RAD-tag and mitochondrial DNA sequencing reveal the genetic structure of a widespread and regionally imperiled freshwater mussel, Obovaria olivaria (Bivalvia: Unionidae).

Obovaria olivaria is a species of freshwater mussel native to the Mississippi River and Laurentian Great Lakes-St. Lawrence River drainages of North America. This mussel has experienced population declines across large parts of its distribution and is imperiled in many jurisdictions. Obovaria olivaria uses the similarly imperiled Acipenser fulvescens (Lake Sturgeon) as a host for its glochidia. We employed mitochondrial DNA sequencing and restriction site-associated DNA sequencing (RAD-seq) to assess patterns of genetic diversity and population structure of O. olivaria from 19 collection locations including the St. Lawrence River drainage, the Great Lakes drainage, the Upper Mississippi River drainage, the Ohioan River drainage, and the Mississippi Embayment. Heterozygosity was highest in Upper Mississippi and Great Lakes populations, followed by a reduction in diversity and relative effective population size in the St. Lawrence populations. Pairwise F ST ranged from 0.00 to 0.20, and analyses of genetic structure revealed two major ancestral populations, one including all St. Lawrence River/Ottawa River sites and the other including remaining sites; however, significant admixture and isolation by river distance across the range were evident. The genetic diversity and structure of O. olivaria is consistent with the existing literature on Acipenser fulvescens and suggests that, although northern and southern O. olivaria populations are genetically distinct, genetic structure in O. olivaria is largely clinal rather than discrete across its range. Conservation and restoration efforts of O. olivaria should prioritize the maintenance and restoration of locations where O. olivaria remain, especially in northern rivers, and to ensure connectivity that will facilitate dispersal of Acipenser fulvescens and movement of encysted glochidia.

Adaptive Introgression Facilitates Adaptation to High Latitudes in European Aspen (Populus tremula L.).

Understanding local adaptation has become a key research area given the ongoing climate challenge and the concomitant requirement to conserve genetic resources. Perennial plants, such as forest trees, are good models to study local adaptation given their wide geographic distribution, largely outcrossing mating systems, and demographic histories. We evaluated signatures of local adaptation in European aspen (Populus tremula) across Europe by means of whole-genome resequencing of a collection of 411 individual trees. We dissected admixture patterns between aspen lineages and observed a strong genomic mosaicism in Scandinavian trees, evidencing different colonization trajectories into the peninsula from Russia, Central and Western Europe. As a consequence of the secondary contacts between populations after the last glacial maximum, we detected an adaptive introgression event in a genome region of ∼500 kb in chromosome 10, harboring a large-effect locus that has previously been shown to contribute to adaptation to the short growing seasons characteristic of Northern Scandinavia. Demographic simulations and ancestry inference suggest an Eastern origin-probably Russian-of the adaptive Nordic allele which nowadays is present in a homozygous state at the north of Scandinavia. The strength of introgression and positive selection signatures in this region is a unique feature in the genome. Furthermore, we detected signals of balancing selection, shared across regional populations, that highlight the importance of standing variation as a primary source of alleles that facilitate local adaptation. Our results, therefore, emphasize the importance of migration-selection balance underlying the genetic architecture of key adaptive quantitative traits.

A dynamic history of admixture from Mediterranean and Carpathian glacial refugia drives genomic diversity in the bank vole.

Understanding the historical contributions of differing glacial refugia is key to evaluating the roles of microevolutionary forces, such as isolation, introgression, and selection in shaping genomic diversity in present-day populations. In Europe, where both Mediterranean and extra-Mediterranean (e.g., Carpathian) refugia of the bank vole (Clethrionomys glareolus) have been identified, mtDNA indicates that extra-Mediterranean refugia were the main source of colonization across the species range, while Mediterranean peninsulas harbor isolated, endemic lineages. Here, we critically evaluate this hypothesis using previously generated genomic data (>6,000 SNPs) for over 800 voles, focusing on genomic contributions to bank voles in central Europe, a key geographic area in considering range-wide colonization. The results provide clear evidence that both extra-Mediterranean (Carpathian) and Mediterranean (Spanish, Calabrian, and Balkan) refugia contributed to the ancestry and genomic diversity of bank vole populations across Europe. Few strong barriers to dispersal and frequent admixture events in central Europe have led to a prominent mid-latitude peak in genomic diversity. Although the genomic contribution of the centrally located Carpathian refugium predominates, populations in different parts of Europe have admixed origins from Mediterranean (28%-47%) and the Carpathian (53%-72%) sources. We suggest that the admixture from Mediterranean refugia may have provisioned adaptive southern alleles to more northern populations, facilitating the end-glacial spread of the admixed populations and contributing to increased bank vole diversity in central Europe. This study adds critical details to the complex end-glacial colonization history of this well-studied organism and underscores the importance of genomic data in phylogeographic interpretation.

Occurrence of apomictic conspecifics and ecological preferences rather than colonization history govern the geographic distribution of sexual Potentilla puberula.

The geographic distribution of sexual-apomictic taxa (i.e., comprising individuals usually reproducing either sexually or asexually via seeds) is traditionally thought to be driven by their ecological preferences and colonization histories. Where sexuals and apomicts get into contact with each other, competitive and reproductive interactions can interfere with these factors, an aspect which hitherto received little attention in biogeographic studies. We disentangled and quantified the relative effects of the three factors on the distribution of tetraploid sexuals in Potentilla puberula in a latitudinal transect through the Eastern European Alps, in which they are codistributed with penta-, hepta-, and octoploid apomictic conspecifics. Effects were explored by means of binomial generalized linear regression models combining a single with a multiple predictor approach. Postglacial colonization history was inferred from population genetic variation (AFLPs and cpDNA) and quantified using a cost distance metric. The study was based on 235 populations, which were purely sexual, purely apomictic, or of mixed reproductive mode. The occurrence of apomicts explained most of the variation in the distribution of sexuals (31%). Specifically, the presence of sexual tetraploids was negatively related to the presence of each of the three apomictic cytotypes. Effects of ecological preferences were substantial too (7% and 12% of the total variation explained by ecological preferences alone, or jointly with apomicts' occurrence, respectively). In contrast, colonization history had negligible effects on the occurrence of sexuals. Taken together, our results highlight the potentially high impact of reproductive interactions on the geographic distribution of sexual and apomictic conspecifics and that resultant mutual exclusion interrelates to ecological differentiation, a situation potentially promoting their local coexistence.

Postglacial colonization history reflects in the genetic structure of natural populations of Festuca rubra in Europe.

We conducted a large-scale population genetic survey of genetic diversity of the host grass Festuca rubra s.l., which fitness can be highly dependent on its symbiotic fungus Epichloë festucae, to evaluate genetic variation and population structure across the European range. The 27 studied populations have previously been found to differ in frequencies of occurrence of the symbiotic fungus E. festucae and ploidy levels. As predicted, we found decreased genetic diversity in previously glaciated areas in comparison with nonglaciated regions and discovered three major maternal genetic groups: southern, northeastern, and northwestern Europe. Interestingly, host populations from Greenland were genetically similar to those from the Faroe Islands and Iceland, suggesting gene flow also between those areas. The level of variation among populations within regions is evidently highly dependent on the postglacial colonization history, in particular on the number of independent long-distance seed colonization events. Yet, also anthropogenic effects may have affected the population structure in F. rubra. We did not observe higher fungal infection rates in grass populations with lower levels of genetic variability. In fact, the fungal infection rates of E. festucae in relation to genetic variability of the host populations varied widely among geographical areas, which indicate differences in population histories due to colonization events and possible costs of systemic fungi in harsh environmental conditions. We found that the plants of different ploidy levels are genetically closely related within geographic areas indicating independent formation of polyploids in different maternal lineages.

Climatic differentiation in polyploid apomictic Ranunculus auricomus complex in Europe.

BACKGROUND: Polyploidy and apomixis are important factors influencing plant distributions often resulting in range shifts, expansions and geographical parthenogenesis. We used the Ranunculus auricomus complex as a model to asses if the past and present distribution and climatic preferences were determined by these phenomena. RESULTS: Ecological differentiation among diploids and polyploids was tested by comparing the sets of climatic variables and distribution modelling using 191 novel ploidy estimations and 561 literature data. Significant differences in relative genome size on the diploid level were recorded between the "auricomus" and "cassubicus" groups and several new diploid occurrences were found in Slovenia and Hungary. The current distribution of diploids overlapped with the modelled paleodistribution (22 kyr BP), except Austria and the Carpathians, which are proposed to be colonized later on from refugia in the Balkans. Current and historical presence of diploids from the R. auricomus complex is suggested also for the foothills of the Caucasus. Based on comparisons of the climatic preferences polyploids from the R. auricomus complex occupy slightly drier and colder habitats than the diploids. CONCLUSIONS: The change of reproductive mode and selection due to competition with the diploid ancestors may have facilitated the establishment of polyploids within the R. auricomus complex in environments slightly cooler and drier, than those tolerated by diploid ancestors. Much broader distribution of polyploid apomicts may have been achieved due to faster colonization mediated by uniparental reproductive system.

Genomics of end-Pleistocene population replacement in a small mammal.

Current species distributions at high latitudes are the product of expansion from glacial refugia into previously uninhabitable areas at the end of the last glaciation. The traditional view of postglacial colonization is that southern populations expanded their ranges into unoccupied northern territories. Recent findings on mitochondrial DNA (mtDNA) of British small mammals have challenged this simple colonization scenario by demonstrating a more complex genetic turnover in Britain during the Pleistocene-Holocene transition where one mtDNA clade of each species was replaced by another mtDNA clade of the same species. Here, we provide evidence from one of those small mammals, the bank vole (Clethrionomys glareolus), that the replacement was genome-wide. Using more than 10 000 autosomal SNPs we found that similar to mtDNA, bank vole genomes in Britain form two (north and south) clusters which admix. Therefore, the genome of the original postglacial colonists (the northern cluster) was probably replaced by another wave of migration from a different continental European population (the southern cluster), and we gained support for this by modelling with approximate Bayesian computation. This finding emphasizes the importance of analysis of genome-wide diversity within species under changing climate in creating opportunities for sophisticated testing of population history scenarios.

Phylogeography of Littorina sitkana in the northwestern Pacific Ocean: evidence of eastward trans-Pacific colonization after the Last Glacial Maximum.

We investigated genetic diversity and population structure of the Sitka periwinkle Littorina sitkana along the coastlines of the northwestern Pacific (NWP) to evaluate the possibility of trans-Pacific colonization of this species from the NWP to the northeastern Pacific (NEP) after the Last Glacial Maximum. We sampled L. sitkana from 32 populations in the NWP, and sequenced a region of the mitochondrial cytochrome b oxidase gene for population genetic analyses. The results were compared with those of previous reports from the NEP. The genetic diversity of L. sitkana was much higher in the NWP than in the NEP. Genetic connectivity between the NWP and NEP populations was indicated by an extremely abundant haplotype in the NEP that was also present in eastern Hokkaido and the Kuril Islands. To confirm these results, we compared sequences of the longest intron of the aminopeptidase N gene (APN54) in the nuclear genome in four populations of L. sitkana in the NWP with previous results from the NEP. Again, much higher genetic diversity was found in the NWP than in the NEP and genetic connectivity was supported between the Kuril Islands and the NEP. These results imply postglacial colonization of this species from the NWP to the NEP, probably along the Kuril and Aleutian Island chains. This study is the first report of possible trans-Pacific postglacial colonization of a direct-developing gastropod, inferred from genetic data.

Contrasting patterns of genetic diversity across the ranges of Pinus monticola and P. strobus: a comparison between eastern and western North American postglacial colonization histories.

UNLABELLED: • Premises of the study: Understanding the influence of recent glacial and postglacial periods on species' distributions is key for predicting the effects of future environmental changes. We investigated the influence of two physiographic landscapes on population structure and postglacial colonization of two white pine species of contrasting habitats: P. monticola, which occurs in the highly mountainous region of western North America, and P. strobus, which occurs in a much less mountainous area in eastern North America.• METHODS: To characterize the patterns of genetic diversity and population structure across the ranges of both species, 158 and 153 single nucleotide polymorphism (SNP) markers derived from expressed genes were genotyped on range-wide samples of 61 P. monticola and 133 P. strobus populations, respectively.• KEY RESULTS: In P. monticola, a steep latitudinal decrease in genetic diversity likely resulted from postglacial colonization involving rare long-distance dispersal (LDD) events. In contrast, no geographic patterns of diversity were detected in P. strobus, suggesting recolonization via a gradually advancing front or frequent LDD events. For each species, structure analyses identified two distinct southern and northern genetic groups that likely originated from two different glacial lineages. At a finer scale, and for the two species, smaller subgroups were detected that could be remnants of cryptic refugia.• CONCLUSION: During postglacial colonization, the western and eastern North American landscapes had different impacts on genetic signatures in P. monticola compared with P. strobus. We discuss the importance of our findings for conservation programs and predictions of species' response to climate change.

New insights on postglacial colonization in western Europe: the phylogeography of the Leisler's bat (Nyctalus leisleri).

Despite recent advances in the understanding of the interplay between a dynamic physical environment and phylogeography in Europe, the origins of contemporary Irish biota remain uncertain. Current thinking is that Ireland was colonized post-glacially from southern European refugia, following the end of the last glacial maximum (LGM), some 20 000 years BP. The Leisler's bat (Nyctalus leisleri), one of the few native Irish mammal species, is widely distributed throughout Europe but, with the exception of Ireland, is generally rare and considered vulnerable. We investigate the origins and phylogeographic relationships of Irish populations in relation to those across Europe, including the closely related species N. azoreum. We use a combination of approaches, including mitochondrial and nuclear DNA markers, in addition to approximate Bayesian computation and palaeo-climatic species distribution modelling. Molecular analyses revealed two distinct and diverse European mitochondrial DNA lineages, which probably diverged in separate glacial refugia. A western lineage, restricted to Ireland, Britain and the Azores, comprises Irish and British N. leisleri and N. azoreum specimens; an eastern lineage is distributed throughout mainland Europe. Palaeo-climatic projections indicate suitable habitats during the LGM, including known glacial refugia, in addition to potential novel cryptic refugia along the western fringe of Europe. These results may be applicable to populations of many species.

Effects of recent and past climatic shifts on the genetic structure of the high mountain yellow-spotted ringlet butterfly Erebia manto (Lepidoptera, Satyrinae): a conservation problem.

Mountain species have evolved important genetic differentiation due to past climatic fluctuations. The genetic uniqueness of many of these lineages is now at risk due to global warming. Here, we analyse allozyme polymorphisms of 1306 individuals (36 populations) of the mountain butterfly Erebia manto and perform Species Distribution Models (SDMs). As a consensus of analyses, we obtained six most likely genetic clusters: (i) Pyrenees with Massif Central; (ii) Vosges; (iii-v) Alps including the Slovakian Carpathians; (vi) southern Carpathians. The Vosges population showed the strongest genetic split from all other populations, being almost as strong as the split between E. manto and its sister species Erebia eriphyle. The distinctiveness of the Pyrenees-Massif Central group and of the southern Carpathians group from all other groups is also quite high. All three groups are assumed to have survived more than one full glacial-interglacial cycle close to their current distributions with up-hill and down-slope shifts conforming climatic conditions. In contrast with these well-differentiated groups, the three groups present in the Alps and the Slovakian Carpathians show a much shallower genetic structure and thus also should be of a more recent origin. As predicted by our SDM projections, rising temperatures will strongly impact the distribution of E. manto. While the populations in the Alps are predicted to shrink, the survival of the three lineages present here should not be at risk. The situation of the three other lineages is quite different. All models predict the extinction of the Vosges lineage in the wake of global warming, and also the southern Carpathians and Pyrenees-Massif Central lineages might be at high risk to disappear. Thus, albeit global warming will therefore be unlikely to threaten E. manto as a species, an important proportion of the species' intraspecific differentiation and thus uniqueness might be lost.

Microsatellite variation and genetic structure of brook trout (Salvelinus fontinalis) populations in Labrador and neighboring Atlantic Canada: evidence for ongoing gene flow and dual routes of post-Wisconsinan colonization.

In conservation genetics and management, it is important to understand the contribution of historical and contemporary processes to geographic patterns of genetic structure in order to characterize and preserve diversity. As part of a 10-year monitoring program by the Government of Newfoundland and Labrador, Canada, we measured the population genetic structure of the world's most northern native populations of brook trout (Salvelinus fontinalis) in Labrador to gather baseline data to facilitate monitoring of future impacts of the recently opened Trans-Labrador Highway. Six-locus microsatellite profiles were obtained from 1130 fish representing 32 populations from six local regions. Genetic diversity in brook trout populations in Labrador (average H(E)= 0.620) is within the spectrum of variability found in other brook trout across their northeastern range, with limited ongoing gene flow occurring between populations (average pairwise F(ST)= 0.139). Evidence for some contribution of historical processes shaping genetic structure was inferred from an isolation-by-distance analysis, while dual routes of post-Wisconsinan recolonization were indicated by STRUCTURE analysis: K= 2 was the most likely number of genetic groups, revealing a separation between northern and west-central Labrador from all remaining populations. Our results represent the first data from the nuclear genome of brook trout in Labrador and emphasize the usefulness of microsatellite data for revealing the extent to which genetic structure is shaped by both historical and contemporary processes.

Multiple ice-age refugia in Pacific cod, Gadus macrocephalus.

Pleistocene ice-ages greatly influenced the historical abundances of Pacific cod, Gadus macrocephalus, in the North Pacific and its marginal seas. We surveyed genetic variation at 11 microsatellite loci and mitochondrial (mt) DNA in samples from twelve locations from the Sea of Japan to Washington State. Both microsatellite (mean H = 0.868) and mtDNA haplotype (mean h = 0.958) diversities were large and did not show any geographical trends. Genetic differentiation between samples was significantly correlated with geographical distance between samples for both microsatellites (FST = 0.028, r(2) = 0.33) and mtDNA (FST = 0.027, r(2) = 0.18). Both marker classes showed a strong genetic discontinuity between northwestern and northeastern Pacific populations that likely represents groups previously isolated during glaciations that are now in secondary contact. Significant differences appeared between samples from the Sea of Japan and Okhotsk Sea that may reflect ice-age isolations in the northwest Pacific. In the northeast Pacific, a microsatellite and mtDNA partition was detected between coastal and Georgia Basin populations. The presence of two major coastal mtDNA lineages on either side of the Pacific Ocean basin implies at least two ice-age refugia and separate postglacial population expansions facilitated by different glacial histories. Northward expansions into the Gulf of Alaska were possible 14-15 kyr ago, but deglaciation and colonization of the Georgia Basin probably occurred somewhat later. Population expansions were evident in mtDNA mismatch distributions and in Bayesian skyline plots of the three major lineages, but the start of expansions appeared to pre-date the last glacial maximum.