Climate Change and Genetic Structure of Leading Edge and Rear End Populations in a Northwards Shifting Marine Fish Species,the Corkwing Wrasse (Symphodus melops)

One mechanism by which marine organisms may respond to climate shifts is range shifts. The corkwing wrasse (Symphodus melops) is a temperate fish species, inhabiting the coasts of Europe, that show strong indications of current as well as historical (ice-age) range shifts towards the north. Nine neutral microsatellite DNA markers were screened to study genetic signatures and spatial population structure over the entire geographic and thermal gradient of the species from Portugal to Norway. A major genetic break (F _ST  = 0.159 average among pairs) was identified between Scandinavian and more southern populations, with a marked reduction (30% or more) in levels of genetic variability in Scandinavia. The break is probably related to bottleneck(s) associated with post-glacial colonization of the Scandinavian coasts, and indicates a lack of present gene flow across the North Sea. The lack of gene flow can most likely be attributed to the species’ need for rocky substrate for nesting and a relatively short pelagic larval phase, limiting dispersal by ocean currents. These findings demonstrate that long-distance dispersal may be severely limited in the corkwing wrasse, and that successful range-shifts following present climate change may be problematic for this and other species with limited dispersal abilities, even in the seemingly continuous marine environment.     

Impact of harvesting cleaner fish for salmonid aquaculture assessed from replicated coastal marine protected areas

Wrasse (Labridae) fisheries have increased markedly in Norway since 2010. Wrasse are being used as cleaner fish in salmonid aquaculture to control sea-lice infestations. However, fundamental knowledge on the demography and abundance of the targeted wrasse populations in Norwegian waters is lacking, and the consequences of harvesting at the current intensity have not been assessed. Here, we compared catch per unit effort (CPUE), size, age and sex ratio of goldsinny wrasse (Ctenolabrus rupestris) and corkwing wrasse (Symphodus melops) between marine protected areas (MPAs) and control areas open for fishing at four localities on the Skagerrak coast in Southern Norway. The CPUE of goldsinny larger than the minimum size limit was 33–65% higher within MPAs, while for corkwing three of four MPAs had higher CPUE with the relative difference between MPAs and control areas ranging from ?16% to 92%. Moreover, corkwing, but not goldsinny, was significantly older and larger within MPAs than in control areas. Sex ratios did not differ between MPAs and control areas for either species. Our study suggests that despite its short history, the wrasse fisheries have considerable impacts on the target populations and, further, that small MPAs hold promise as a management tool for maintaining natural population sizes and size structure. Goldsinny, being a smaller-sized species, also seems to benefit from the traditional minimum size limit management tool, which applies outside MPAs.     

Characterization of strains of Vibrio splendidus and V. tapetis isolated from corkwing wrasse Symphodus melops suffering vibriosis

Two vibrio bacteria pathogenic to the corkwing wrasse Symphodus melops were isolated. Vibriosis-inducing strain LP1 was isolated as the dominanting bacterium in kidney samples of dead and moribund wrasse from a population suffering vibriosis and high daily mortality in 1998 on the Norwegian west coast. The other vibriosis-inducing strain, LP2, was isolated from wrasse captured the following year. Re-infection experiments have confirmed that these strains cause vibriosis in corkwing wrasse. Both strains were typical vibrios sharing the traits of fermentative Gram-negative curved rods with motility and a positive oxidase reaction. Detailed biochemical and genetic characterisation revealed a close affiliation to known species of the marine environment. The first isolate, LP1, is a form of the ubiquitous seawater organism Vibrio splendidus, while the second isolate, LP2, is closely related to V. tapetis (previously only known as the brown ring disease agent in clams). Identification of the new wrasse pathogens V. splendidus LP1 and V. tapetis LP2 is facilitated by break points observed in this study.     

Disentangling the effects of recombination,selection, and demography on the genetic variation at a major histocompatibility complex class II gene in the alpine chamois

The major histocompatibility complex (MHC) harbours some of the most polymorphic loci in vertebrate genomes. MHC genes are thought to be subject to some form of balancing selection, most likely pathogen‐mediated selection. Hence, MHC genes are excellent candidates for exploring adaptive processes. In this study, we investigated the genetic variation at exon 2 of the DRB class II MHC locus in 191 alpine chamois (Rupicapra rupicapra) from 10 populations in the eastern Alps of Italy. In particular, we were interested in distinguishing and estimating the relative impact of selective and demographic factors, while taking into account the confounding effect of recombination. The extremely high d_n/d_s ratio and the presence of trans‐species polymorphisms suggest that a strong long‐term balancing selection effect has been operating at this locus throughout the evolutionary history of this species. We analysed patterns of genetic variation within and between populations, and the mitochondrial D‐loop polymorphism patterns were analysed to provide a baseline indicator of the effects of demographic processes. These analyses showed that (i) the chamois experienced a demographic decline in the last 5000–30 000 years, most likely related to the postglacial elevation in temperature; (ii) this demographic process can explain the results of neutrality tests applied to MHC variation within populations, but cannot justify the much weaker divergence between populations implied by MHC as opposed to mitochondrial DNA; (iii) similar sets of divergent alleles are probably maintained with similar frequencies by balancing selection in different populations, and this mechanism is also operating in small isolated populations, which are strongly affected by drift.     

Lack of gene flow: Narrow and dispersed differentiation islands in a triplet of Leptidea butterfly species

Genome scans in recently separated species can inform on molecular mechanisms and evolutionary processes driving divergence. Large‐scale polymorphism data from multiple species pairs are also key to investigate the repeatability of divergence—whether radiations tend to show parallel responses to similar selection pressures and/or underlying molecular forces. Here, we used whole‐genome resequencing data from six wood white (Leptidea sp.) butterfly populations, representing three closely related species with karyomorph variation, to infer the species' demographic history and characterize patterns of genomic diversity and differentiation. The analyses supported previously established species relationships, and there was no evidence for postdivergence gene flow. We identified significant intraspecific genetic structure, in particular between karyomorph extremes in the wood white (L. sinapis)—a species with a remarkable chromosome number cline across the distribution range. The genomic landscapes of differentiation were erratic, and outlier regions were narrow and dispersed. Highly differentiated (F_ST) regions generally had low genetic diversity (θ_π), but increased absolute divergence (D_XY) and excess of rare frequency variants (low Tajima's D). A minority of differentiation peaks were shared across species and population comparisons. However, highly differentiated regions contained genes with overrepresented functions related to metabolism, response to stimulus and cellular processes, indicating recurrent directional selection on a specific set of traits in all comparisons. In contrast to the majority of genome scans in recently diverged lineages, our data suggest that divergence landscapes in Leptidea have been shaped by directional selection and genetic drift rather than stable recombination landscapes and/or introgression.     

A continuous genome assembly of the corkwing wrasse (Symphodus melops)

The wrasses (Labridae) are one of the most successful and species-rich families of the Perciformes order of teleost fish. Its members display great morphological diversity, and occupy distinct trophic levels in coastal waters and coral reefs. The cleaning behaviour displayed by some wrasses, such as corkwing wrasse (Symphodus melops), is of particular interest for the salmon aquaculture industry to combat and control sea lice infestation as an alternative to chemicals and pharmaceuticals. There are still few genome assemblies available within this fish family for comparative and functional studies, despite the rapid increase in genome resources generated during the past years. Here, we present a highly continuous genome assembly of the corkwing wrasse using PacBio SMRT sequencing (x28.8) followed by error correction with paired-end Illumina data (x132.9). The present genome assembly consists of 5040 contigs (N50?=?461,652?bp) and a total size of 614 Mbp, of which 8.5% of the genome sequence encode known repeated elements. The genome assembly covers 94.21% of highly conserved genes across ray-finned fish species. We find evidence for increased copy numbers specific for corkwing wrasse possibly highlighting diversification and adaptive processes in gene families including N-linked glycosylation (ST8SIA6) and stress response kinases (HIPK1). By comparative analyses, we discover that de novo repeats, often not properly investigated during genome annotation, encode hundreds of immune-related genes. This new genomic resource, together with the ballan wrasse (Labrus bergylta), will allow for in-depth comparative genomics as well as population genetic analyses for the understudied wrasses.     

Divergence genetics analysis reveals historical population genetic processes leading to contrasting phylogeographic patterns in co-distributed species

Coalescent samplers are computational time machines for inferring the historical demographic genetic processes that have given rise to observable patterns of spatial genetic variation among contemporary populations. We have used traditional characterizations of population structure and coalescent‐based inferences about demographic processes to reconstruct the population histories of two co‐distributed marine species, the frilled dog whelk, Nucella lamellosa, and the bat star, Patiria miniata. Analyses of population structure were consistent with previous work in both species except that additional samples of N. lamellosa showed a larger regional genetic break on Vancouver Island (VI) rather than between the southern Alexander Archipelago as in P. miniata. Our understanding of the causes, rather than just the patterns, of spatial genetic variation was dramatically improved by coalescent analyses that emphasized variation in population divergence times. Overall, gene flow was greater in bat stars (planktonic development) than snails (benthic development) but spatially homogeneous within species. In both species, these large phylogeographic breaks corresponded to relatively ancient divergence times between populations rather than regionally restricted gene flow. Although only N. lamellosa shows a large break on VI, population separation times on VI are congruent between species, suggesting a similar response to late Pleistocene ice sheet expansion. The absence of a phylogeographic break in P. miniata on VI can be attributed to greater gene flow and larger effective population size in this species. Such insights put the relative significance of gene flow into a more comprehensive historical biogeographic context and have important implications for conservation and landscape genetic studies that emphasize the role of contemporary gene flow and connectivity in shaping patterns of population differentiation.     

Post-settlement emigration affects mortality estimates for two Bahamian wrasses

Understanding the dynamics of open marine populations is inherently complex, and this complexity has led to decades of debate regarding the relative importance of pre- versus post-settlement processes in structuring these populations. Movement between patches may be an important modifier of patterns established at settlement, yet local immigration and emigration have received less attention than other demographic rates. I examined loss rates from tagged populations of juvenile wrasses (yellowhead wrasse Halichoeres garnoti and bluehead wrasse Thalassoma bifasciatum) at two sites in the Bahamas. Assuming that all losses were due solely to mortality would have significantly underestimated survivorship of yellowhead wrasse by 29% and bluehead wrasse by 14%. On average, per capita mortality and emigration rates were higher for yellowhead than bluehead wrasse, but neither demographic rate differed between sites for either species. With respect to within-species density, bluehead wrasse mortality was density-dependent at the patch reef site, but mortality rates of yellowhead wrasse were consistently density-independent. Evaluating the effects of between-species density, yellowhead wrasse mortality increased with a decrease in bluehead wrasse density, but this effect was limited to the patch reef site. Emigration rates were not a function of either within-species or between-species density, but instead varied inversely with isolation distance. Numerous previous studies of coral-reef fish, conducted on patch reefs separated by only a few meters of sand and often using untagged fish, may have confounded losses due to emigration with those due to mortality. A better understanding of the factors affecting emigration in marine fishes is important to their effective management using spatial tools such as marine protected areas.     

Gene flow in the anemone Anthopleura elegantissima limits signatures of local adaptation across an extensive geographic range

Species inhabiting marine environments face a wide range of environmental conditions that vary spatially across several orders of magnitude. The selective pressures that these conditions impose on marine organisms, in combination with potentially high rates of gene flow between distant populations, make it difficult to predict the extent to which these populations can locally adapt. Here, I identify how selection and gene flow influence the population genetic structure of the anemone Anthopleura elegantissima along the Pacific coast of North America. Isolation by distance is the dominant pattern across the range of this species, with a genetic break near Pt. Conception, CA. Furthermore, demographic modelling suggests that this species was historically confined to southerly latitudes before expanding northward. Outlier analyses identify 24 loci under selection (out of ~1,100), but the same analysis on simulated genetic data generated using the most likely demographic model erroneously identified the same number of loci under selection, if not more. Taken together, these results suggest that demographic processes are the dominant force shaping population genetic patterns in A. elegantissima along the Pacific coast of North America. I discuss these patterns in terms of the evolutionary history of A. elegantissima, the potential for local adaptation, and their consequences with respect to interactions with the endosymbiont Breviolum muscatinei across their geographic range.     

Extraordinarily rapid life-history divergence between Cryptasterina sea star species

Life history plays a critical role in governing microevolutionary processes such as gene flow and adaptation, as well as macroevolutionary processes such speciation. Here, we use multilocus phylogeographic analyses to examine a speciation event involving spectacular life-history differences between sister species of sea stars. Cryptasterina hystera has evolved a suite of derived life-history traits (including internal self-fertilization and brood protection) that differ from its sister species Cryptasterina pentagona, a gonochoric broadcast spawner. We show that these species have only been reproductively isolated for approximately 6000 years (95% highest posterior density of 905-22 628), and that this life-history change may be responsible for dramatic genetic consequences, including low nucleotide diversity, zero heterozygosity and no gene flow. The rapid divergence of these species rules out some mechanisms of isolation such as adaptation to microhabitats in sympatry, or slow divergence by genetic drift during prolonged isolation. We hypothesize that the large phenotypic differences between species relative to the short divergence time suggests that the life-history differences observed may be direct responses to disruptive selection between populations. We speculate that local environmental or demographic differences at the southern range margin are possible mechanisms of selection driving one of the fastest known marine speciation events.     

Quantifying population structure on short timescales

Quantifying the contribution of the various processes that influence population genetic structure is important, but difficult. One of the reasons is that no single measure appropriately quantifies all aspects of genetic structure. An increasing number of studies is analysing population structure using the statistic D, which measures genetic differentiation, next to G_ST, which quantifies the standardized variance in allele frequencies among populations. Few studies have evaluated which statistic is most appropriate in particular situations. In this study, we evaluated which index is more suitable in quantifying postglacial divergence between three‐spined stickleback (Gasterosteus aculeatus) populations from Western Europe. Population structure on this short timescale (10 000 generations) is probably shaped by colonization history, followed by migration and drift. Using microsatellite markers and anticipating that D and G_ST might have different capacities to reveal these processes, we evaluated population structure at two levels: (i) between lowland and upland populations, aiming to infer historical processes; and (ii) among upland populations, aiming to quantify contemporary processes. In the first case, only D revealed clear clusters of populations, putatively indicative of population ancestry. In the second case, only G_ST was indicative for the balance between migration and drift. Simulations of colonization and subsequent divergence in a hierarchical stepping stone model confirmed this discrepancy, which becomes particularly strong for markers with moderate to high mutation rates. We conclude that on short timescales, and across strong clines in population size and connectivity, D is useful to infer colonization history, whereas G_ST is sensitive to more recent demographic events.     

Genetic Structure Among 50 Species of the Northeastern Pacific Rocky Intertidal Community

Comparing many species'' population genetic patterns across the same seascape can identify species with different levels of structure, and suggest hypotheses about the processes that cause such variation for species in the same ecosystem. This comparative approach helps focus on geographic barriers and selective or demographic processes that define genetic connectivity on an ecosystem scale, the understanding of which is particularly important for large-scale management efforts. Moreover, a multispecies dataset has great statistical advantages over single-species studies, lending explanatory power in an effort to uncover the mechanisms driving population structure. Here, we analyze a 50-species dataset of Pacific nearshore invertebrates with the aim of discovering the most influential structuring factors along the Pacific coast of North America. We collected cytochrome c oxidase I (COI) mtDNA data from populations of 34 species of marine invertebrates sampled coarsely at four coastal locations in California, Oregon, and Alaska, and added published data from 16 additional species. All nine species with non-pelagic development have strong genetic structure. For the 41 species with pelagic development, 13 show significant genetic differentiation, nine of which show striking F_ST levels of 0.1–0.6. Finer scale geographic investigations show unexpected regional patterns of genetic change near Cape Mendocino in northern California for five of the six species tested. The region between Oregon and Alaska is a second focus of intraspecific genetic change, showing differentiation in half the species tested. Across regions, strong genetic subdivision occurs more often than expected in mid-to-high intertidal species, a result that may reflect reduced gene flow due to natural selection along coastal environmental gradients. Finally, the results highlight the importance of making primary research accessible to policymakers, as unexpected barriers to marine dispersal break the coast into separate demographic zones that may require their own management plans.     

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.     

Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds

Successful urban colonization by formerly rural species represents an ideal situation in which to study adaptation to novel environments. We address this issue using candidate genes for behavioural traits that are expected to play a role in such colonization events. We identified and genotyped 16 polymorphisms in candidate genes for circadian rhythms, harm avoidance and migratory and exploratory behaviour in 12 paired urban and rural populations of the blackbird Turdus merula across the Western Palaearctic. An exonic microsatellite in the SERT gene, a candidate gene for harm avoidance behaviour, exhibited a highly significant association with habitat type in an analysis conducted across all populations. Genetic divergence at this locus was consistent in 10 of the 12 population pairs; this contrasts with previously reported stochastic genetic divergence between these populations at random markers. Our results indicate that behavioural traits related to harm avoidance and associated with the SERT polymorphism experience selection pressures during most blackbird urbanization events. These events thus appear to be influenced by homogeneous adaptive processes in addition to previously reported demographic founder events.     

Cryptic biodiversity and phylogeographical patterns in a snapping shrimp species complex

Recent investigations suggest that marine biodiversity may be much higher than earlier estimates, and an important hidden source of diversity in marine systems is the phenomenon of cryptic species complexes. Such complexes are informative models for research into the evolutionary processes that govern species compositions of marine fauna. The snapping shrimp genera Alpheus and Synalpheus are known to harbour large numbers of cryptic species; here, I characterize the genetic structure of the Alpheus armillatus species complex in the northern Caribbean, west Atlantic, and Gulf of Mexico using mitochondrial and nuclear sequence data. Over this geographical region, the complex harbours at least three lineages that are probable reproductively isolated species; all major lineages diverged subsequent to the close of the Isthmus of Panama. Only one lineage was present in the Gulf of Mexico, whereas outside the Gulf of Mexico there was no clear tendency for lineage dominance by geographical region, as most sites were populated by shrimp from at least two lineages. However, within each lineage, there was strong evidence of population genetic differentiation between geographical regions. All lineages showed strong signals of demographic expansion, and one lineage showed sharply reduced genetic diversity, suggestive of past population bottlenecks or recently founded populations with low gene flow from other sites. These results show that evolutionary processes leading to divergence and speciation have been common and recent in the snapping shrimp, and suggest that connectivity among shrimp populations may be limited.     

Divergent selection and drift shape the genomes of two avian sister species spanning a saline–freshwater ecotone

The role of species divergence due to ecologically based divergent selection—or ecological speciation—in generating and maintaining biodiversity is a central question in evolutionary biology. Comparison of the genomes of phylogenetically related taxa spanning a selective habitat gradient enables discovery of divergent signatures of selection and thereby provides valuable insight into the role of divergent ecological selection in speciation. Tidal marsh ecosystems provide tractable opportunities for studying organisms' adaptations to selective pressures that underlie ecological divergence. Sharp environmental gradients across the saline–freshwater ecotone within tidal marshes present extreme adaptive challenges to terrestrial vertebrates. Here, we sequence 20 whole genomes of two avian sister species endemic to tidal marshes—the saltmarsh sparrow (Ammospiza caudacutus) and Nelson's sparrow (A. nelsoni)—to evaluate the influence of selective and demographic processes in shaping genome‐wide patterns of divergence. Genome‐wide divergence between these two recently diverged sister species was notably high (genome‐wide F_ST = 0.32). Against a background of high genome‐wide divergence, regions of elevated divergence were widespread throughout the genome, as opposed to focused within islands of differentiation. These patterns may be the result of genetic drift resulting from past tidal march colonization events in conjunction with divergent selection to different environments. We identified several candidate genes that exhibited elevated divergence between saltmarsh and Nelson's sparrows, including genes linked to osmotic regulation, circadian rhythm, and plumage melanism—all putative candidates linked to adaptation to tidal marsh environments. These findings provide new insights into the roles of divergent selection and genetic drift in generating and maintaining biodiversity.     

The influence of stochastic and selective forces in the population divergence of female colour polymorphism in damselflies of the genus Ischnura

Disentangling the relative importance and potential interactions of selection and genetic drift in driving phenotypic divergence of species is a classical research topic in population genetics and evolutionary biology. Here, we evaluate the role of stochastic and selective forces on population divergence of a colour polymorphism in seven damselfly species of the genus Ischnura, with a particular focus on I. elegans and I. graellsii. Colour-morph frequencies in Spanish I. elegans populations varied greatly, even at a local scale, whereas more similar frequencies were found among populations in eastern Europe. In contrast, I. graellsii and the other five Ischnura species showed little variation in colour-morph frequencies between populations. F(ST)-outlier analyses revealed that the colour locus deviated strongly from neutral expectations in Spanish populations of I. elegans, contrasting the pattern found in eastern European populations, and in I. graellsii, where no such discrepancy between morph divergence and neutral divergence could be detected. This suggests that divergent selection has been operating on the colour locus in Spanish populations of I. elegans, whereas processes such as genetic drift, possibly in combination with other forms of selection (such as negative frequency-dependent selection), appear to have been present in other regions, such as eastern Europe. Overall, the results indicate that both selective and stochastic processes operate on these colour polymorphisms, and suggest that the relative importance of factors varies between geographical regions.     

Genomics of invasion: diversity and selection in introduced populations of monkeyflowers (Mimulus guttatus)

Global trade and travel is irreversibly changing the distribution of species around the world. Because introduced species experience drastic demographic events during colonization and often face novel environmental challenges from their native range, introduced populations may undergo rapid evolutionary change. Genomic studies provide the opportunity to investigate the extent to which demographic, historical and selective processes shape the genomic structure of introduced populations by analysing the signature that these processes leave on genomic variation. Here, we use next‐generation sequencing to compare genome‐wide relationships and patterns of diversity in native and introduced populations of the yellow monkeyflower (Mimulus guttatus). Genome resequencing data from 10 introduced populations from the United Kingdom (UK) and 12 native M. guttatus populations in North America (NA) demonstrated reduced neutral genetic diversity in the introduced range and showed that UK populations are derived from a geographic region around the North Pacific. A selective‐sweep analysis revealed site frequency changes consistent with selection on five of 14 chromosomes, with genes in these regions showing reduced silent site diversity. While the target of selection is unknown, genes associated with flowering time and biotic and abiotic stresses were located within the swept regions. The future identification of the specific source of origin of introduced UK populations will help determining whether the observed selective sweeps can be traced to unsampled native populations or occurred since dispersal across the Atlantic. Our study demonstrates the general potential of genome‐wide analyses to uncover a range of evolutionary processes affecting invasive populations.