specific conservation measures that should include our genetic information, directed to the long-term viability of these endemic carnivores.

     

Using pre- and postexploitation samples to assess the impact of commercial whaling on the genetic characteristics of eastern North Pacific gray and humpback whales and to compare methods used to infer historic demography

Many species of whales went through recent bottlenecks due to commercial whaling. These declines were rapid and recent relative to the life spans and generation times of these species, raising questions regarding to what degree commercial whaling influenced the genetic characteristics of these populations. We analyzed mitochondrial and nuclear DNA from pre- and postwhaling samples from two populations that have arguably shown the greatest degree of recovery: eastern North Pacific gray and humpback whales. We also compare the performance of different methods to test for historic bottlenecks and infer past demography based on genetic data. We found substantially higher levels of genetic diversity in gray than in humpback whales (for both time periods), likely due to recent connectivity between Atlantic and Pacific gray whale populations. Other than mitochondrial diversity in humpback whales, levels of diversity were not lower in contemporary samples relative to prewhaling samples, indicating that commercial whaling had a minimal impact on metrics of genetic diversity themselves. However, it did have large impacts on the patterns of diversity, as evidenced by all coalescent-based methods showing clear evidence of a bottleneck for both populations, whereas all but one method not based on the coalescent failed to detect a bottleneck.     

Colonization from divergent ancestors: glaciation signatures on contemporary patterns of genomic variation in Collared Pikas (Ochotona collaris)

Identifying the genetic structure of a species and the factors that drive it is an important first step in modern population management, in part because populations evolving from separate ancestral sources may possess potentially different characteristics. This is especially true for climate‐sensitive species such as pikas, where the delimitation of distinct genetic units and the characterization of population responses to contemporary and historical environmental pressures are of particular interest. We combined a restriction site‐associated DNA sequencing (RADSeq) data set containing 4156 single nucleotide polymorphisms with ecological niche models (ENMs) of present and past habitat suitability to characterize population composition and evaluate the effects of historical range shifts, contemporary climates and landscape factors on gene flow in Collared Pikas, which are found in Alaska and adjacent regions of northwestern Canada and are the lesser‐studied of North America's two pika species. The results suggest that contemporary environmental factors contribute little to current population connectivity. Instead, genetic diversity is strongly shaped by the presence of three ancestral lineages isolated during the Pleistocene (~148 and 52 kya). Based on ENMs and genetic data, populations originating from a northern refugium experienced longer‐term stability, whereas both southern lineages underwent population expansion – contradicting the southern stability and northern expansion patterns seen in many other taxa. Current populations are comparable with respect to generally low diversity within populations and little‐to‐no recent admixture. The predominance of divergent histories structuring populations implies that if we are to understand and manage pika populations, we must specifically assess and accurately account for the forces underlying genetic similarity.     

Experimental evaluation of the usefulness of microsatellite DNA for detecting demographic bottlenecks

Evolutionary and conservation biologists often use molecular markers to evaluate whether populations have experienced demographic bottlenecks that resulted in a loss of genetic variation. We evaluated the utility of microsatellites for detection of recent, severe bottlenecks and compared the amounts of genetic diversity lost in bottlenecks of different sizes. In experimental mesocosms, we established replicate populations by releasing 1, 2, 4 or 8 pairs of the western mosquitofish, Gambusia affinis (Poeciliidae). Using eight polymorphic microsatellite loci, we quantified seven indices of genetic diversity or change that have been used to assess the effects of demographic bottlenecks on populations. We compared indices for the experimentally bottlenecked populations to those for the source population and examined differences between populations established with different numbers of founders. Direct count heterozygosity and the proportion of polymorphic loci were not very sensitive to genetic changes that resulted from the experimental bottlenecks. Heterozygosity excess and expected heterozygosity were useful to varying degrees in the detection of bottlenecks. Allelic diversity and temporal variance in allele frequencies were most sensitive to genetic changes that resulted from the bottlenecks, and the temporal variance method was slightly more correlated with bottleneck size than was allelic diversity. Based on comparisons to a previous study with allozymes, heterozygosity, temporal variance in allele frequencies and allelic diversity, but not proportion of polymorphic loci, appear to be more sensitive to demographic bottlenecks when quantified using microsatellites. We found that analysis of eight highly polymorphic loci was sufficient to detect a recent demographic bottleneck and to obtain an estimate of the magnitude of bottleneck severity.     

Consequences of a demographic bottleneck on genetic structure and variation in the Scandinavian brown bear

The Scandinavian brown bear went through a major decline in population size approximately 100 years ago, due to intense hunting. After being protected, the population subsequently recovered and today numbers in the thousands. The genetic diversity in the contemporary population has been investigated in considerable detail, and it has been shown that the population consists of several subpopulations that display relatively high levels of genetic variation. However, previous studies have been unable to resolve the degree to which the demographic bottleneck impacted the contemporary genetic structure and diversity. In this study, we used mitochondrial and microsatellite DNA markers from pre‐ and postbottleneck Scandinavian brown bear samples to investigate the effect of the bottleneck. Simulation and multivariate analysis suggested the same genetic structure for the historical and modern samples, which are clustered into three subpopulations in southern, central and northern Scandinavia. However, the southern subpopulation appears to have gone through a marked change in allele frequencies. When comparing the mitochondrial DNA diversity in the whole population, we found a major decline in haplotype numbers across the bottleneck. However, the loss of autosomal genetic diversity was less pronounced, although a significant decline in allelic richness was observed in the southern subpopulation. Approximate Bayesian computations provided clear support for a decline in effective population size during the bottleneck, in both the southern and northern subpopulations. These results have implications for the future management of the Scandinavian brown bear because they indicate a recent loss in genetic diversity and also that the current genetic structure may have been caused by historical ecological processes rather than recent anthropogenic persecution.     

bottlesim: a bottleneck simulation program for long‐lived species with overlapping generations

Population bottlenecks reduce genetic diversity and thus cause great concern in conservation biology. Previous theoretical studies often assume discrete generations in projecting declines in genetic diversity caused by bottlenecks. This assumption creates complexities when applying the models to long‐lived species with overlapping generations. bottlesim is a program for simulating bottlenecks to estimate the impact on genetic diversity; the novelties include an overlapping‐generation model, a wide range of reproductive systems, and flexible population size settings. With these features, bottlesim will be a useful tool for estimating the genetic consequences of bottlenecks, evaluating conservation plans, and performing power analysis.     

Conservation genomics in the fight to help the recovery of the critically endangered Siamese crocodile Crocodylus siamensis

Endangered species are often characterized by low genetic diversity and it is imperative for conservation efforts to incorporate the knowledge obtained from genetic studies for effective management. However, despite the promise of technological advances in sequencing, application of genome‐wide data to endangered populations remains uncommon. In the present study we pursued a holistic conservation‐genomic approach to inform a field‐based management programme of a Critically Endangered species, the Siamese crocodile Crocodylus siamensis. Using thousands of single nucleotide polymorphisms from throughout the genome, we revealed signals of introgression from two other crocodile species within our sample of both wild and captive‐bred Siamese crocodiles from Cambodia. Our genetic screening of the Siamese crocodiles resulted in the subsequent re‐introduction of 12 individuals into the wild as well as the selection of four individuals for captive breeding programmes. Comparison of intraspecific genetic diversity revealed an alarmingly low contemporary effective population size in the wild (<50) with evidence of a recent bottleneck around Tonle Sap Lake. We also projected a probable future extinction in the wild (within fewer than five generations) in this population in the absence of re‐introduction efforts. However, an increase in the number of potential breeders through re‐introductions, including the one resulting from this project, could counter this trend. Our results have been implemented in ongoing re‐introduction and captive breeding programmes, with major implications for the conservation management of Siamese crocodiles, and provide a blueprint for the rescue effort of other “terminally ill” populations of critically endangered species.     

Landscape genetics in a changing world: disentangling historical and contemporary influences and inferring change

Landscape genetics seeks to determine the effect of landscape features on gene flow and genetic structure. Often, such analyses are intended to inform conservation and management. However, depending on the many factors that influence the time to reach equilibrium, genetic structure may more strongly represent past rather than contemporary landscapes. This well‐known lag between current demographic processes and population genetic structure often makes it challenging to interpret how contemporary landscapes and anthropogenic activity shape gene flow. Here, we review the theoretical framework for factors that influence time lags, summarize approaches to address this temporal disconnect in landscape genetic studies, and evaluate ways to make inferences about landscape change and its effects on species using genetic data alone or in combination with other data. Those approaches include comparing correlation of genetic structure with historical versus contemporary landscapes, using molecular markers with different rates of evolution, contrasting metrics of genetic structure and gene flow that reflect population genetic processes operating at different temporal scales, comparing historical and contemporary samples, combining genetic data with contemporary estimates of species distribution or movement, and controlling for phylogeographic history. We recommend using simulated data sets to explore time lags in genetic structure, and argue that time lags should be explicitly considered both when designing and interpreting landscape genetic studies. We conclude that the time lag problem can be exploited to strengthen inferences about recent landscape changes and to establish conservation baselines, particularly when genetic data are combined with other data.     

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.     

Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline

Most of the white-tailed eagle (Haliaeetus albicilla) populations in Europe experienced dramatic declines during the twentieth century. However, owing to intense conservation actions and the ban of DDT and other persistent pollutants, populations are currently recovering. We show that despite passing through demographic bottlenecks, white-tailed eagle populations have retained significant levels of genetic diversity. Both genetic and ringing data indicate that migration between populations has not been a major factor for the maintenance of genetic variability. We argue that the long generation time of eagles has acted as an intrinsic buffer against loss of genetic diversity, leading to a shorter effective time of the experienced bottleneck. Notably, conservation actions taken in several small sub-populations have ensured the preservation of a larger proportion of the total genetic diversity than if conservation had focused on the population stronghold in Norway. For conservation programmes targeting other endangered, long-lived species, our results highlight the possibility for local retention of high genetic diversity in isolated remnant populations.