Environmental selection on transcriptome-derived SNPs in a high gene flow marine fish, the Atlantic herring (Clupea harengus)

High gene flow is considered the norm for most marine organisms and is expected to limit their ability to adapt to local environments. Few studies have directly compared the patterns of differentiation at neutral and selected gene loci in marine organisms. We analysed a transcriptome-derived panel of 281 SNPs in Atlantic herring (Clupea harengus), a highly migratory small pelagic fish, for elucidating neutral and selected genetic variation among populations and to identify candidate genes for environmental adaptation. We analysed 607 individuals from 18 spawning locations in the northeast Atlantic, including two temperature clines (5-12 °C) and two salinity clines (5-35‰). By combining genome scan and landscape genetic analyses, four genetically distinct groups of herring were identified: Baltic Sea, Baltic-North Sea transition area, North Sea/British Isles and North Atlantic; notably, samples exhibited divergent clustering patterns for neutral and selected loci. We found statistically strong evidence for divergent selection at 16 outlier loci on a global scale, and significant correlations with temperature and salinity at nine loci. On regional scales, we identified two outlier loci with parallel patterns across temperature clines and five loci associated with temperature in the North Sea/North Atlantic. Likewise, we found seven replicated outliers, of which five were significantly associated with low salinity across both salinity clines. Our results reveal a complex pattern of varying spatial genetic variation among outlier loci, likely reflecting adaptations to local environments. In addition to disclosing the fine scale of local adaptation in a highly vagile species, our data emphasize the need to preserve functionally important biodiversity.

High-resolution genetic analysis reveals extensive gene flow within the jellyfish Pelagia noctiluca (Scyphozoa) in the North Atlantic and Mediterranean Sea

Despite the importance of gelatinous zooplankton as components of marine ecosystems, both ecologically and socio-economically, relatively little is known about population persistence or connectivity in jellyfish. In the present study, we employed a combination of nuclear microsatellite markers and sequence data from the mitochondrial cytochrome oxidase I (COI) gene to determine levels and patterns of population genetic structuring in the holoplanktonic jellyfish Pelagia noctiluca across the northeast Atlantic Ocean and Mediterranean Sea. Our results indicate a high degree of connectivity in P. noctiluca, with little evidence of geographical structuring of genetic variation. A small but significant differentiation of Atlantic Ocean and Mediterranean stocks was detected based on the microsatellite data, but no evidence of differentiation was observed with the mtDNA, probably due to the higher power of the microsatellites to detect low levels of genetic structuring. Two clearly distinct groups of genotypes were observed within the mtDNA COI, which probably diverged in the early Pleistocene, but with no evidence of geographical structuring. Palaeodistribution modelling of P. noctiluca at the Last Glacial Maximum (LGM; ca. 21 KYA) indicated large areas of suitable habitat south of the species’ current-day distribution, with little reduction in area. The congruent evidence for minimal genetic differentiation from the nuclear microsatellites and the mtDNA, coupled with the results of the palaeodistribution modelling, supports the idea of long-term population stability and connectivity, thus providing key insights into the population dynamics and demography of this important species

Genetic structure of the lumpfish Cyclopterus lumpus across the North Atlantic

Lumpfish, or lumpsucker, Cyclopterus lumpus (Linnaeus, 1758) is widely distributed in the North Atlantic Ocean. It has a considerable economic value and substantial fisheries occur in several North Atlantic regions owing to the use of its fully ripe internal egg masses in the ovaries as an alternative to sturgeon caviar. Despite being intensively fished in several locations, biological knowledge is limited and no genetic structure information is available. In this study, the stock structure of C. lumpus was investigated across the North Atlantic using ten microsatellite loci. Out of ten loci, two exhibited higher level of differentiation but their inclusion/ exclusion from the analyses did not drastically change the observed genetic pattern. A total of three distinct genetic groups were detected: Maine-Canada-Greenland, Iceland-Norway and Baltic Sea. These results, discussed in terms of origin of differentiation, gene flow, and selection, showed that gene flow was rather limited among the detected groups, and also between Greenland and Maine-Canada.

Restricted gene flow in fragmented populations of a wind-pollinated tree

Fragmentation of natural populations can have negative effects at the genetic level, thus threatening their evolutionary potential. Many of the negative genetic impacts of population fragmentation can be ameliorated by gene flow and it has been suggested that in wind-pollinated tree species, high or even increased levels of gene flow are a feature of fragmented populations, although several studies have disputed this. We have used a combination of nuclear microsatellites and allele-specific PCR (AS-PCR) analysis of chloroplast single nucleotide polymorphisms (SNPs) to examine the levels and patterns of genetic diversity and population differentiation in fragmented populations of juniper (Juniperus communis) in Ireland and inform conservation programs for the species. Significant population differentiation was found for both chloroplast and nuclear markers, indicating restricted gene flow, particularly over larger geographic scales. For conservation purposes, the existence of genetically distinct clusters and geographically localised chloroplast haplotypes suggests that the concept of provenance should be taken into account when formulating augmentation or reintroduction strategies. Furthermore, the potential lack of seed dispersal and seedling establishment means that ex-situ approaches to seed and seedling management may have to be considered.

Extensive local-scale gene flow and long-term population stability in the intertidal mollusc Katharina tunicata (Mollusca: Polyplacophora)

The dispersal capabilities of intertidal organisms may represent a key factor to their survival in the face of global warming, as species that cannot adapt to the various effects of climate change will have to migrate to track suitable habitat. Although species with pelagic larval phases might be expected to have a greater capacity for dispersal than those with benthic larvae, interspecies comparisons have shown that this is not always the case. Consequently, population genetic approaches are being increasingly used to gain insights into dispersal through studying patterns of gene flow. In the present study, we used nuclear single-nucleotide polymorphisms (SNPs) and mitochondrial DNA (mtDNA) sequencing to elucidate fine-scale patterns of genetic variation between populations of the Black Katy Chiton, Katharina tunicata, separated by 15-150 km in south-west Vancouver Island. Both the nuclear and mitochondrial data sets revealed no genetic differentiation between the populations studied, and an isolation-with-migration analysis indicated extensive local-scale gene flow, suggesting an absence of barriers to dispersal. Population demographic analysis also revealed long-term population stability through previous periods of climate change associated with the Pleistocene glaciations. Together, the findings of the present study suggest that this high potential for dispersal may allow K. tunicata to respond to current global warming by tracking suitable habitat, consistent with its long-term demographic stability through previous changes in the Earth's climate. (C) 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 589597.

Genetic analyses reveal high levels of seed and pollen flow in hawthorn (Crataegus monogyna Jacq.), a key component of hedgerows

Hedgerows represent important components of agri-environment landscapes that are increasingly coming under threat from climate change, emergent diseases, invasive species and land use change. Given that population genetic data can be used to inform best-practice management strategies for woodland and hedgerow tree species, we carried out a study on hawthorn (Crataegus monogyna Jacq.), a key component of hedgerows, on a regional basis using a combination of nuclear and chloroplast microsatellite markers. We found that levels of genetic diversity were high and comparable to, or slightly higher than, other tree species from the same region. Levels of population differentiation for both sets of markers, however, were extremely low, suggesting extensive gene flow via both seed and pollen. These findings suggest that a holistic approach to woodland management, one which does not necessarily rely on the concept of “seed zones” previously suggested, but which also takes into account populations with high and/or rare chloroplast (i.e. seed-specific) genetic variation, might be the best approach to restocking and replanting.

Pleistocene glaciation events shape genetic structure across the range of the American lobster, Homarus americanus

A north/south discontinuity along the northeastern coast of North America in the genetic structure of the American lobster (Homarus americanus) was detected using a suite of 13 microsatellite loci assessed using spatial analyses. Population genetic data laid over existing data on physiographic changes and sea-surface temperatures were used to reconstruct the Pleistocene distribution of this species. A postglacial northern-edge colonization model best explains the relative genetic homogeneity of the northern region compared to the southern region centred in the Gulf of Maine. Population genetic analyses identified significant structure (range of standardized theta 0-0.02) but no significant evidence for isolation by distance. The novel application of spatial genetic analyses to a marine species allowed us to interpret these results by providing a greater insight into the evolutionary factors responsible for shaping the genetic structure of this species throughout is natural range.

Ecological coherence in marine reserve network design: an empirical evaluation of sequential site selection using genetic structure

Ecological coherence is a multifaceted conservation objective that includes some potentially conflicting concepts. These concepts include the extent to which the network maximises diversity (including genetic diversity) and the extent to which protected areas interact with non-reserve locations. To examine the consequences of different selection criteria, the preferred location to complement protected sites was examined using samples taken from four locations around each of two marine protected areas: Strangford Lough and Lough Hyne, Ireland. Three different measures of genetic distance were used: FST, Dest and a measure of allelic dissimilarity, along with a direct assessment of the total number of alleles in different candidate networks. Standardized site scores were used for comparisons across methods and selection criteria. The average score for Castlehaven, a site relatively close to Lough Hyne, was highest, implying that this site would capture the most genetic diversity while ensuring highest degree of interaction between protected and unprotected sites. Patterns around Strangford Lough were more ambiguous, potentially reflecting the weaker genetic structure around this protected area in comparison to Lough Hyne. Similar patterns were found across species with different dispersal capacities, indicating that methods based on genetic distance could be used to help maximise ecological coherence in reserve networks. ⺠Ecological coherence is a key component of marine protected area network design. ⺠Coherence contains a number of competing concepts. ⺠Genetic information from field populations can help guide assessments of coherence. ⺠Average choice across different concepts of coherence was consistent among species. ⺠Measures can be combined to compare the coherence of different network designs.

Lack of genetic structure and evidence for long-distance dispersal in ash (Fraxinus excelsior) populations under threat from an emergent fungal pathogen: implications for restorative planting

Genetic analysis on populations of European ash (Fraxinus excelsior) throughout Ireland was carried out to determine the levels and patterns of genetic diversity in naturally seeded trees in ash woodlands and hedgerows, with the aim of informing conservation and replanting strategies in the face of potential loss of trees as a result of ash dieback. Samples from 33 sites across Northern Ireland and three sites in the Republic of Ireland were genotyped for eight nuclear and ten chloroplast microsatellites. Levels of diversity were high (mean A R = 10.53; mean H O = 0.709; mean H E = 0.765) and were similar to those in Great Britain and continental Europe, whilst levels of population genetic differentiation based on nuclear microsatellites were extremely low (Φ ST = 0.0131). Levels of inbreeding (mean F IS = 0.067) were significantly lower than those reported for populations from Great Britain. Fine-scale analysis of seed dispersal indicated potential for dispersal over hundreds of metres. Our results suggest that ash woodlands across Ireland could be treated as a single management unit, and thus native material from anywhere in Ireland could be used as a source for replanting. In addition, high potential for dispersal has implications for recolonization processes post-ash dieback (Chalara fraxinea) infection, and could aid in our assessment of the capacity of ash to shift its range in response to global climate change.

A genomic island linked to ecotype divergence in Atlantic cod

The genomic architecture underlying ecological divergence and ecological speciation with gene flow is still largely unknown for most organisms. One central question is whether divergence is genome-wide or localized in 'genomic mosaics' during early stages when gene flow is still pronounced. Empirical work has so far been limited, and the relative impacts of gene flow and natural selection on genomic patterns have not been fully explored. Here, we use ecotypes of Atlantic cod to investigate genomic patterns of diversity and population differentiation in a natural system characterized by high gene flow and large effective population sizes, properties which theoretically could restrict divergence in local genomic regions. We identify a genomic region of strong population differentiation, extending over approximately 20 cM, between pairs of migratory and stationary ecotypes examined at two different localities. Furthermore, the region is characterized by markedly reduced levels of genetic diversity in migratory ecotype samples. The results highlight the genomic region, or 'genomic island', as potentially associated with ecological divergence and suggest the involvement of a selective sweep. Finally, we also confirm earlier findings of localized genomic differentiation in three other linkage groups associated with divergence among eastern Atlantic populations. Thus, although the underlying mechanisms are still unknown, the results suggest that 'genomic mosaics' of differentiation may even be found under high levels of gene flow and that marine fishes may provide insightful model systems for studying and identifying initial targets of selection during ecological divergence.

Evaluating genetic traceability methods for captive-bred marine fish and their applications in fisheries management and wildlife forensics

Growing demands for marine fish products is leading to increased pressure on already depleted wild populations and a rise in aquaculture production. Consequently, more captive-bred fish are released into the wild through accidental escape or deliberate releases. The increased mixing of captive-bred and wild fish may affect the ecological and/or genetic integrity of wild fish populations. Unambiguous identification tools for captive-bred fish will be highly valuable to manage risks (fisheries management) and tracing of escapees and seafood products (wildlife forensics). Using single nucleotide polymorphism (SNP) data from captive-bred and wild populations of Atlantic cod Gadus morhua L. and sole Solea solea L., we explored the efficiency of population and parentage assignment techniques for the identification and tracing of captive-bred fish. Simulated and empirical data were used to correct for stochastic genetic effects. Overall, parentage assignment performed well when a large effective population size characterized the broodstock and escapees originated from early generations of captive breeding. Consequently, parentage assignments are particularly useful from a fisheries management perspective to monitor the effects of deliberate releases of captive-bred fish on wild populations. Population assignment proved to be more efficient after several generations of captive breeding, which makes it a useful method in forensic applications for well-established aquaculture species. We suggest the implementation of a case-by-case strategy when choosing the best method.

Tracing early stages of species differentiation: Ecological, morphological and genetic divergence of Galapagos sea lion populations

Background: Oceans are high gene flow environments that are traditionally believed to hamper the build-up of genetic divergence. Despite this, divergence appears to occur occasionally at surprisingly small scales. The Galápagos archipelago provides an ideal opportunity to examine the evolutionary processes of local divergence in an isolated marine environment. Galápagos sea lions (Zalophus wollebaeki) are top predators in this unique setting and have an essentially unlimited dispersal capacity across the entire species range. In theory, this should oppose any genetic differentiation.
Results: We find significant ecological, morphological and genetic divergence between the western colonies and colonies from the central region of the archipelago that are exposed to different ecological conditions. Stable isotope analyses indicate that western animals use different food sources than those from the central area. This is likely due to niche partitioning with the second Galápagos eared seal species, the Galápagos fur seal (Arctocephalus galapagoensis) that exclusively dwells in the west. Stable isotope patterns correlate with significant differences in foraging-related skull morphology. Analyses of mitochondrial sequences as well as microsatellites reveal signs of initial genetic differentiation.
Conclusion: Our results suggest a key role of intra- as well as inter-specific niche segregation in the evolution of genetic structure among populations of a highly mobile species under conditions of free movement. Given the monophyletic arrival of the sea lions on the archipelago, our study challenges the view that geographical barriers are strictly needed for the build-up of genetic divergence. The study further raises the interesting prospect that in social, colonially breeding mammals additional forces, such as social structure or feeding traditions, might bear on the genetic partitioning of populations.

Spatial genetic structuring in a vagile species, the European wood mouse

We examined the genetic structure of natural populations of the European wood mouse Apodemus sylvaticus at the microgeographic ( 30 km) scales. Ecological and behavioural studies indicate that this species exhibits considerable dispersal relative to its home-range size. Thus, there is potential for high gene flow over larger geographic areas. As levels of population genetic structure are related to gene flow, we hypothesized that population genetic structuring at the microgeographic level should be negligible, increasing only with geographic distance. To test this, four sites were sampled within a microgeographic scale with two additional samples at the macrogeographic level. Individuals (n=415) were screened and analysed for seven polymorphic microsatellite loci. Contrary to our hypothesis, significant levels of population structuring were detected at both scales. Comparing genetic differentiation with geographic distance suggests increasing genetic isolation with distance. However, this distance effect was non-significant being confounded by surprisingly high levels of differentiation among microgeographic samples. We attribute this pattern of genetic differentiation to the effect of habitat fragmentation, splitting large populations into components with small effective population sizes resulting in enhanced genetic drift. Our results indicate that it is incorrect to assume genetic homogeneity among populations even where there is no evidence of physical barriers and dispersal can occur freely. In the case of A. sylvaticus, it is not clear whether dispersal does not occur across habitat barriers or behavioural dispersal occurs without consequent gene flow.