Range‐wide genetic structure of a cooperative mouse in a semi‐arid zone: Evidence for panmixia

Landscape topography and the mobility of individuals will have fundamental impacts on a species’ population structure, for example by enhancing or reducing gene flow and therefore influencing the effective size and genetic diversity of the population. However, social organization will also influence population genetic structure. For example, species that live and breed in cooperative groups may experience high levels of inbreeding and strong genetic drift. The western pebble‐mound mouse (Pseudomys chapmani), which occupies a highly heterogeneous, semi‐arid landscape in Australia, is an enigmatic social mammal that has the intriguing behaviour of working cooperatively in groups to build permanent pebble mounds above a subterranean burrow system. Here, we used both nuclear (microsatellite) and mitochondrial (mtDNA) markers to analyse the range‐wide population structure of western pebble‐mound mice sourced from multiple social groups. We observed high levels of genetic diversity at the broad scale, very weak genetic differentiation at a finer scale and low levels of inbreeding. Our genetic analyses suggest that the western pebble‐mound mouse population is both panmictic and highly viable. We conclude that high genetic connectivity across the complex landscape is a consequence of the species’ ability to permeate their environment, which may be enhanced by “boom‐bust” population dynamics driven by the semi‐arid climate. More broadly, our results highlight the importance of sampling strategies to infer social structure and demonstrate that sociality is an important component of population genetic structure.     

Genetic differentiation of the pine processionary moth at the southern edge of its range: contrasting patterns between mitochondrial and nuclear markers

The pine processionary moth (Thaumetopoea pityocampa) is an important pest of coniferous forests at the southern edge of its range in Maghreb. Based on mitochondrial markers, a strong genetic differentiation was previously found in this species between western (pityocampa clade) and eastern Maghreb populations (ENA clade), with the contact zone between the clades located in Algeria. We focused on the moth range in Algeria, using both mitochondrial (a 648 bp fragment of the tRNA‐cox2) and nuclear (11 microsatellite loci) markers. A further analysis using a shorter mtDNA fragment and the same microsatellite loci was carried out on a transect in the contact zone between the mitochondrial clades. Mitochondrial diversity showed a strong geographical structure and a well‐defined contact zone between the two clades. In particular, in the pityocampa clade, two inner subclades were found whereas ENA did not show any further structure. Microsatellite analysis outlined a different pattern of differentiation, with two main groups not overlapping with the mitochondrial clades. The inconsistency between mitochondrial and nuclear markers is probably explained by sex‐biased dispersal and recent afforestation efforts that have bridged isolated populations.     

The association between mitochondrial genetic variation and reduced colony fitness in an invasive wasp

Despite the mitochondrion's long‐recognized role in energy production, mitochondrial DNA (mtDNA) variation commonly found in natural populations was assumed to be effectively neutral. However, variation in mtDNA has now been increasingly linked to phenotypic variation in life history traits and fitness. We examined whether the relative fitness in native and invasive common wasp (Vespula vulgaris) populations in Belgium and New Zealand (NZ), respectively, can be linked to mtDNA variation. Social wasp colonies in NZ were smaller with comparatively fewer queen cells, indicating a reduced relative fitness in the invaded range. Interestingly, queen cells in this population were significantly larger leading to larger queen offspring. By sequencing 1,872 bp of the mitochondrial genome, we determined mitochondrial haplotypes and detected reduced genetic diversity in NZ. Three common haplotypes in NZ frequently produced many queens, whereas the four rare haplotypes produced significantly fewer or no queens. The entire mitochondrial genome for each of these haplotypes was sequenced to identify polymorphisms associated with fitness reduction. We found 16 variable sites; however, no nonsynonymous mutation that was clearly causing impaired mitochondrial function was detected. We discuss how detected variants may alter secondary structures, gene expression or mito‐nuclear interactions, or could be associated with nuclear‐encoded variation. Whatever the ultimate mechanism, we show reduced fitness and mtDNA variation in an invasive wasp population as well as specific mtDNA variants associated with fitness variation within this population. Ours is one of only a few studies that confirm fitness impacts of mtDNA variation in wild nonmodel populations.     

SNPs across time and space: population genomic signatures of founder events and epizootics in the House Finch (Haemorhous mexicanus)

Identifying genomic signatures of natural selection can be challenging against a background of demographic changes such as bottlenecks and population expansions. Here, we disentangle the effects of demography from selection in the House Finch (Haemorhous mexicanus) using samples collected before and after a pathogen‐induced selection event. Using ddRADseq, we genotyped over 18,000 SNPs across the genome in native pre‐epizootic western US birds, introduced birds from Hawaii and the eastern United States, post‐epizootic eastern birds, and western birds sampled across a similar time span. We found 14% and 7% reductions in nucleotide diversity, respectively, in Hawaiian and pre‐epizootic eastern birds relative to pre‐epizootic western birds, as well as elevated levels of linkage disequilibrium and other signatures of founder events. Despite finding numerous significant frequency shifts (outlier loci) between pre‐epizootic native and introduced populations, we found no signal of reduced genetic diversity, elevated linkage disequilibrium, or outlier loci as a result of the epizootic. Simulations demonstrate that the proportion of outliers associated with founder events could be explained by genetic drift. This rare view of genetic evolution across time in an invasive species provides direct evidence that demographic shifts like founder events have genetic consequences more widespread across the genome than natural selection.     

The combined use of raw and phylogenetically independent methods of outlier detection uncovers genome‐wide dynamics of local adaptation in a lizard

Local adaptation is a dynamic process by which different allele combinations are selected in different populations at different times, and whose genetic signature can be inferred by genome‐wide outlier analyses. We combined gene flow estimates with two methods of outlier detection, one of them independent of population coancestry (CIOA) and the other one not (ROA), to identify genetic variants favored when ecology promotes phenotypic convergence. We analyzed genotyping‐by‐sequencing data from five populations of a lizard distributed over an environmentally heterogeneous range that has been changing since the split of eastern and western lineages ca. 3 mya. Overall, western lizards inhabit forest habitat and are unstriped, whereas eastern ones inhabit shrublands and are striped. However, one population (Lerma) has unstriped phenotype despite its eastern ancestry. The analysis of 73,291 SNPs confirmed the east–west division and identified nonoverlapping sets of outliers (12 identified by ROA and 9 by CIOA). ROA revealed ancestral adaptive variation in the uncovered outliers that were subject to divergent selection and differently fixed for eastern and western populations at the extremes of the environmental gradient. Interestingly, such variation was maintained in Lerma, where we found high levels of heterozygosity for ROA outliers, whereas CIOA uncovered innovative variants that were selected only there. Overall, it seems that both the maintenance of ancestral variation and asymmetric migration have counterbalanced adaptive lineage splitting in our model species. This scenario, which is likely promoted by a changing and heterogeneous environment, could hamper ecological speciation of locally adapted populations despite strong genetic structure between lineages.     

Diversifying selection drives parallel evolution of gill raker number and body size along the speciation continuum of European whitefish

Adaptive radiation is the evolution of ecological and phenotypical diversity. It arises via ecological opportunity that promotes the exploration of underutilized or novel niches mediating specialization and reproductive isolation. The assumed precondition for rapid local adaptation is diversifying natural selection, but random genetic drift could also be a major driver of this process. We used 27 populations of European whitefish (Coregonus lavaretus) from nine lakes distributed in three neighboring subarctic watercourses in northern Fennoscandia as a model to test the importance of random drift versus diversifying natural selection for parallel evolution of adaptive phenotypic traits. We contrasted variation for two key adaptive phenotypic traits correlated with resource utilization of polymorphic fish; the number of gill rakers and the total length of fish, with the posterior distribution of neutral genetic differentiation from 13 microsatellite loci, to test whether the observed phenotypic divergence could be achieved by random genetic drift alone. Our results show that both traits have been under diversifying selection and that the evolution of these morphs has been driven by isolation through habitat adaptations. We conclude that diversifying selection acting on gill raker number and body size has played a significant role in the ongoing adaptive radiation of European whitefish morphs in this region.     

Parallel plumage colour evolution and introgressive hybridization in wheatears

Genetic and phenotypic mosaics, in which various phenotypes and different genomic regions show discordant patterns of species or population divergence, offer unique opportunities to study the role of ancestral and introgressed genetic variation in phenotypic evolution. Here, we investigated the evolution of discordant phenotypic and genetic divergence in a monophyletic clade of four songbird taxa—pied wheatear (O. pleschanka), Cyprus wheatear (Oenanthe cypriaca), and western and eastern subspecies of black‐eared wheatear (O. h. hispanica and O. h. melanoleuca). Phenotypically, black back and neck sides distinguish pied and Cyprus wheatears from the white‐backed/necked black‐eared wheatears. Meanwhile, mitochondrial variation only distinguishes western black‐eared wheatear. In the absence of nuclear genetic data, and given frequent hybridization among eastern black‐eared and pied wheatear, it remains unclear whether introgression is responsible for discordance between mitochondrial divergence patterns and phenotypic similarities, or whether plumage coloration evolved in parallel. Multispecies coalescent analyses of about 20,000 SNPs obtained from RAD data mapped to a draft genome assembly resolve the species tree, provide evidence for the parallel evolution of colour phenotypes and establish western and eastern black‐eared wheatears as independent taxa that should be recognized as full species. The presence of the entire admixture spectrum in the Iranian hybrid zone and the detection of footprints of introgression from pied into eastern black‐eared wheatear beyond the hybrid zone despite strong geographic structure of ancestry proportions furthermore suggest a potential role for introgression in parallel plumage colour evolution. Our results support the importance of standing heterospecific and/or ancestral variation in phenotypic evolution.     

Population genomics reveals multiple drivers of population differentiation in a sex‐role‐reversed pipefish

A major goal of molecular ecology is to identify the causes of genetic and phenotypic differentiation among populations. Population genomics is suitably poised to tackle these key questions by diagnosing the evolutionary mechanisms driving divergence in nature. Here, we set out to investigate the evolutionary processes underlying population differentiation in the Gulf pipefish, Syngnathus scovelli. We sampled approximately 50 fish from each of 12 populations distributed from the Gulf coast of Texas to the Atlantic coast of Florida and performed restriction‐site‐associated DNA sequencing to identify SNPs throughout the genome. After imposing quality and stringency filters, we selected a panel of 6348 SNPs present in all 12 populations, 1753 of which were not physically linked. We identified a genome‐wide pattern of isolation by distance, in addition to a more substantial genetic break separating populations in the Gulf of Mexico from those in the Atlantic. We also used several divergence outlier approaches and tests for genotype–environment correlations to identify 400 SNPs putatively involved in local adaptation. Patterns of phenotypic differentiation and variation diverged from the overall genomic pattern, suggesting that selection, phenotypic plasticity or demographic factors may be shaping phenotypes in distinct populations. Overall, our results suggest that population divergence is driven by a variety of factors in S. scovelli, including neutral processes and selection on multiple traits.     

A biogeographical profile of the sand cockroach Arenivaga floridensis and its bearing on origin hypotheses for Florida scrub biota

Florida scrub is a xeric ecosystem associated with the peninsula's sand ridges, whose intermittent Pliocene–Pleistocene isolation is considered key to scrub endemism. One scrub origin hypothesis posits endemics were sourced by the Pliocene dispersal of arid‐adapted taxa from southwestern North America; a second invokes Pleistocene migration within eastern North America. Only one study to date has explicitly tested these competing hypotheses, supporting an eastern origin for certain scrub angiosperms. For further perspective, we conducted a genetic analysis of an endemic arthropod, the Florida sand cockroach (Arenivaga floridensis), with two aims: (1) to reconstruct the peninsular colonization and residence history of A. floridensis and (2) determine whether its biogeographic profile favors either origin hypothesis. We sequenced the cox2 mitochondrial gene for 237 specimens (65 populations) as well as additional loci (cox1, nuclear H3) for a subset of Florida roaches and congeners. Using Network and Bayesian inference methods, we identified three major lineages whose genetic differentiation and phylogeographical structure correspond with late Pliocene peninsula insularization, indicating Arenivaga was present and broadly distributed in Florida at that time. Stem and crown divergence estimates (6.36 Ma; 2.78 Ma) between A. floridensis and western sister taxa span a period of extensive dispersal by western biota along an arid Gulf Coast corridor. These phylogeographical and phylogenetic results yield a biogeographic profile consistent with the western origin hypothesis. Moreover, age estimates for the roach's peninsular residence complement those of several other endemics, favoring a Pliocene (or earlier) inception of the scrub ecosystem. We argue that eastern versus western hypotheses are not mutually exclusive; rather, a composite history of colonization involving disparate biotas better explains the diverse endemism of Florida scrub.     

Radiation of the polymorphic Little Devil poison frog (Oophaga sylvatica) in Ecuador

Some South American poison frogs (Dendrobatidae) are chemically defended and use bright aposematic colors to warn potential predators of their unpalatability. Aposematic signals are often frequency‐dependent where individuals deviating from a local model are at a higher risk of predation. However, extreme diversity in the aposematic signal has been documented in poison frogs, especially in Oophaga. Here, we explore the phylogeographic pattern among color‐divergent populations of the Little Devil poison frog Oophaga sylvatica by analyzing population structure and genetic differentiation to evaluate which processes could account for color diversity within and among populations. With a combination of PCR amplicons (three mitochondrial and three nuclear markers) and genome‐wide markers from a double‐digested RAD (ddRAD) approach, we characterized the phylogenetic and genetic structure of 199 individuals from 13 populations (12 monomorphic and 1 polymorphic) across the O. sylvatica distribution. Individuals segregated into two main lineages by their northern or southern latitudinal distribution. A high level of genetic and phenotypic polymorphism within the northern lineage suggests ongoing gene flow. In contrast, low levels of genetic differentiation were detected among the southern lineage populations and support recent range expansions from populations in the northern lineage. We propose that a combination of climatic gradients and structured landscapes might be promoting gene flow and phylogenetic diversification. Alternatively, we cannot rule out that the observed phenotypic and genomic variations are the result of genetic drift on near or neutral alleles in a small number of genes.     

RAD sequencing reveals genomewide divergence between independent invasions of the European green crab (Carcinus maenas) in the Northwest Atlantic

Genomic studies of invasive species can reveal both invasive pathways and functional differences underpinning patterns of colonization success. The European green crab (Carcinus maenas) was initially introduced to eastern North America nearly 200 years ago where it expanded northwards to eastern Nova Scotia. A subsequent invasion to Nova Scotia from a northern European source allowed further range expansion, providing a unique opportunity to study the invasion genomics of a species with multiple invasions. Here, we use restriction‐site‐associated DNA sequencing‐derived SNPs to explore fine‐scale genomewide differentiation between these two invasions. We identified 9137 loci from green crab sampled from 11 locations along eastern North America and compared spatial variation to mitochondrial COI sequence variation used previously to characterize these invasions. Overall spatial divergence among invasions was high (pairwise F_ST ~0.001 to 0.15) and spread across many loci, with a mean F_ST ~0.052 and 52% of loci examined characterized by F_ST values >0.05. The majority of the most divergent loci (i.e., outliers, ~1.2%) displayed latitudinal clines in allele frequency highlighting extensive genomic divergence among the invasions. Discriminant analysis of principal components (both neutral and outlier loci) clearly resolved the two invasions spatially and was highly correlated with mitochondrial divergence. Our results reveal extensive cryptic intraspecific genomic diversity associated with differing patterns of colonization success and demonstrates clear utility for genomic approaches to delineating the distribution and colonization success of aquatic invasive species.     

Investigation of the geographical scale of adaptive phenological variation and its underlying genetics in Arabidopsis thaliana

Despite the increasing number of genomic tools, identifying the genetics underlying adaptive complex traits remains challenging in the model species Arabidopsis thaliana. This is due, at least in part, to the lack of data on the geographical scale of adaptive phenotypic variation. The aims of this study were (i) to tease apart the historical roles of adaptive and nonselective processes in shaping phenological variation in A. thaliana in France and (ii) to gain insights into the spatial scale of adaptive variation by identifying the putative selective agents responsible for this selection. Forty‐nine natural stands from four climatically contrasted French regions were characterized (i) phenologically for six traits, (ii) genetically using 135 SNP markers and (iii) ecologically for 42 variables. Up to 63% of phenological variation could be explained by neutral genetic diversity. The remaining phenological variation displayed stronger associations with ecological variation within regions than among regions, suggesting the importance of local selective agents in shaping adaptive phenological variation. Although climatic conditions have often been suggested as the main selective agents acting on phenology in A. thaliana, both edaphic conditions and interspecific competition appear to be strong selective agents in some regions. In a first attempt to identify the genetics of phenological variation at different geographical scales, we phenotyped worldwide accessions and local polymorphic populations from the French RegMap in a genome‐wide association (GWA) mapping study. The genomic regions associated with phenological variation depended upon the geographical scale considered, stressing the need to account for the scale of adaptive phenotypic variation when choosing accession panels for GWAS.     

Phylogeography and adaptation genetics of stickleback from the Haida Gwaii archipelago revealed using genome‐wide single nucleotide polymorphism genotyping

Threespine stickleback populations are model systems for studying adaptive evolution and the underlying genetics. In lakes on the Haida Gwaii archipelago (off western Canada), stickleback have undergone a remarkable local radiation and show phenotypic diversity matching that seen throughout the species distribution. To provide a historical context for this radiation, we surveyed genetic variation at >1000 single nucleotide polymorphism (SNP) loci in stickleback from over 100 populations. SNPs included markers evenly distributed throughout genome and candidate SNPs tagging adaptive genomic regions. Based on evenly distributed SNPs, the phylogeographic pattern differs substantially from the disjunct pattern previously observed between two highly divergent mtDNA lineages. The SNP tree instead shows extensive within watershed population clustering and different watersheds separated by short branches deep in the tree. These data are consistent with separate colonizations of most watersheds, despite underlying genetic connections between some independent drainages. This supports previous suppositions that morphological diversity observed between watersheds has been shaped independently, with populations exhibiting complete loss of lateral plates and giant size each occurring in several distinct clades. Throughout the archipelago, we see repeated selection of SNPs tagging candidate freshwater adaptive variants at several genomic regions differentiated between marine–freshwater populations on a global scale (e.g. EDA, Na/K ATPase). In estuarine sites, both marine and freshwater allelic variants were commonly detected. We also found typically marine alleles present in a few freshwater lakes, especially those with completely plated morphology. These results provide a general model for postglacial colonization of freshwater habitat by sticklebacks and illustrate the tremendous potential of genome‐wide SNP data sets hold for resolving patterns and processes underlying recent adaptive divergences.     

Y‐chromosome evidence supports widespread signatures of three‐species Canis hybridization in eastern North America

There has been considerable discussion on the origin of the red wolf and eastern wolf and their evolution independent of the gray wolf. We analyzed mitochondrial DNA (mtDNA) and a Y‐chromosome intron sequence in combination with Y‐chromosome microsatellites from wolves and coyotes within the range of extensive wolf–coyote hybridization, that is, eastern North America. The detection of divergent Y‐chromosome haplotypes in the historic range of the eastern wolf is concordant with earlier mtDNA findings, and the absence of these haplotypes in western coyotes supports the existence of the North American evolved eastern wolf (Canis lycaon). Having haplotypes observed exclusively in eastern North America as a result of insufficient sampling in the historic range of the coyote or that these lineages subsequently went extinct in western geographies is unlikely given that eastern‐specific mtDNA and Y‐chromosome haplotypes represent lineages divergent from those observed in extant western coyotes. By combining Y‐chromosome and mtDNA distributional patterns, we identified hybrid genomes of eastern wolf, coyote, gray wolf, and potentially dog origin in Canis populations of central and eastern North America. The natural contemporary eastern Canis populations represent an important example of widespread introgression resulting in hybrid genomes across the original C. lycaon range that appears to be facilitated by the eastern wolf acting as a conduit for hybridization. Applying conventional taxonomic nomenclature and species‐based conservation initiatives, particularly in human‐modified landscapes, may be counterproductive to the effective management of these hybrids and fails to consider their evolutionary potential.     

Niche differentiation and colonization of a novel environment by an asexual parasitic wasp

How do asexual taxa become adapted to a diversity of environments, and how do they persist despite changing environmental conditions? These questions are linked by their mutual focus on the relationship between genetic variation, which is often limited in asexuals, and the ability to respond to environmental variation. Asexual taxa originating from a single ancestor present a unique opportunity to assess rates of phenotypic and genetic change when access to new genetic variation is limited to mutation. Diachasma muliebre is an asexual Hymenopteran wasp that is geographically and genetically isolated from all sexual relatives. D. muliebre attack larvae of the western cherry fruit fly (Rhagoletis indifferens), which in turn feed inside bitter cherry fruit (Prunus emarginata) in August and September. R. indifferens has recently colonized a new host plant with an earlier fruiting phenology (June/July), domesticated sweet cherries (P. avium), and D. muliebre has followed its host into this temporally earlier niche. We tested three hypotheses: 1) that all D. muliebre lineages originate from a single asexual ancestor; 2) that different D. muliebre lineages (as defined by unique mtDNA haplotypes) have differentiated on their ancestral host in an important life‐history trait, eclosion timing; and 3) that early‐eclosing lineages have preferentially colonized the new sweet cherry niche. We find that mitochondrial COI and microsatellite data provide strong support for a single ancestral origin for all lineages. Furthermore, COI sequencing revealed five mitochondrial haplotypes among D. muliebre, and individual wasps possessing one distinctive mitochondrial haplotype (haplotype II) eclosed as reproductive adults significantly earlier than wasps with all other haplotypes. In addition, this early‐eclosing lineage of D. muliebre is one of two lineages that have colonized the P. avium habitat, consistent with the preferential colonization hypothesis. These data suggest that D. muliebre has evolved adaptive phenotypic variation despite limited genetic variation, and that this variation has subsequently allowed an expansion of some wasps into a novel habitat. The D. muliebre system may allow for in‐depth study of adaptation and long‐term persistence of asexual taxa.     

Phylogeography and lineage‐specific patterns of genetic diversity and molecular evolution in a group of North American skinks

Geography influences the evolutionary trajectory of species by mediating opportunities for hybridization, gene flow, demographic shifts and adaptation. We sought to understand how geography and introgression can generate species‐specific patterns of genetic diversity by examining phylogeographical relationships in the North American skink species Plestiodon multivirgatus and P. tetragrammus (Squamata: Scincidae). Using a multilocus dataset (three mitochondrial genes, four nuclear genes; a total of 3455 bp) we discovered mito‐nuclear discordance, consistent with mtDNA introgression. We further tested for evidence of species‐wide mtDNA introgression by using comparisons of genetic diversity, selection tests and extended Bayesian skyline analyses. Our findings suggest that P. multivirgatus acquired its mitochondrial genome from P. tetragrammus after their initial divergence. This putative species‐wide mitochondrial capture was further evidenced by statistically indistinguishable substitution rates between mtDNA and nDNA in P. multivirgatus. This rate discrepancy was observed in P. multivirgatus but not P. tetragrammus, which has important implications for studies that combine mtDNA and nDNA sequences when inferring time since divergence between taxa. Our findings suggest that by facilitating opportunities for interspecific introgression, geography can alter the course of molecular evolution between recently diverged lineages.     

Population structure and phylogeography reveal pathways of colonization by a migratory marine reptile (Chelonia mydas) in the central and eastern Pacific

Climate, behavior, ecology, and oceanography shape patterns of biodiversity in marine faunas in the absence of obvious geographic barriers. Marine turtles are an example of highly migratory creatures with deep evolutionary lineages and complex life histories that span both terrestrial and marine environments. Previous studies have focused on the deep isolation of evolutionary lineages (>3 mya) through vicariance; however, little attention has been given to the pathways of colonization of the eastern Pacific and the processes that have shaped diversity within the most recent evolutionary time. We sequenced 770 bp of the mtDNA control region to examine the stock structure and phylogeography of 545 green turtles from eight different rookeries in the central and eastern Pacific. We found significant differentiation between the geographically separated nesting populations and identified five distinct stocks (F_ST = 0.08–0.44, P < 0.005). Central and eastern Pacific Chelonia mydas form a monophyletic group containing 3 subclades, with Hawaii more closely related to the eastern Pacific than western Pacific populations. The split between sampled central/eastern and western Pacific haplotypes was estimated at around 0.34 mya, suggesting that the Pacific region west of Hawaii has been a more formidable barrier to gene flow in C. mydas than the East Pacific Barrier. Our results suggest that the eastern Pacific was colonized from the western Pacific via the Central North Pacific and that the Revillagigedos Islands provided a stepping‐stone for radiation of green turtles from the Hawaiian Archipelago to the eastern Pacific. Our results fit with a broader paradigm that has been described for marine biodiversity, where oceanic islands, such as Hawaii and Revillagigedo, rather than being peripheral evolutionary “graveyards”, serve as sources and recipients of diversity and provide a mechanism for further radiation.     

Parasite‐mediated selection in a natural metapopulation of Daphnia magna

Parasite‐mediated selection varying across time and space in metapopulations is expected to result in host local adaptation and the maintenance of genetic diversity in disease‐related traits. However, nonadaptive processes like migration and extinction‐(re)colonization dynamics might interfere with adaptive evolution. Understanding how adaptive and nonadaptive processes interact to shape genetic variability in life‐history and disease‐related traits can provide important insights into their evolution in subdivided populations. Here we investigate signatures of spatially fluctuating, parasite‐mediated selection in a natural metapopulation of Daphnia magna. Host genotypes from infected and uninfected populations were genotyped at microsatellite markers, and phenotyped for life‐history and disease traits in common garden experiments. Combining phenotypic and genotypic data a Q_ST–F_ST‐like analysis was conducted to test for signatures of parasite mediated selection. We observed high variation within and among populations for phenotypic traits, but neither an indication of host local adaptation nor a cost of resistance. Infected populations have a higher gene diversity (Hs) than uninfected populations and Hs is strongly positively correlated with fitness. These results suggest a strong parasite effect on reducing population level inbreeding. We discuss how stochastic processes related to frequent extinction‐(re)colonization dynamics as well as host and parasite migration impede the evolution of resistance in the infected populations. We suggest that the genetic and phenotypic patterns of variation are a product of dynamic changes in the host gene pool caused by the interaction of colonization bottlenecks, inbreeding, immigration, hybrid vigor, rare host genotype advantage and parasitism. Our study highlights the effect of the parasite in ameliorating the negative fitness consequences caused by the high drift load in this metapopulation.     

Evidence for contemporary and historical gene flow between guppy populations in different watersheds,with a test for associations with adaptive traits

In dendritic river systems, gene flow is expected to occur primarily within watersheds. Yet, rare cross‐watershed transfers can also occur, whether mediated by (often historical) geological events or (often contemporary) human activities. We explored these events and their potential evolutionary consequences by analyzing patterns of neutral genetic variation (microsatellites) and adaptive phenotypic variation (male color) in wild guppies (Poecilia reticulata) distributed across two watersheds in northern Trinidad. We found the expected signatures of within‐watershed gene flow; yet we also inferred at least two instances of cross‐watershed gene flow—one in the upstream reaches and one further downstream. The upstream cross‐watershed event appears to be very recent (41 ± 13 years), suggesting dispersal via recent flooding or undocumented human‐mediated transport. The downstream cross‐watershed event appears to be considerably older (577 ± 265 years), suggesting a role for rare geological or climatological events. Alongside these strong signatures of both contemporary and historical gene flow, we found little evidence of impacts on presumably adaptive phenotypic differentiation, except perhaps in the one instance of very recent cross‐watershed gene flow. Selection in this system seems to overpower gene flow—at least on the spatiotemporal scales investigated here.