Evidence of rapid change in genetic structure and diversity during range expansion in a recovering large terrestrial carnivore

Recovery of natural populations occurs often with simultaneous or subsequent range expansions. According to population genetic theory, genetic structuring emerges at the expansion front together with decreasing genetic diversity, owing to multiple founder events. Thereupon, as the expansion proceeds and connectivity among populations is established, homogenization and a resurgence of genetic diversity are to be expected. Few studies have used a fine temporal scale combined with genetic sampling to track range expansions as they proceed in wild animal populations. As a natural experiment, the historical eradication of large terrestrial carnivores followed by their recovery and recolonization may facilitate empirical tests of these ideas. Here, using brown bear (Ursus arctos) as model species, we tested predictions from genetic theory of range expansion. Individuals from all over Finland were genotyped for every year between 1996 and 2010 using 12 validated autosomal microsatellite markers. A latitudinal shift of about 110 km was observed in the distribution and delineation of genetic clusters during this period. As the range expansion proceeded, we found, as theory predicts, that the degree of genetic structure decreased, and that both genetic variation and admixture increased. The genetic consequences of range expansions may first be detected after multiple generations, but we found major changes in genetic composition after just 1.5 generations, accompanied by population growth and increased migration. These rapid genetic changes suggest an ongoing concerted action of geographical and demographic expansion combined with substantial immigration of bears from Russia during the recovery of brown bears within the large ecosystem of northern Europe.     

Maintenance of high levels of allelic variation in spite of a severe bottleneck in population size: the brown bear (Ursus arctos) in the Western Carpathians

Genetic variation in an isolated brown bear population of the Western Carpathians was studied by electrophoretic analysis of 51 presumptive allozyme loci. In spite of a severe population bottleneck at the beginning of the 1930s (40 survivors), average heterozygosity (H=5.3%) was within the range commonly found in mammals and the mean number of alleles per polymorphic locus (A_p=3, over five polymorphic loci) was very high. Possible reasons for the maintenance of high allelic variation are discussed.     

Rapid range expansion increases genetic differentiation while causing limited reduction in genetic diversity in a damselfly

Many ectothermic species are currently expanding their geographic range due to global warming. This can modify the population genetic diversity and structure of these species because of genetic drift during the colonization of new areas. Although the genetic signatures of historical range expansions have been investigated in an array of species, the genetic consequences of natural, contemporary range expansions have received little attention, with the only studies available focusing on range expansions along a narrow front. We investigate the genetic consequences of a natural range expansion in the Mediterranean damselfly Coenagrion scitulum, which is currently rapidly expanding along a broad front in different directions. We assessed genetic diversity and genetic structure using 12 microsatellite markers in five centrally located populations and five recently established populations at the edge of the geographic distribution. Our results suggest that, although a marginal significant decrease in the allelic richness was found in the edge populations, genetic diversity has been preserved during the range expansion of this species. Nevertheless, edge populations were genetically more differentiated compared with core populations, suggesting genetic drift during the range expansion. The smaller effective population sizes of the edge populations compared with central populations also suggest a contribution of genetic drift after colonization. We argue and document that range expansion along multiple axes of a broad expansion front generates little reduction in genetic diversity, yet stronger differentiation of the edge populations.     

Conservation implications of the mating system of the Pampa Hermosa landrace of peach palm analyzed with microsatellite markers

Peach palm (Bactris gasipaes) is cultivated by many indigenous and traditional communities from Amazonia to Central America for its edible fruits, and is currently important for its heart-of-palm. The objective of this study was to investigate the mating system of peach palm, as this is important for conservation and breeding. Eight microsatellite loci were used to genotype 24 open-pollinated progenies from three populations of the Pampa Hermosa landrace maintained in a progeny trial for genetic improvement. Both the multi-locus outcrossing rates (0.95 to 0.99) and the progeny level multi-locus outcrossing rates (0.9 to 1.0) were high, indicating that peach palm is predominantly allogamous. The outcrossing rates among relatives were significantly different from zero (0.101 to 0.202), providing evidence for considerable biparental inbreeding within populations, probably due to farmers planting seeds of a small number of open-pollinated progenies in the same plot. The correlations of paternity estimates were low (0.051 to 0.112), suggesting a large number of pollen sources (9 to 20) participating in pollination of individual fruit bunches. Effective population size estimates suggest that current germplasm collections are insufficient for long-term ex situ conservation. As with most underutilized crops, on farm conservation is the most important component of an integrated conservation strategy.     

Genomic sweep and potential genetic rescue during limiting environmental conditions in an isolated wolf population

Genetic rescue, in which the introduction of one or more unrelated individuals into an inbred population results in the reduction of detrimental genetic effects and an increase in one or more vital rates, is a potentially important management tool for mitigating adverse effects of inbreeding. We used molecular techniques to document the consequences of a male wolf (Canis lupus) that immigrated, on its own, across Lake Superior ice to the small, inbred wolf population in Isle Royale National Park. The immigrant's fitness so exceeded that of native wolves that within 2.5 generations, he was related to every individual in the population and his ancestry constituted 56 per cent of the population, resulting in a selective sweep of the total genome. In other words, all the male ancestry (50% of the total ancestry) descended from this immigrant, plus 6 per cent owing to the success of some of his inbred offspring. The immigration event occurred in an environment where space was limiting (i.e. packs occupied all available territories) and during a time when environmental conditions had deteriorated (i.e. wolves' prey declined). These conditions probably explain why the immigration event did not obviously improve the population's demography (e.g. increased population numbers or growth rate). Our results show that the beneficial effects of gene flow may be substantial and quickly manifest, short-lived under some circumstances, and how the demographic benefits of genetic rescue might be masked by environmental conditions.     

Short-term genetic changes: evaluating effective population size estimates in a comprehensively described brown trout (Salmo trutta) population

The effective population size (N(e)) is notoriously difficult to accurately estimate in wild populations as it is influenced by a number of parameters that are difficult to delineate in natural systems. The different methods that are used to estimate N(e) are affected variously by different processes at the population level, such as the life-history characteristics of the organism, gene flow, and population substructure, as well as by the frequency patterns of genetic markers used and the sampling design. Here, we compare N(e) estimates obtained by different genetic methods and from demographic data and elucidate how the estimates are affected by various factors in an exhaustively sampled and comprehensively described natural brown trout (Salmo trutta) system. In general, the methods yielded rather congruent estimates, and we ascribe that to the adequate genotyping and exhaustive sampling. Effects of violating the assumptions of the different methods were nevertheless apparent. In accordance with theoretical studies, skewed allele frequencies would underestimate temporal allele frequency changes and thereby upwardly bias N(e) if not accounted for. Overlapping generations and iteroparity would also upwardly bias N(e) when applied to temporal samples taken over short time spans. Gene flow from a genetically not very dissimilar source population decreases temporal allele frequency changes and thereby acts to increase estimates of N(e). Our study reiterates the importance of adequate sampling, quantification of life-history parameters and gene flow, and incorporating these data into the N(e) estimation.     

Developing a common bean core collection suitable for association mapping studies

Because of the continuous introduction of germplasm from abroad, some collections have a high number of accessions, making it difficult to explore the genetic variability present in a germplasm bank for conservation and breeding purposes. Therefore, the aim of this study was to quantify and analyze the structure of genetic variability among 500 common bean accessions to construct a core collection. A total of 58 SSRs were used for this purpose. The polymorphism information content (PIC) in the 180 common bean accessions selected to compose the core collection ranged from 0.17 to 0.86, and the discriminatory power (DP) ranged from 0.21 to 0.90. The 500 accessions were clustered into 15 distinct groups and the 180 accessions into four distinct groups in the Structure analysis. According to analysis of molecular variance, the most divergent accessions comprised 97.2% of the observed genetic variability present within the base collection, confirming the efficiency of the selection criterion. The 180 selected accessions will be used for association mapping in future studies and could be potentially used by breeders to direct new crosses and generate elite cultivars that meet current and future global market needs.     

Linking extinction-colonization dynamics to genetic structure in a salamander metapopulation

Theory predicts that founder effects have a primary role in determining metapopulation genetic structure. However, ecological factors that affect extinction-colonization dynamics may also create spatial variation in the strength of genetic drift and migration. We tested the hypothesis that ecological factors underlying extinction-colonization dynamics influenced the genetic structure of a tiger salamander (Ambystoma tigrinum) metapopulation. We used empirical data on metapopulation dynamics to make a priori predictions about the effects of population age and ecological factors on genetic diversity and divergence among 41 populations. Metapopulation dynamics of A. tigrinum depended on wetland area, connectivity and presence of predatory fish. We found that newly colonized populations were more genetically differentiated than established populations, suggesting that founder effects influenced genetic structure. However, ecological drivers of metapopulation dynamics were more important than age in predicting genetic structure. Consistent with demographic predictions from metapopulation theory, genetic diversity and divergence depended on wetland area and connectivity. Divergence was greatest in small, isolated wetlands where genetic diversity was low. Our results show that ecological factors underlying metapopulation dynamics can be key determinants of spatial genetic structure, and that habitat area and isolation may mediate the contributions of drift and migration to divergence and evolution in local populations.     

Phylogeographic and population genetic analyses reveal Pleistocene isolation followed by high gene flow in a wide ranging,but endangered,freshwater mussel

Freshwater organisms of North America have had their contemporary genetic structure shaped by vicariant events, especially Pleistocene glaciations. Life history traits promoting dispersal and gene flow continue to shape population genetic structure. Cumberlandia monodonta, a widespread but imperiled (IUCN listed as endangered) freshwater mussel, was examined to determine genetic diversity and population genetic structure throughout its range. Mitochondrial DNA sequences and microsatellite loci were used to measure genetic diversity and simulate demographic events during the Pleistocene using approximate Bayesian computation (ABC) to test explicit hypotheses explaining the evolutionary history of current populations. A phylogeny and molecular clock suggested past isolation created two mtDNA lineages during the Pleistocene that are now widespread. Two distinct groups were also detected with microsatellites. ABC simulations indicated the presence of two glacial refugia and post-glacial admixture of them followed by simultaneous dispersal throughout the current range of the species. The Ouachita population is distinct from others and has the lowest genetic diversity, indicating that this is a peripheral population of the species. Gene flow within this species has maintained high levels of genetic diversity in most populations; however, all populations have experienced fragmentation. Extirpation from the center of its range likely has isolated remaining populations due to the geographic distances among them.     

Antimicrobial susceptibility patterns,emm type distribution and genetic diversity of Streptococcus pyogenes recovered in Brazil

Streptococcus pyogenes is responsible for a variety of infectious diseases and immunological complications. In this study, 91 isolates of S. pyogenes recovered from oropharynx secretions were submitted to antimicrobial susceptibility testing, emm typing and pulsed-field gel electrophoresis (PFGE) analysis. All isolates were susceptible to ceftriaxone, levofloxacin, penicillin G and vancomycin. Resistance to erythromycin and clindamycin was 15.4%, which is higher than previous reports from this area, while 20.9% of the isolates were not susceptible to tetracycline. The macrolide resistance phenotypes were cMLSB (10) and iMLSB (4). The ermB gene was predominant, followed by the ermA gene. Thirty-two emm types and subtypes were found, but five (emm1, emm4, emm12, emm22, emm81) were detected in 48% of the isolates. Three new emm subtypes were identified (emm1.74, emm58.14, emm76.7). There was a strong association between emm type and PFGE clustering. A variety of PFGE profiles as well as emm types were found among tetracycline and erythromycin-resistant isolates, demonstrating that antimicrobial resistant strains do not result from the expansion of one or a few clones. This study provides epidemiological data that contribute to the development of suitable strategies for the prevention and treatment of such infections in a poorly studied area.     

Maintaining genetic diversity and population panmixia through dispersal and not gene flow in a holocyclic heteroecious aphid species

Heteroecious holocyclic aphids exhibit both sexual and asexual reproduction and alternate among primary and secondary hosts. Most of these aphids can feed on several related hosts, and invasions to new habitats may limit the number of suitable hosts. For example, the aphid specialist Aphis glycines survives only on the primary host buckthorn (Rhamnus spp.) and the secondary host soybean (Glycine max) in North America where it is invasive. Owing to this specialization and sparse primary host distribution, host colonization events could be localized and involve founder effects, impacting genetic diversity, population structure and adaptation. We characterized changes in the genetic diversity and structure across time among A. glycines populations. Populations were sampled from secondary hosts twice in the same geographical location: once after secondary colonization (early season), and again immediately before primary host colonization (late season). We tested for evidence of founder effects and genetic isolation in early season populations, and whether or not late-season dispersal restored genetic diversity and reduced fragmentation. A total of 24 single-nucleotide polymorphisms and 6 microsatellites were used for population genetic statistics. We found significantly lower levels of genotypic diversity and more genetic isolation among early season collections, indicating secondary host colonization occurred locally and involved founder effects. Pairwise F(ST) decreased from 0.046 to 0.017 in early and late collections, respectively, and while genetic relatedness significantly decreased with geographical distance in early season collections, no spatial structure was observed in late-season collections. Thus, late-season dispersal counteracts the secondary host colonization through homogenization and increases genetic diversity before primary host colonization.     

Accounting for cryptic population substructure enhances detection of inbreeding depression with genomic inbreeding coefficients: an example from a critically endangered marsupial

Characterizing inbreeding depression in wildlife populations can be critical to their conservation. Coefficients of individual inbreeding can be estimated from genome‐wide marker data. The degree to which sensitivity of inbreeding coefficients to population genetic substructure alters estimates of inbreeding depression in wild populations is not well understood. Using generalized linear models, we tested the power of two frequently used inbreeding coefficients that are calculated from genome‐wide SNP markers, F_H and F^^III, to predict four fitness traits estimated over two decades in an isolated population of the critically endangered Leadbeater's possum. F_H estimates inbreeding as excess observed homozygotes relative to equilibrium expectations, whereas F^^III quantifies allelic similarity between the gametes that formed an individual, and upweights rare homozygotes. We estimated F_H and F^^III from 1,575 genome‐wide SNP loci in individuals with fitness trait data (N = 179–237 per trait), and computed revised coefficients, F_H^{by group} and F^^{IIIby group}, adjusted for population genetic substructure by calculating them separately within two different genetic groups of individuals identified in the population. Using F_H or F^^III in the models, inbreeding depression was detected for survival to sexual maturity, longevity and whether individuals bred during their lifetime. F^^{IIIby group} (but not F_H^{by group}) additionally revealed significant inbreeding depression for lifetime reproductive output (total offspring assigned to each individual). Estimates of numbers of lethal equivalents indicated substantial inbreeding load, but differing between inbreeding estimators. Inbreeding depression, declining population size, and low and declining genetic diversity suggest that genetic rescue may assist in preventing extinction of this unique Leadbeater's possum population.     

Challenges in the conservation and sustainable use of genetic resources

The meeting on 'Genetic Resources in the Face of New Environmental, Economic and Social Challenges' held in Montpellier (France) from 20-22 September 2011 brought together about 200 participants active in research and management of the genetic diversity of plant, animal, fungal and microbial species. Attendees had the rare opportunity to hear about agronomy, botany, microbiology, mycology, the social sciences and zoology in the same conference. The research teams presented the results of about 50 projects funded by the French Foundation for Research on Biodiversity to preserve genetic diversity carried out in Africa, Asia, Europe and the Americas. These projects aimed to better understand and manage genetic resources in a rapidly changing world (e.g. structural changes in the agricultural industry, the need for climate change mitigation and adaptation, the challenge of achieving food security despite the growing world population and changing dietary habits, the opportunities provided by the many new molecular biology tools, the problems caused by widespread scientific budget cuts). The meeting also hosted some roundtables open to all participants which provided a forum to establish a much needed dialogue between policy-makers, managers and researchers.     

Individual genetic diversity correlates with the size and spatial isolation of natal colonies in a bird metapopulation

The genetic consequences of small population size and isolation are of central concern in both population and conservation biology. Organisms with a metapopulation structure generally show effective population sizes that are much smaller than the number of mature individuals and this can reduce genetic diversity especially in small sized and isolated subpopulations. Here, we examine the association between heterozygosity and the size and spatial isolation of natal colonies in a metapopulation of lesser kestrels (Falco naumanni). For this purpose, we used capture-mark-recapture data to determine the patterns of immigration into the studied colonies, and 11 highly polymorphic microsatellite markers that allowed us to estimate genetic diversity of locally born individuals. We found that individuals born in smaller and more isolated colonies were genetically less diverse. These colonies received a lower number of immigrants, supporting the idea that both reduced gene flow and small population size are responsible for the genetic pattern observed. Our results are particularly intriguing because the lesser kestrel is a vagile and migratory species with great movement capacity and dispersal potential. Overall, this study provides evidence of the association between individual heterozygosity and the size and spatial isolation of natal colonies in a highly mobile vertebrate showing relatively frequent dispersal and low genetic differentiation among local subpopulations.     

Living on a volcano's edge: genetic isolation of an extremophile terrestrial metazoan

Communities of organisms inhabiting extreme terrestrial environments provide a unique opportunity to study evolutionary forces that drive population structure and genetic diversity under the combined challenges posed by multiple geogenic stressors. High abundance of an invasive pantropical earthworm (and the absence of indigenous lumbricid species) in the Furnas geothermal field (Sao Miguel Island, Azores) indicates its remarkable tolerance to high soil temperature, exceptionally high carbon dioxide and low oxygen levels, and elevated metal bioavailability, conditions which are lethal for the majority of terrestrial metazoans. Mitochondrial and nuclear markers were used to analyze the relationship between populations living inside and outside the geothermal field. Results showed that Pontoscolex corethrurus (Annelida, Oligochaeta, Glossoscolecidae) to be a genetically heterogeneous complex within the Sao Miguel landscape and is probably differentiated into cryptic species. The population exposed to the hostile soil conditions within the volcanic caldera possesses the lowest within-population mitochondrial diversity but an unexpectedly high degree of nuclear variability with several loci evidencing positive selection, parameters indicative of a genetically unique population only distantly related to conspecifics living outside the caldera. In conclusion, P. corethrurus inhabiting active volcanic soil is a discrete extremophile population that has evolved by tolerating a mixture of non-anthropogenic chemical and physical stressors.     

Preferred habitat and effective population size drive landscape genetic patterns in an endangered species

Landscape genetics provides a framework for pinpointing environmental features that determine the important exchange of migrants among populations. These studies usually test the significance of environmental variables on gene flow, yet ignore one fundamental driver of genetic variation in small populations, effective population size, N_e. We combined both approaches in evaluating genetic connectivity of a threatened ungulate, woodland caribou. We used least-cost paths to calculate matrices of resistance distance for landscape variables (preferred habitat, anthropogenic features and predation risk) and population-pairwise harmonic means of N_e, and correlated them with genetic distances, F_ST and D_c. Results showed that spatial configuration of preferred habitat and N_e were the two best predictors of genetic relationships. Additionally, controlling for the effect of N_e increased the strength of correlations of environmental variables with genetic distance, highlighting the significant underlying effect of N_e in modulating genetic drift and perceived spatial connectivity. We therefore have provided empirical support to emphasize preventing increased habitat loss and promoting population growth to ensure metapopulation viability.     

Extending glacial refugia for a European tree: genetic markers show that Iberian populations of white elm are native relicts and not introductions

Conservation policies usually focus on in situ protection of native populations, a priority that requires accurate assessment of population status. Distinction between native and introduced status can be particularly difficult (and at the same time, is most important) for species whose natural habitat has become both rare and highly fragmented. Here, we address the status of the white elm (Ulmus laevis Pallas), a European riparian tree species whose populations have been fragmented by human activity and is protected wherever it is considered native. Small populations of this species are located in Iberia, where they are unprotected because they are considered introductions due to their rarity. However, Iberia and neighbouring regions in southwestern France have been shown to support discrete glacial refuge populations of many European trees, and the possibility remains that Iberian white elms are native relicts. We used chloroplast RFLPs and nuclear microsatellites to establish the relationship between populations in Iberia and the Central European core distribution. Bayesian approaches revealed significant spatial structure across populations. Those in Iberia and southwestern France shared alleles absent from Central Europe, and showed spatial population structure within Iberia common in recognized native taxa. Iberian populations show a demographic signature of ancient population bottlenecks, while those in Central European show a signature of recent population bottlenecks. These patterns are not consistent with historical introduction of white elm to Iberia, and instead strongly support native status, arguing for immediate implementation of conservation measures for white elm populations in Spain and contiguous areas of southern France.