Population genetic structure of the endangered crayfish Austropotamobius pallipes in France based on microsatellite variation: biogeographical inferences and conservation implications

1. One important goal in conservation biology is to characterise evolutionary lineages within endangered species before management decisions are taken. Here, we assess population differentiation in the freshwater crayfish Austropotamobius pallipes, an endangered species endemic to western Europe and provide valuable information for the conservation of French populations. 2. Analysis of five microsatellite loci in 44 populations revealed very different within population levels of genetic diversity (0.000 < H₀ < 0.564). Two groups, corresponding to northern and southern French populations, showed a high degree of genetic differentiation in both allele frequencies and allele sizes. Comparison of these results with previous studies of A. pallipes strongly suggests that the divergence between northern and southern populations could have occurred during the last glaciation period of the Pleistocene from one Atlantic and one Mediterranean refuge. 3. Evidence for genetic admixture between these two lineages was revealed by correspondence analyses in southern populations, probably as the result of artificial translocations. 4. French populations appeared significantly differentiated among the different river drainages and were highly structured within rivers. The impact of population size, population bottlenecks and founder events on the population genetic differentiation are discussed. 5. Based on these results, we propose the designation of two evolutionarily significant units for A. pallipes in France. Our data also support the maintenance of separate demographic management strategies for crayfish inhabiting different river systems. However, genetic analyses will have to be combined with demographic and ecological data for sustainable conservation programmes.     

Landscape conservation genetics of <Emphasis Type="Italic">Dipteryx alata</Emphasis> (“baru” tree: Fabaceae) from Cerrado region of central Brazil

In this paper random amplified polymorphic DNA (RAPD) was used to evaluate the degree of among-population differentiation and associated spatial patterns of genetic divergence for Dipteryx alata Vogel populations from Cerrado region of central Brazil, furnishing support for future programs of conservation of this species. We analyzed patterns of genetic and spatial population structure using 45 RAPD loci scored for 309 trees, sampled from five different regions with two populations each. Genetic structure analysis suggested that panmixia null hypothesis can be rejected, with significant among-population components of 15%. Hierarchical partition by Analysis of Molecular Variance (AMOVA) shows that 5% of genetic variation is within regions, whereas 10% of variation is among regions, and these results were confirmed by a Bayesian analyses on HICKORY. The Mantel correlogram revealed that this divergence is spatially structured, so that local populations situated at short geographic distances could not be considered independent units for conservation and management. However, genetic discontinuities among populations were found in the northwest and southeast parts of the study area, corresponding to regions of recent socio-economic expansion and high population density, respectively. Taking both geographic distances and genetic discontinuities into account it is possible to establish a group of population to be conserved, covering most of D. alata geographic distribution and congruent with previously established priority areas for conservation in the Cerrado region.     

Genetic diversity of the endangered endemic Agave victoriae-reginae (Agavaceae) in the Chihuahuan Desert

Long-lived perennials are a species-rich, ecologically important component of the North American deserts, yet we know little about their genetic structure, information important for their conservation. Agave victoriae-reginae is an endemic of the Chihuahuan Desert of northern Mexico that is endangered by collection for the ornamental trade. We examined levels and patterns of variation at ten polymorphic allozyme loci in ten populations representing the range of the species. Levels of genetic variation (mean H_e= 0.335) and differentiation (mean F_ST = 0.236) were high. Phenetic clustering suggested the existence of at least three distinct groups of populations. If this pattern of variation is representative of other long-lived desert perennials, it may explain the species richness of this group and will pose a real challenge to gene conservation efforts.     

Genetic diversity and structure of a Mediterranean endemic plant in Corsica (<Emphasis Type="Italic">Mercurialis corsica</Emphasis>, Euphorbiaceae)

The island of Corsica is a Mediterranean hotspot of plant biodiversity characterized by a high rate of plant endemism, but also by a lack of studies combining genetic diversity and conservation. In Corsica, the dioecious and Corso-Sardinian endemic Mercurialis corsica Cosson (Euphorbiaceae) occurs across a wide ecological gradient, but the number of populations have decreased considerably over the last century. The main aim of this study was to examine the patterns of genetic diversity occurring in the Corsican populations of M. corsica, depending on their location and demographic structure. The rDNA sequences did not show the existence of any polymorphism, whereas the cpDNA sequences revealed the divergence of the western Corsican populations. By contrast, when the AFLP markers were examined, although significant levels of differentiation were detected between populations, no distinct geographical patterns were observed except for the pronounced isolation of the Cap Corse genotypes. No significant correlations were found to exist between population size and the genetic diversity indexes used. The results of this study suggest that M. corsica has undergone a complex gene flow history involving past population admixtures, followed by fragmentation processes resulting in population differentiation but no geographical patterns of isolation. These results support the existence of three evolutive conservation units which have to be monitored in priority to determine whether the current pattern of demographic structure is still declining or has stabilized.     

Evidence of connectivity between continental and differentiated insular populations in a highly mobile species

Aim Genetically differentiated insular populations are candidates for independent units for conservation. However, occasional immigration to reduced island populations may occur and potentially have important consequences in their future viability and evolutionary potential. In this study, we investigate the conservation implications of population structure and connectivity of insular and continental populations of a migratory raptor as determined using genetic tools and satellite tracking. Location Western European populations in the Iberian Peninsula and two insular populations in the Mediterranean Sea (Balearic Islands) and Atlantic Ocean (Canary Islands). Methods We genotyped 22 microsatellite loci in 96 Egyptian vultures (Neophron percnopterus) from the Iberian Peninsula, 36 from Menorca (Balearic archipelago) and 242 (85% of the current population) from Fuerteventura (Canary Islands). We analysed genetic variation to estimate structure, gene flow, genetic diversity, effective size and recent demographic history of the populations. Additionally, 19 vultures were marked with satellite transmitters to track their migration routes. Results Insular populations were genetically differentiated from those of the mainland. We detected immigration in the insular populations and within the continental counterpart. We found similar levels of genetic variability between the continent and the islands, and a bottleneck analysis indicated recent sharp population declines in both archipelagos but not on the continent. Main conclusions Our study provides evidence that, in spite of significant differentiation, insular populations of highly mobile species may remain connected with the mainland. Conservation programmes should take into account population connectivity and integrate differentiated units of management within complex units of conservation that can best maintain processes and potential for evolutionary change.     

The role of genetic structure in the adaptive divergence of populations experiencing saltwater intrusion due to relative sea‐level rise

Saltwater intrusion into estuaries creates stressful conditions for nektonic species. Previous studies have shown that Gambusia affinis populations with exposure to saline environments develop genetic adaptations for increased survival during salinity stress. Here, we evaluate the genetic structure of G. affinis populations, previously shown to have adaptations for increased salinity tolerance, and determine the impact of selection and gene flow on structure of these populations. We found that gene flow was higher between populations experiencing different salinity regimes within an estuary than between similar marsh types in different estuaries, suggesting the development of saline‐tolerant phenotypes due to local adaptation. There was limited evidence of genetic structure along a salinity gradient, and only some of the genetic variation among sites was correlated with salinity. Our results suggest limited structure, combined with selection to saltwater intrusion, results in phenotypic divergence in spite of a lack of physical barriers to gene flow.     

HIERARCHICAL COMPARISON OF GENETIC VARIANCE-COVARIANCE MATRICES. II COASTAL-INLAND DIVERGENCE IN THE GARTER SNAKE,THAMNOPHIS ELEGANS

The time-scale for the evolution of additive genetic variance-covariance matrices (G-matrices) is a crucial issue in evolutionary biology. If the evolution of G-matrices is slow enough, we can use standard multivariate equations to model drift and selection response on evolutionary time scales. We compared the G-matrices for meristic traits in two populations of gaiter snakes (Thamnophis elegans) with an apparent separation time of 2 million years. Despite considerable divergence in the meristic traits, foraging habits, and diet, these populations show conservation of structure in their G-matrices. Using Flury's hierarchial approach to matrix comparisons, we found that the populations have retained the principal components (eigenvectors) of their G-matrices, but their eigenvalues have diverged. In contrast, we were unable to reject the hypothesis of equal environmental matrices (E-matrices) for these populations. We propose that a conserved pattern of multivariate stabilizing selection may have contributed to conservation of G- and E-matrix structure during the divergence of these populations.     

Defining evolutionary boundaries across parapatric ecomorphs of Black Salamanders (Aneides flavipunctatus) with conservation implications

The accurate delimitation of evolutionary population units represents an important component in phylogeographic and conservation genetic studies. Here, we used a combined population assignment and historical demographic approach to study a complex of ecomorphologically distinctive populations of Black Salamanders (Aneides flavipunctatus) that are parapatrically distributed and meet at a three‐way contact zone in north‐western California. We used mitochondrial tree‐based and multilocus clustering methods to evaluate a priori two‐ (Northern and Southern) and three (Northern, Coast and Inland) population hypotheses derived from previous studies. Mitochondrial results were consistent with the two‐ and three‐population hypotheses, while the nDNA clustering results supported only the two‐population hypothesis. Historical demographic analyses and mtDNA gene divergence estimates revealed that the Northern and Southern populations split during the Pliocene (2–5 Ma). Subdivision of the Southern population into Coast and Inland populations was estimated to be late Pleistocene (0.24 Ma), although our mtDNA results suggested a Pliocene divergence. Effective gene flow estimates (2N_em) suggest that either the two‐ or three‐population hypotheses remain valid. However, our results unexpectedly revealed that the Northern population might instead represent two parapatric populations that separated nearly 4 Ma. These results are surprising because the Pliocene divergence between these ecomorphologically conservative forms is similar or older than for the ecomorphologically divergent Coast and Inland sister populations. We conclude that Black Salamanders in north‐western California belong to at least three or four populations or species, and these all meet criteria for being Evolutionary Significant Units or ‘ESUs’ and therefore warrant conservation consideration.     

Phylogeography of a pearl oyster (Pinctada maxima) across the Indo‐Australian Archipelago: evidence of strong regional structure and population expansions but no phylogenetic breaks

This study investigates the genetic structure and phylogeography of a broadcast spawning bivalve mollusc, Pinctada maxima, throughout the Indo‐West Pacific and northern Australia. DNA sequence variation of the mitochondrial cytochrome oxidase subunit I (COI) gene was analysed in 367 individuals sampled from nine populations across the Indo‐West Pacific. Hierarchical AMOVA indicated strong genetic structuring amongst populations (Φ_ST = 0.372, P < 0.001); however, sequence divergence between the 47 haplotypes detected was low (maximum 1.8% difference) and no deep phylogenetic divergence was observed. Results suggest the presence of genetic barriers isolating populations of the South China Sea and central Indonesian regions, which, in turn, show patterns of historical separation from northern Australian regions. In P. maxima, historical vicariance during Pleistocene low sea levels is likely to have restricted planktonic larval transport, causing genetic differentiation amongst populations. However, low genetic differentiation is observed where strong ocean currents are present and is most likely due to contemporary larval transport along these pathways. Geographical association with haplotype distributions may indicate signs of early lineage sorting arising from historical population separations, yet an absence of divergent phylogenetic clades related to geography could be the consequence of periodic pulses of high genetic exchange. We compare our results with previous microsatellite DNA analysis of these P. maxima populations, and discuss implications for future conservation management of this species. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 632–646.     

Conservation genetics of highly isolated populations of the xerothermic beetle Crioceris quatuordecimpunctata (Chrysomelidae)

Xerothermic species are rare and threatened in central and eastern Europe. In light of the continuing loss of steppe‐like habitats due to anthropogenic fragmentation and degradation, the evaluation of genetic variation in populations inhabiting them is of immediate importance if appropriate conservation measures are to be undertaken. Here we report on the genetic diversity of the rare leaf beetle Crioceris quatuordecimpunctata, whose populations in central and eastern Europe inhabit highly geographically isolated areas. All of the studied populations (in Poland, Ukraine, and Slovakia) were differentiated at the mitochondrial marker COI. However, with respect to the nuclear marker ITS1, Polish populations were monomorphic, but distinct from all other populations. The distinctiveness of the studied populations was confirmed by Wolbachia screening, which showed that all populations carried different strains (one or two), which were probably transferred independently from other insects. On the other hand, no diversity was found in any marker within particular populations, which could be caused (at least for mtDNA) by a Wolbachia selective sweep. Crioceris quatuordecimpunctata probably consists of isolated populations, which went through narrow bottlenecks leading to a drastic reduction in their genetic diversity. As these populations are reciprocally monophyletic for mtDNA haplotypes and show a significant divergence of allele frequencies at nuclear loci, they could be classified as evolutionarily significant units (ESUs). In addition, DNA barcodes were used to identify Asparagus officinalis as the host plant for members of all studied populations. These data should be valuable in efforts to conserve populations of C. quatuordecimpunctata (e.g., for guiding reintroductions).     

Interaction of landscape and life history attributes on genetic diversity,neutral divergence and gene flow in a pristine community of salmonids

Landscape genetics holds promise for the forecasting of spatial patterns of genetic diversity based on key environmental features. Yet, the degree to which inferences based on single species can be extended to whole communities is not fully understood. We used a pristine and spatially structured community of three landlocked salmonids (Salvelinus fontinalis, Salmo salar, and Salvelinus alpinus) from Gros Morne National Park (Newfoundland, Canada) to test several predictions on the interacting effects of landscape and life history variation on genetic diversity, neutral divergence, and gene flow (m, migration rate). Landscape factors consistently influenced multispecies genetic patterns: (i) waterfalls created strong dichotomies in genetic diversity and divergence between populations above and below them in all three salmonids; (ii) contemporary m decreased with waterway distance in all three species, while neutral genetic divergence (θ) increased with waterway distance, albeit in only two taxa; (iii) river flow generally produced downstream‐biased m between populations when waterfalls separated these, but not otherwise. In contrast, we expected differential life history to result in a hierarchy of neutral divergence (S. salar > S. fontinalis > S. alpinus) based on disparities in dispersal abilities and population size from previous mark‐recapture studies. Such hierarchy additionally matched varying degrees of spatial genetic structure among species revealed through individual‐based analyses. We conclude that, whereas key landscape attributes hold power to predict multispecies genetic patterns in equivalent communities, they are likely to interact with species‐specific life history attributes such as dispersal, demography, and ecology, which will in turn affect holistic conservation strategies.     

Species‐level view of population structure and gene flow for a critically endangered primate (Varecia variegata)

Lemurs are among the world's most threatened mammals. The critically endangered black‐and‐white ruffed lemur (Varecia variegata), in particular, has recently experienced rapid population declines due to habitat loss, ecological sensitivities to habitat degradation, and extensive human hunting pressure. Despite this, a recent study indicates that ruffed lemurs retain among the highest levels of genetic diversity for primates. Identifying how this diversity is apportioned and whether gene flow is maintained among remnant populations will help to diagnose and target conservation priorities. We sampled 209 individuals from 19 sites throughout the remaining V. variegata range. We used 10 polymorphic microsatellite loci and ~550 bp of mtDNA sequence data to evaluate genetic structure and population dynamics, including dispersal patterns and recent population declines. Bayesian cluster analyses identified two distinct genetic clusters, which optimally partitioned data into populations occurring on either side of the Mangoro River. Localities north of the Mangoro were characterized by greater genetic diversity, greater gene flow (lower genetic differentiation) and higher mtDNA haplotype and nucleotide diversity than those in the south. Despite this, genetic differentiation across all sites was high, as indicated by high average F_ST (0.247) and Φ_ST (0.544), and followed a pattern of isolation‐by‐distance. We use these results to suggest future conservation strategies that include an effort to maintain genetic diversity in the north and restore connectivity in the south. We also note the discordance between patterns of genetic differentiation and current subspecies taxonomy, and encourage a re‐evaluation of conservation management units moving forward.     

HETEROGENEOUS GENOMIC DIFFERENTIATION IN MARINE THREESPINE STICKLEBACKS: ADAPTATION ALONG AN ENVIRONMENTAL GRADIENT

Evolutionary divergence among populations occupying ecologically distinct environments can occur even in the face of on‐going gene flow. However, the genetic underpinnings, as well as the scale and magnitude at which this differentiation occurs in marine habitats are not well understood. We investigated the patterns and degree of genomic heterogeneity in threespine sticklebacks (Gasterosteus aculeatus) by assessing genetic variability in 20 nongenic and 20 genic (associated with genes important for freshwater adaptation) microsatellite loci in samples collected from 38 locations spanning the entire Baltic Sea coast to the North Sea boundary. Population divergence (F_ST ≈ 0.026) and structuring (five genetic clusters) was significantly more pronounced in the genic as compared to nongenic markers (F_ST ≈ 0.008; no genetic clusters). Patterns of divergence in the genic markers—45% of which were identified as outliers—correlated with local differences in salinity. Yet, a strong positive correlation between divergence in genic and nongenic markers, and their association with environmental factors suggests that adaptive divergence is reducing gene flow across the genome. Apart from providing a clear demonstration of heterogeneous genomic patterns of differentiation in a marine species, the results are indicative of adaptive population structuring across the relatively young Baltic Sea in spite of ample opportunities for gene flow.     

A survey of equid mitochondrial DNA: Implications for the evolution, genetic diversity and conservation of Equus

The evolution, taxonomy and conservation of the genus Equuswere investigated by examining the mitochondrial DNA sequences of thecontrol region and 12S rRNA gene. The phylogenetic analysis of thesesequences provides further evidence that the deepest node in thephylogeny of the extant species is a divergence between twolineages; one leading to the ancestor of modern horses (E.ferus, domestic and przewalskii) and the other to thezebra and ass ancestor, with the later speciation events of the zebrasand asses occurring either as one or more rapid radiations, or withextensive secondary contact after speciation. Examination of the geneticdiversity within species suggested that two of the E. hemionussubspecies (E. h. onager and E. h. kulan) onlyrecently diverged, and perhaps, are insufficiently different to beclassified as separate subspecies. The genetic divergence betweendomestic and wild forms of E. ferus (horse) and E.africanus (African ass) was no greater than expected within anequid species. In E. burchelli (plains zebra) there was anindication of mtDNA divergence between populations increasing withdistance. The implications of these results for equid conservation arediscussed and recommendations are made for conservation action.     

Population structure,diversity, and phylogeography in the near‐threatened Eurasian black vultures Aegypius monachus (Falconiformes; Accipitridae) in Europe: insights from microsatellite and mitochondrial DNA variation

The Eurasian black vulture (Aegypius monachus) has experienced a severe decline during the last two centuries and is globally classified as near‐threatened. This has led to the extinction of many traditional breeding areas in Europe and resulted in the present patchy distribution (Iberian and Balkan peninsulas) in the Western Palearctic. In the present study, we describe the current genetic status of the European populations using both mitochondrial cytochrome b sequences and nuclear microsatellite markers, comparing with those found in Asia (Mongolia and Caucasus region). Although, mitochondrial (mt)DNA revealed a relatively low genetic variability (haplotype diversity), no evidence of genome‐wide genetic erosion exists because nuclear diversity exhibits normal levels and strong differentiation. A highly philopatric dispersal behaviour must be invoked to explain the existence of a clear pattern that revealed by the phylogeographic analysis, which indicates a sharp East–West clinal distribution and an allopatric differentiation. The distribution of mtDNA haplotypes one in the Iberian population and two in Balkan population and the significance divergence at nuclear loci fulfill the definitions of those populations as evolutionary significant units. We discuss how management strategies should aim at the maintenance (or increase) of current genetic variability levels, suggesting that independent conservation plans are urgently required to protect these two breeding European populations from extinction. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 859–872.     

Distinctiveness in the face of gene flow: hybridization between specialist and generalist gartersnakes

Patterns of divergence and polymorphism across hybrid zones can provide important clues as to their origin and maintenance. Unimodal hybrid zones or hybrid swarms are composed predominantly of recombinant individuals whose genomes are patchworks of alleles derived from each parental lineage. In contrast, bimodal hybrid zones contain few identifiable hybrids; most individuals fall within distinct genetic clusters. Distinguishing between hybrid swarms and bimodal hybrid zones can be important for taxonomic and conservation decisions regarding the status and value of hybrid populations. In addition, the causes of bimodality are important in understanding the generation and maintenance of biological diversity. For example, are distinct clusters mostly reproductively isolated and co‐adapted gene complexes, or can distinctiveness be maintained by a few ‘genomic islands’ despite rampant gene flow across much of the genome? Here we focus on three patterns of distinctiveness in the face of gene flow between gartersnake taxa in the Great Lakes region of North America. Bimodality, the persistence of distinct clusters of genotypes, requires strong barriers to gene flow and supports recognition of distinct specialist (Thamnophis butleri) and generalist (Thamnophis radix) taxa. Concordance of DNA‐based clusters with morphometrics supports the hypothesis that trophic morphology is a key component of divergence. Finally, disparity in the level of differentiation across molecular markers (amplified fragment length polymorphisms) indicates that distinctiveness is maintained by strong selection on a few traits despite high gene flow currently or in the recent past.     

The subspecies concept in butterflies: has its application in taxonomy and conservation biology outlived its usefulness?

Subspecies lie at the interface between systematics and population genetics, and represent a unit of biological organization in zoology that is widely used in the disciplines of taxonomy and conservation biology. In this review, we explore the utility of subspecies in relation to their application in systematics and biodiversity conservation, and briefly summarize species concepts and criteria for their diagnosis, particularly from an invertebrate perspective. The subspecies concept was originally conceived as a formal means of documenting geographical variation within species based on morphological characters; however, the utility of subspecies is hampered by inconsistencies by which they are defined conceptually, a lack of objective criteria or properties that serve to delimit their boundaries, and their frequent failure to reflect distinct evolutionary units according to population genetic structure. Moreover, the concept has been applied to populations largely comprising different components of genetic diversity reflecting contrasting evolutionary processes. We recommend that, under the general lineage (unified) species concept, the definition of subspecies be restricted to extant animal groups that comprise evolving populations representing partially isolated lineages of a species that are allopatric, phenotypically distinct, and have at least one fixed diagnosable character state, and that these character differences are (or are assumed to be) correlated with evolutionary independence according to population genetic structure. Phenotypic character types include colour pattern, morphology, and behaviour or ecology. Under these criteria, allopatric subspecies are a type of evolutionarily significant unit within species in that they show both neutral divergence through the effects of genetic drift and adaptive divergence under natural selection, and provide an historical context for identifying biodiversity units for conservation. Conservation of the adaptedness and adaptability of gene pools, however, may require additional approaches. Recent studies of Australian butterflies exemplify these points. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Genetic structure and demographic history of the endangered tree species Dysoxylum malabaricum (Meliaceae) in Western Ghats,India: implications for conservation in a biodiversity hotspot

The impact of fragmentation by human activities on genetic diversity of forest trees is an important concern in forest conservation, especially in tropical forests. Dysoxylum malabaricum (white cedar) is an economically important tree species, endemic to the Western Ghats, India, one of the world's eight most important biodiversity hotspots. As D. malabaricum is under pressure of disturbance and fragmentation together with overharvesting, conservation efforts are required in this species. In this study, range‐wide genetic structure of twelve D. malabaricum populations was evaluated to assess the impact of human activities on genetic diversity and infer the species’ evolutionary history, using both nuclear and chloroplast (cp) DNA simple sequence repeats (SSR). As genetic diversity and population structure did not differ among seedling, juvenile and adult age classes, reproductive success among the old‐growth trees and long distance seed dispersal by hornbills were suggested to contribute to maintain genetic diversity. The fixation index (F_IS) was significantly correlated with latitude, with a higher level of inbreeding in the northern populations, possibly reflecting a more severe ecosystem disturbance in those populations. Both nuclear and cpSSRs revealed northern and southern genetic groups with some discordance of their distributions; however, they did not correlate with any of the two geographic gaps known as genetic barriers to animals. Approximate Bayesian computation‐based inference from nuclear SSRs suggested that population divergence occurred before the last glacial maximum. Finally we discussed the implications of these results, in particular the presence of a clear pattern of historical genetic subdivision, on conservation policies.     

Recent physical connections may explain weak genetic structure in western Alaskan chum salmon (Oncorhynchus keta) populations

Low genetic divergence at neutral loci among populations is often the result of high levels of contemporary gene flow. Western Alaskan summer‐run chum salmon (Oncorhynchus keta) populations demonstrate weak genetic structure, but invoking contemporary gene flow as the basis for the low divergence is problematic because salmon home to their natal streams and some of the populations are thousands of kilometers apart. We used genotypes from microsatellite and single nucleotide polymorphism loci to investigate alternative explanations for the current genetic structure of chum salmon populations from western Alaska. We also estimated current levels of gene flow among Kuskokwim River populations. Our results suggest that weak genetic structure is best explained by physical connections that occurred after the Holocene Thermal Maximum among the Yukon, Kuskokwim, and Nushagak drainages that allowed gene flow to occur among now distant populations.     

Divergence with gene flow in a population of thermophilic bacteria: a potential role for spatially varying selection

A fundamental goal of evolutionary biology is to understand how ecological diversity arises and is maintained in natural populations. We have investigated the contributions of gene flow and divergent selection to the distribution of genetic variation in an ecologically differentiated population of a thermophilic cyanobacterium (Mastigocladus laminosus) found along the temperature gradient of a nitrogen‐limited stream in Yellowstone National Park. For most loci sampled, gene flow appears to be sufficient to prevent substantial genetic divergence. However, one locus (rfbC) exhibited a comparatively low migration rate as well as other signatures expected for a gene experiencing spatially varying selection, including an excess of common variants, an elevated level of polymorphism and extreme genetic differentiation along the gradient. rfbC is part of an expression island involved in the production of the polysaccharide component of the protective envelope of the heterocyst, the specialized nitrogen‐fixing cell of these bacteria. SNP genotyping in the vicinity of rfbC revealed a ~5‐kbp region including a gene content polymorphism that is tightly associated with environmental temperature and therefore likely contains the target of selection. Two genes have been deleted both in the predominant haplotype found in the downstream region of White Creek and in strains from other Yellowstone populations of M. laminosus, which may result in the production of heterocysts with different envelope properties. This study implicates spatially varying selection in the maintenance of variation related to thermal performance at White Creek despite on‐going or recent gene flow.