Article

Genomic evidence of hybridization between two independent invasions of European green crab (Carcinus maenas) in the Northwest Atlantic

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Abstract

Invasive species have been associated with significant negative impacts in their introduced range often outcompeting native species, yet the long-term evolutionary dynamics of biological invasions are not well understood. Hybridization, either among waves of invasion or between native and introduced populations, could alter the ecological and evolutionary impacts of invasions yet has rarely been studied in marine invasive species. The European green crab (Carcinus maenas) invaded eastern North America twice from northern and southern locations in its native range. Here we examine the frequency of hybridization among these two distinct invasions at locations from New Jersey, USA to Newfoundland, Canada using restriction-site-associated DNA sequencing (RAD-seq), microsatellite loci and cytochrome c oxidase subunit I mitochondrial DNA (mtDNA) sequences. We used Bayesian clustering and hybrid assignment analyses to investigate hybridization between the northern and southern populations. Of the samples analyzed, six locations contained at least one hybrid individual, while two locations were characterized by extensive hybridization, with 95% of individuals collected from Placentia Bay, Newfoundland being hybrids (mostly F2) and 90% of individuals from Kejimkujik, Nova Scotia being classified as hybrids, mostly backcrosses to the northern ecotype. The presence of both F2 hybrids and backcrossed individuals suggests that these hybrids are viable and introgression is occurring between invasions. Our results provide insight into the demographic and evolutionary consequences of hybridization between independent invasions, and will inform the management of green crabs in eastern North America.

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... Based on physiological evidence from Tepolt and Somero (2014), we predict that seasonal temperature minima are limiting the range expansion of the invasive green crab ecotypes and that environmentally-associated genomic regions will track a steep cline in temperature previously reported in Atlantic Canada. This work builds directly on previous studies highlighting the genomic differences (Tepolt and Palumbi 2015;Jeffery et al. 2017b) and subsequent hybridization of two independent waves of invasion (Darling et al. 2014;Jeffery et al. 2017a) to better understand the environmental correlates of population specific invasion success and secondary contact in this species. Our results will provide insight into how secondary contact dynamics can be correlated with environmental heterogeneity potentially constraining the success of coastal marine invaders, and will help to understand and predict future range expansions and contractions of green crab ecotypes. ...
... This method detects correlations between environmental variables and genotypic variation to reveal outliers, while controlling for population structure (K) and unmeasured environmental variables as latent factors. We set K=2 based on the results of previous discriminant analyses of principal components (DAPC) and STRUCTURE (Pritchard, Stephens, and Donnelly 2000) results (Jeffery et al. 2017a;Jeffery et al. 2017b). LFMM was run with a burn-in of 5000 iterations and 15,000 Markov Chain Monte Carlo (MCMC) iterations which were replicated five times. ...
... It is this cold seasonal temperature that likely constrains the range and gene flow of two genetically distinct invasions, showing an abrupt break in population structure within their northwestern Atlantic range, except for a zone of secondary contact in southern Nova Scotia. The broad-scale environmental correlations observed in the present study are most likely carried over from structure in the native range, as both our outlier and non-outlier loci showed similar relationships to temperature, potentially reflective of the long-term divergence between ecotypes in Europe (Jeffery et al. 2017a). Because the observed environmental associations are present both in outlier and non-outlier loci (although to a lesser extent), a simplistic interpretation of the factors responsible for these associations remains elusive. ...
Article
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Genetic-environment associations are increasingly revealed through population genomic data and can occur through a number of processes, including secondary contact, divergent natural selection, or isolation-by-distance. Here we investigate the influence of the environment, including seasonal temperature and salinity, on the population structure of the invasive European green crab (Carcinus maenas) in eastern North America. Green crab populations in eastern North America are associated with two independent invasions, previously shown to consist of distinct northern and southern ecotypes, with a contact zone in southern Nova Scotia, Canada. Using a RAD-seq panel of 9137 genome-wide SNPs, we detected 41 SNPs (0.49%) whose allele frequencies were highly correlated with environmental data. A principal components analysis of 25 environmental variables differentiated populations into northern, southern, and admixed sites in concordance with the observed genomic spatial structure. Furthermore, a spatial principal components analysis conducted on genomic and geographic data revealed a high degree of global structure (p<0.0001) partitioning a northern and southern ecotype. Redundancy and partial redundancy analyses revealed that among the environmental variables tested, winter sea surface temperature had the strongest association with spatial structuring, suggesting that it is an important factor defining range and expansion limits of each ecotype. Understanding environmental thresholds associated with intraspecific diversity will facilitate the ability to manage current and predict future distributions of this aquatic invasive species.
... Over the last two decades, this northern lineage has subsequently spread through NS and New Brunswick (NB) and has made secondary contact with the original southern introduction. As a result, hybridization between the lineages has occurred in these areas resulting in latitudinal genetic clines (Pringle et al., 2011;Darling et al., 2014;Jeffery et al., 2017a). Additionally, anthropogenic transport of individuals from the zone of secondary contact has resulted in a recent introduction of admixed individuals in southeastern Newfoundland (NL) (Blakeslee et al., 2010). ...
... In this system, we take advantage of the strong genetic differentiation between lineages from the past and recent introductions, and the interaction of invasion fronts, as a platform to examine dynamics in the hybrid zone and study the temporal changes in the genetic clines. Such investigations are possible because the clinal genetic structure of C. maenas in eastern North America has been well characterized in previous studies (Pringle et al., 2011;Darling et al., 2014;Jeffery et al., 2017a), allowing for a historical perspective and thus the ability to investigate temporal dynamics. Previous studies exploring C. maenas genetic structure between 1999 and 2007 documented a southward progression of the genetic clines (Pringle et al., 2011;Darling et al., 2014), consistent with the predominant southward circulation on the eastern Scotian Shelf (DFO, 2003;Wu, Tang, & Hannah, 2012) and the broad dispersal potential of larval C. maenas, which can remain in the water column for >50 days (Behrens Yamada et al., 2005;Klassen & Locke, 2007;Pringle et al., 2011). ...
... Here, we examine the distribution patterns of C. maenas lineages in eastern North America from New Jersey, US, to western NL, Canada (~39-49°N) between 2011 and 2015 and compare to previous studies. We used single nucleotide polymorphisms (SNPs) selected to discriminate between northern and southern lineages, building directly on previous studies of population structure using SNPs (Jeffery et al., 2017a;Jeffery et al., 2017b) by expanding the scale of sampling, both in number of samples and by life stage (juveniles and adults). In addition, to evaluate the temporal progression of the clines, we incorporated genetic data collected over several time points from 2000 to 2015 from both mitochondrial and microsatellite markers. ...
Article
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Two genetically distinct lineages of European green crabs (Carcinus maenas) were independently introduced to eastern North America, the first in the early 19th century and the second in the late 20th century. These lineages first came into secondary contact in southeastern Nova Scotia, Canada (NS), where they hybridized, producing latitudinal genetic clines. Previous studies have documented a persistent southward shift in the clines of different marker types, consistent with existing dispersal and recruitment pathways. We evaluated current clinal structure by quantifying the distribution of lineages and fine‐scale hybridization patterns across the eastern North American range (25 locations, ~39‐49°N) using informative single nucleotide polymorphisms (SNPs; n=96). In addition, temporal changes in the genetic clines were evaluated using mitochondrial DNA and microsatellite loci (n=9‐11) over a 15‐year period (2000‐2015). Clinal structure was consistent with prior work demonstrating the existence of both northern and southern lineages with a hybrid zone occurring between southern New Brunswick (NB) and southern NS. Extensive later generation hybrids were detected in this region and in southeastern Newfoundland. Temporal genetic analysis confirmed the southward progression of clines over time; however, the rate of this progression was slower than predicted by forecasting models, and current clines for all marker types deviated significantly from these predictions. Our results suggest that neutral and selective processes contribute to cline dynamics, and ultimately, highlight how selection, hybridization, and dispersal can collectively influence invasion success. This article is protected by copyright. All rights reserved.
... Often the status of non-native taxa is defined by geographical isolation rather than specific evidence of reproductive isolation. The observation of fast introgression and genetic swamping (as in the aforementioned Hawaiian sergeant major damselfishes [30] and green crab ecotypes [44]) would indicate that there is minimal reproductive isolation and thus admixture proceeds largely unimpeded for these species. ...
... In general, postzygotic barriers are expected to scale with species divergence [50], as illustrated by Tigriopus copepods [51] or Strongylocentrotus sea urchins [52]. In line with this expectation, reproductive isolation is substantial between C. robusta and C. intestinalis (Box 1) and similarly high between M. galloprovincilis and M. trossulus (divergence time of 3.5 MY, Box 2), whereas reproductive isolation is negligible for taxa with recent divergence times (e.g., M. galloprovincialis X M. planulatus [53]; damselfish in Hawaii [30]; green crabs [44]), and intermediate between M. galloprovincialis and M. edulis with a mixture of heterosis and hybrid breakdown due to multigenic interactions [9] (divergence time of ~2.5 MY [38]). In the context of marine anthropogenic hybridization, the observations made in Ciona spp. ...
... Similar questions are raised with invasive species management, as illustrated by recent studies of the invasive green crab Carcinus maenas. Two lineages, geographically separated in the native range and both introduced in North East America, were shown to be genome-wide divergent and to hybridize [44]. Introgression occurred in a few locations, suggesting some reproductive isolation mechanisms at play between so-called "ecotypes" [44], which may differ by their ecology (e.g., winter sea water temperature preferences), therefore questioning that they will spread more or less [44,62]. ...
Preprint
Species introductions promote secondary contacts between taxa with long histories of allopatric divergence. Anthropogenic contact zones thus offer valuable contrasts to speciation studies in natural systems where past spatial isolations may have been brief or intermittent. Investigations of anthropogenic hybridization are rare for marine animals, which have high fecundity and high dispersal ability, characteristics that contrast to most terrestrial animals. Genomic studies indicate that gene flow can still occur after millions of years of divergence, as illustrated by invasive mussels and tunicates. In this context, we highlight three issues: 1) the effects of high propagule pressure and demographic asymmetries on introgression directionality, 2) the role of hybridization in preventing introduced species spread, and 3) the importance of postzygotic barriers in maintaining reproductive isolation. Anthropogenic contact zones offer evolutionary biologists unprecedented large scale hybridization experiments. In addition to breaking the highly effective reproductive isolating barrier of spatial segregation, they allow researchers to explore unusual demographic contexts with strong asymmetries. The outcomes are diverse from introgression swamping to strong barriers to gene flow, and lead to local containment or widespread invasion. These outcomes should not be neglected in management policies of marine invasive species.
... Often the status of non-native taxa is defined by geographical isolation rather than specific evidence of reproductive isolation. The observation of fast introgression and genetic swamping (as in the aforementioned Hawaiian sergeant major damselfishes [30] and green crab ecotypes [44]) would indicate that there is minimal reproductive isolation and thus admixture proceeds largely unimpeded for these species. ...
... In general, postzygotic barriers are expected to scale with species divergence [50], as illustrated by Tigriopus copepods [51] or Strongylocentrotus sea urchins [52]. In line with this expectation, reproductive isolation is substantial between C. robusta and C. intestinalis (Box 1) and similarly high between M. galloprovincilis and M. trossulus (divergence time of 3.5 MY, Box 2), whereas reproductive isolation is negligible for taxa with recent divergence times (e.g., M. galloprovincialis X M. planulatus [53]; damselfish in Hawaii [30]; green crabs [44]), and intermediate between M. galloprovincialis and M. edulis with a mixture of heterosis and hybrid breakdown due to multigenic interactions [9] (divergence time of ~2.5 MY [38]). In the context of marine anthropogenic hybridization, the observations made in Ciona spp. ...
... Similar questions are raised with invasive species management, as illustrated by recent studies of the invasive green crab Carcinus maenas. Two lineages, geographically separated in the native range and both introduced in North East America, were shown to be genome-wide divergent and to hybridize [44]. Introgression occurred in a few locations, suggesting some reproductive isolation mechanisms at play between so-called "ecotypes" [44], which may differ by their ecology (e.g., winter sea water temperature preferences), therefore questioning that they will spread more or less [44,62]. ...
Article
Species introductions promote secondary contacts between taxa with long histories of allopatric divergence. Anthropogenic contact zones thus offer valuable contrasts to speciation studies in natural systems where past spatial isolations may have been brief or intermittent. Investigations of anthropogenic hybridization are rare for marine animals, which have high fecundity and high dispersal ability, characteristics that contrast to most terrestrial animals. Genomic studies indicate that gene flow can still occur after millions of years of divergence, as illustrated by invasive mussels and tunicates. In this context, we highlight three issues: (i) the effects of high propagule pressure and demographic asymmetries on introgression directionality, (ii) the role of hybridization in preventing introduced species spread, and (iii) the importance of postzygotic barriers in maintaining reproductive isolation. Anthropogenic contact zones offer evolutionary biologists unprecedented large scale hybridization experiments. In addition to breaking the highly effective reproductive isolating barrier of spatial segregation, they allow researchers to explore unusual demographic contexts with strong asymmetries. The outcomes are diverse, from introgression swamping to strong barriers to gene flow, and lead to local containment or widespread invasion. These outcomes should not be neglected in management policies of marine invasive species. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.
... The structure of this zone presents a number of interesting experimental opportunities to examine links between genotype and phenotype. For example, mitochondrial haplotypes are spreading more rapidly than nuclear markers, leading to strong mito-nuclear discordance outside the 'nuclear' hybrid zone, and novel mito-nuclear combinations within the region of nuclear admixture (Darling et al., 2014;Jeffery et al., 2017). Furthermore, the two lineages are mixing across an ecological seascape that varies in a number of physical and biological factors. ...
... In 2011, transcriptome sequencing showed extensive admixture in the recent Newfoundland expansion, which is believed to derive from an admixed Nova Scotia population, with no evidence for any nuclear introgression in 'southern' populations in New Jersey and central Maine (Blakeslee et al., 2010;Tepolt and Palumbi, 2015). A geographically broad RAD-seq-based study showed extensive nuclear introgression in southeastern Nova Scotia and southeastern Newfoundland, with most other east coast populations composed primarily or exclusively of animals from a primarily northern or southern nuclear background (Jeffery et al., 2017). Given both this prior work and the nuclear patterns we see here, it is likely that our Harpswell crabs had primarily southern nuclear backgrounds; the Kent Island crabs had admixed nuclear backgrounds; and the Pomquet crabs had northern backgrounds. ...
... We have established a clear link between mitochondrial haplotype and male cold tolerance in C. maenas, which suggests that differences in cline structure between mitochondrial markers and other, putatively neutral, nuclear markers (e.g. microsatellites and SNPs; Darling et al., 2014;Jeffery et al., 2017) are likely related to a shifting balance between selection and stochastic demographic processes that is marker dependent. With regards to gradients in temperature in the Gulf of Maine and the Canadian Maritimes, the influence of the cold Labrador current is particularly strong as it moves southward along the coast of Nova Scotia and into the upper reaches of the Gulf of Maine, essentially splitting the eastern and western Gulf into two different thermal regimes (Pettigrew et al., 2005). ...
Article
Hybrid zones provide natural experiments in recombination within and between genomes that may have strong effects on organismal fitness. On the East Coast of North America, two distinct lineages of the European green crab (Carcinus maenas) have been introduced in the last two centuries. These two lineages with putatively different adaptive properties have hybridized along the coast of the eastern Gulf of Maine, producing new nuclear and mitochondrial combinations that show clinal variation correlated with water temperature. To test the hypothesis that mitochondrial or nuclear genes have effects on thermal tolerance, we first measured the response to cold stress in crabs collected throughout the hybrid zone, then sequenced the mitochondrial CO1 gene and two nuclear single nucleotide polymorphisms (SNPs) representative of nuclear genetic lineage. Mitochondrial haplotype had a strong association with the ability of crabs to right themselves at 4.5°C that was sex specific: haplotypes originally from northern Europe gave male crabs an advantage while there was no haplotype effect on righting in female crabs. By contrast, the two nuclear SNPs that were significant outliers in a comparison between northern and southern C. maenas populations had no effect on righting response at low temperature. These results add C. maenas to the shortlist of ectotherms in which mitochondrial variation has been shown to affect thermal tolerance, and suggest that natural selection is shaping the structure of the hybrid zone across the Gulf of Maine. Our limited genomic sampling does not eliminate the strong possibility that mito-nuclear co-adaptation may play a role in the differences in thermal phenotypes documented here. Linkage between mitochondrial genotype and thermal tolerance suggests a role for local adaptation in promoting the spread of invasive populations of C. maenas around the world.
... Carcinus maenas' wide range and genetic variability between populations of C. maenas may require different primers for the detection of each C. maenas population (Darling et al. 2008;Darling and Mahon 2011;Jeffery et al. 2017;Roman and Palumbi 2004). Primers and probes for qPCR specific to C. maenas have previously been designed and implemented in detection methods in Australia and have proven to amplify only C. maenas DNA and not that of other local Australian species (Bott et al. 2010;Roux et al. 2020). ...
Article
Full-text available
The early detection of invasive species is essential to cease the spread of the species before it can cause irreversible damage to the environment. The analysis of environmental DNA (eDNA) has emerged as a non-harmful method to detect the presence of a species before visual detection and is a promising approach to monitor invasive species. Few studies have investigated the use of eDNA for arthropods, as their exoskeleton is expected to limit the release of eDNA into the environment. We tested published primers for the invasive European green crab, Carcinus maenas , in the Gulf of Maine and found them not species-specific enough for reliable use outside of the area for which they were designed for. We then designed new primers, tested them against a broad range of local faunal species, and validated these primers in a field study. We demonstrate that eDNA analyses can be used for crustaceans with an exoskeleton and suggest that primers and probe sequences must be tested on local fauna at each location of use to ensure no positive amplification of these other species.
... It has not yet been determined if physiological differences in crabs from different areas is correlated with the three different genetic lineages in the native range (northern Europe, western Europe, and off-shelf of the Faroe Islands and Iceland) [10,11]. Genome-wide studies are exposing the complexity of the genetic background of this species [12][13][14][15][16][17][18]. Whenever possible this review will provide the consensus view on a particular topic, but in most cases there is so much variability in published data that no consensus is possible and we will instead present a variety of results from different studies. ...
Article
Carcinus maenas (the "shore crab" or "European green crab") is a very proficient invader (considered to be one of the world's 100 worst invaders by the IUCN) due to its phenotypic plasticity, wide temperature and salinity tolerance, and an extensive omnivorous diet. Native to Atlantic Europe, it has established two well-studied nonindigenous populations in the northwestern Atlantic and northeastern Pacific and less-studied populations in Australia, Argentina and South Africa. Green crabs are eurythermal and euryhaline as adults, but they are limited to temperate coastlines due to more restrictive temperature requirements for breeding and larval development. They cannot tolerate wave-swept open shores so are found in wave-protected sheltered bays, estuaries and harbors. Carcinus maenas has been the subject of numerous papers, with over 1000 published in the past decade. This review provides an up-to-date account of the current published information on the life history and population dynamics of this very important species, including genetic differentiation, habitat preferences, physical parameter tolerances, reproduction and larval development, sizes of crabs, densities of populations, sex ratios, ecosystem dynamics and ecological impacts in the various established global populations of green crabs.
... Despite the acute need for improved understanding of the evolutionary dynamics of marine invasions, notably for setting up more effective management and for curtailing the invasion rates, few studies have examined population genomics of non-indigenous species, and most have focused on issues related to hybridization between lineages (e.g., Carcinus maenas, Jeffery et al., 2017) or species (e.g., Mytilus spp. Saarman & Pogson, 2015), or for comparing native and non-native populations (e.g., Crassostrea spp., Gagnaire et al., 2018). ...
Article
Full-text available
Ports and farms are well‐known primary introduction hotspots for marine non‐indigenous species (NIS). The extent to which these anthropogenic habitats are sustainable sources of propagules and influence the evolution of NIS in natural habitats was examined in the edible seaweed Undaria pinnatifida, native to Asia and introduced to Europe in the 1970s. Following its deliberate introduction 40 years ago along the French coast of the English Channel, this kelp is now found in three contrasting habitat types: farms, marinas, and natural rocky reefs. In light of the continuous spread of this NIS, it is imperative to better understand the processes behind its sustainable establishment in the wild. In addition, developing effective management plans to curtail the spread of U. pinnatifida requires determining how the three types of populations interact with one another. In addition to an analysis using microsatellite markers, we developed, for the first time in a kelp, a ddRAD‐sequencing technique to genotype 738 individuals sampled in 11 rocky reefs, 12 marinas, and 2 farms located along ca. 1000 km of coastline. As expected, the RAD‐seq panel showed more power than the microsatellite panel for identifying fine‐grained patterns. However, both panels demonstrated habitat‐specific properties of the study populations. In particular, farms displayed very low genetic diversity and no inbreeding conversely to populations in marinas and natural rocky reefs. In addition, strong, but chaotic regional genetic structure, was revealed, consistent with human‐mediated dispersal (e.g., leisure boating). We also uncovered a tight relationship between populations in rocky reefs and those in nearby marinas, but not with nearby farms, suggesting spill‐over from marinas into the wild. Finally, a temporal survey spanning 20 generations showed that wild populations are now self‐sustaining, albeit there was no evidence for local adaptation to any of the three habitats. These findings highlight that limiting the spread of U. pinnatifida requires efficient management policies that also target marinas. This article is protected by copyright. All rights reserved.
... It has not yet been determined if physiological differences in crabs from different areas is correlated with the three different genetic lineages in the native range (northern Europe, western Europe, and off-shelf of the Faroe Islands and Iceland) [10,11]. Genome-wide studies are exposing the complexity of the genetic background of this species [12][13][14][15][16][17][18]. Whenever possible this review will provide the consensus view on a particular topic, but in most cases there is so much variability in published data that no consensus is possible and we will instead present a variety of results from different studies. ...
Preprint
Full-text available
Carcinus maenas (the “shore crab” or “European green crab”) is a very proficient invader (considered to be one of the world’s 100 worst invaders by the IUCN) due to its phenotypic plasticity, wide temperature and salinity tolerance, and an extensive omnivorous diet. Native to Atlantic Europe, it has established two well-studied nonindigenous populations in the northwestern Atlantic and northeastern Pacific and less-studied populations in Australia, Argentina and South Africa. Green crabs are eurythermal and euryhaline as adults, but they are limited to temperate coastlines due to more restrictive temperature requirements for breeding and larval development. They cannot tolerate wave-swept open shores so are found in wave-protected sheltered bays, estuaries and harbors. C. maenas has been the subject of numerous papers, with over 1000 published in the past decade. This literature review provides an up-to-date account of the current published information on the population dynamics of this very important species, including habitat preferences, physical parameter tolerances, reproduction and larval development, sizes of crabs, densities of populations, sex ratios, ecosystem dynamics and ecological impacts in the various established global populations of green crabs.
... It has not yet been determined if physiological differences in crabs from different areas is correlated with the three different genetic lineages in the native range (northern Europe, western Europe, and off-shelf of the Faroe Islands and Iceland) [10,11]. Genome-wide studies are exposing the complexity of the genetic background of this species [12][13][14][15][16][17][18]. Whenever possible this review will provide the consensus view on a particular topic, but in most cases there is so much variability in published data that no consensus is possible and we will instead present a variety of results from different studies. ...
Preprint
Full-text available
Carcinus maenas (the “shore crab” or “European green crab”) is a very proficient invader (considered to be one of the world’s 100 worst invaders by the IUCN) due to its phenotypic plasticity, wide temperature and salinity tolerance, and an extensive omnivorous diet. Native to Atlantic Europe, it has established two well-studied nonindigenous populations in the northwestern Atlantic and northeastern Pacific and less-studied populations in Australia, Argentina and South Africa. Green crabs are eurythermal and euryhaline as adults, but they are limited to temperate coastlines due to more restrictive temperature requirements for breeding and larval development. They cannot tolerate wave-swept open shores so are found in wave-protected sheltered bays, estuaries and harbors. C. maenas has been the subject of numerous papers, with over 1000 published in the past decade. This literature review provides an up-to-date account of the current published information on the population dynamics of this very important species, including habitat preferences, physical parameter tolerances, reproduction and larval development, sizes of crabs, densities of populations, sex ratios, ecosystem dynamics and ecological impacts in the various established global populations of green crabs.
... A notorious exception is the European green crab (Carcinus maenas) in the Northwest Atlantic (Darling et al. 2008). However, although the genome-wide genetic differentiation has been studied in the introduced range (Jeffery et al. 2017(Jeffery et al. , 2018, it has not been compared with the differentiation observed in the native range to date. ...
Article
Full-text available
The Pacific cupped oyster is genetically subdivided into two sister taxa, Crassostrea gigas and C. angulata, which are in contact in the north-western Pacific. The nature and origin of their genetic and taxonomic differentiation remains controversial due the lack of known reproductive barriers and the high degree of morphologic similarity. In particular, whether the presence of ecological and/or intrinsic isolating mechanisms contributes to species divergence is unknown. The recent co-introduction of both taxa into Europe offers a unique opportunity to test how genetic differentiation is maintained under new environmental and demographic conditions. We generated a pseudo-chromosome assembly of the Pacific oyster genome using a combination of BAC-end sequencing and scaffold anchoring to a new high-density linkage map. We characterized genome-wide differentiation between C. angulata and C. gigas in both their native and introduced ranges, and showed that gene flow between species has been facilitated by their recent co-introductions in Europe. Nevertheless, patterns of genomic divergence between species remain highly similar in Asia and Europe, suggesting that the environmental transition caused by the co-introduction of the two species did not affect the genomic architecture of their partial reproductive isolation. Increased genetic differentiation was preferentially found in regions of low recombination. Using historical demographic inference, we show that the heterogeneity of differentiation across the genome is well explained by a scenario whereby recent gene flow has eroded past differentiation at different rates across the genome after a period of geographical isolation. Our results thus support the view that low-recombining regions help in maintaining intrinsic genetic differences between the two species.
... In fact, multiple introductions (i.e., green crab, Carcinus maenas) increase genetic polymorphisms in alien species in an invaded area (Jeffery et al., 2017;Roman, 2006). Apparently, alien species are unlikely to be established in a non-native area when the introduction effort is inadequate (Dlugosch & Parker, 2008). ...
Article
Invasion of alien species has led to serious problems, including the destruction of native ecosystems. In general, invasive species adapt to new environments rapidly, suggesting that they have high genetic diversity that can directly influence environmental adaptability. However, it is not known how genomic architecture causes genetic diversity that leads to invasiveness. Recent studies have showed that the proportion of duplicated genes (PD) in whole animal genomes correlate with environmental variability within a habitat. Here, we show that PD and propagule size significantly explain the differences in species categories (invasive species, noninvasive species, and parasites). PD correlated negatively with the propagule size. The residual values of regression of PD on propagule size revealed that the invasive species had higher PD values and larger propagule size than those of the noninvasive species, whereas the parasites had lower PD values and smaller propagule size than those of others. There were no correlations between the invasive species and other genomic factors including the genome size, number of genes, and certain gene families. Our results suggest that the PD values of a genome might be a potential genomic source causing genetic variations for adaptation to diverse environments. The results also showed that the invasiveness status of a species would be predicted by the residual values of regression of PD on propagule size. Our innovative approach provides a measure to estimate the environmental adaptability of organisms based on genomic data.
... The subsequent introduction of this lineage in Porto might have led to admixture between the two lineages. In the American introduced range of C. maenas hybridization between two lineages independently and successively introduced, each of them presumably adapted to different thermal conditions had been shown(Jeffery, DiBacco, Wringe, et al., 2017). A similar situation might occur along the Portuguese coasts. ...
Article
Full-text available
Twenty‐years of genetic studies of marine invaders have shown that successful invaders are often characterized by native and introduced populations displaying similar levels of genetic diversity. This pattern is presumably due to high propagule pressure and repeated introductions. The opposite pattern is reported in this study of the brown seaweed, Sargassum muticum, an emblematic species for circumglobal invasions. Albeit demonstrating polymorphism in the native range, microsatellites failed to detect any genetic variation over 1269 individuals sampled from 46 locations over the Pacific‐Atlantic introduction range. Single‐Nucleotide Polymorphisms (SNPs) obtained from ddRAD‐sequencing revealed some genetic variation, but confirmed severe founder events in both the Pacific and Atlantic introduction ranges. Our study thus exemplifies the need for extreme caution in interpreting neutral genetic diversity as a proxy for invasive potential. Our results confirm a previously hypothesized trans‐oceanic secondary introduction from NE Pacific to Europe. However, the SNPs panel unexpectedly revealed two additional distinct genetic origins of introductions. Also, conversely to scenarios based on historical records, southern rather than northern NE Pacific populations could have seeded most of the European populations. Finally, the most recently introduced populations showed the lowest selfing rates, suggesting higher levels of recombination might be beneficial at the early stage of the introduction process (i.e., facilitating evolutionary novelties), whereas uniparental reproduction might be favored later in sustainably established populations (i.e., sustaining local adaptation). This article is protected by copyright. All rights reserved.
... At three migration edges, there was admixture between G M and G H2 , while at four migration edges, an unsampled M. rugosa-like population was admixed with N. At five migration edges, there was additional gene flow originating from the common ancestor of the Hawaii Island populations into G H2 . This suggests that five migration edges may over-fit the data or that Hawaii Island M. polymorpha may have originated as a hybrid swarm (Jeffery et al. 2017;Wang et al. 2017;Richards et al. 2018). In addition, at five migration edges, the log-likelihood of the model started to plateau (supplementary fig. ...
Article
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A long-standing goal of evolutionary biology is to understand the mechanisms underlying the formation of species. Of particular interest is whether or not speciation can occur in the presence of gene flow and without a period of physical isolation. Here, we investigated this process within Hawaiian Metrosideros, a hyper-variable and highly dispersible woody species complex that dominates the Hawaiian Islands in continuous stands. Specifically, we investigated the origin of Metrosideros polymorpha var. newellii (newellii), a riparian ecotype endemic to Hawaii Island that is purportedly derived from the archipelago-wide M. polymorpha var. glaberrima (glaberrima). Disruptive selection across a sharp forest-riparian ecotone contributes to the isolation of these varieties and is a likely driver of newellii's origin. We examined genome-wide variation of 42 trees from Hawaii Island and older islands. Results revealed a split between glaberrima and newellii within the past 0.3-1.2 million years. Admixture was extensive between lineages within Hawaii Island and between islands, but introgression from populations on older islands (i.e. secondary gene flow) did not appear to contribute to the emergence of newellii. In contrast, recurrent gene flow (i.e. primary gene flow) between glaberrima and newellii contributed to the formation of genomic islands of elevated absolute and relative divergence. These regions were enriched for genes with regulatory functions as well as for signals of positive selection, especially in newellii, consistent with divergent selection underlying their formation. In sum, our results support riparian newellii as a rare case of incipient ecological speciation with primary gene flow in trees.
... It has not yet been determined if physiological differences in crabs from different areas is correlated with the three different genetic lineages in the native range (northern Europe, western Europe, and off-shelf of the Faroe Islands and Iceland) [10,11]. Genome-wide studies are exposing the complexity of the genetic background of this species [12][13][14][15][16][17][18]. Whenever possible this review will provide the consensus view on a particular topic, but in most cases there is so much variability in published data that no consensus is possible and we will instead present a variety of results from different studies. ...
Preprint
Carcinus maenas (the “shore crab” or “European green crab”) is a very proficient invader (considered to be one of the world’s 100 worst invaders by the IUCN) due to its phenotypic plasticity, wide temperature and salinity tolerance, and an extensive omnivorous diet. Native to Atlantic Europe, it has established two well‐studied nonindigenous populations in the northwestern Atlantic and northeastern Pacific and less‐studied populations in Australia, Argentina and South Africa. Green crabs are eurythermal and euryhaline as adults, but they are limited to temperate coastlines due to more restrictive temperature requirements for breeding and larval development. They cannot tolerate wave‐swept open shores so are found in wave‐protected sheltered bays, estuaries and harbors. Carcinus maenas has been the subject of numerous papers, with over 1000 published in the past decade. This review provides an up‐to‐date account of the current published information on the life history and population dynamics of this very important species, including genetic differentiation, habitat preferences, physical parameter tolerances, reproduction and larval development, sizes of crabs, densities of populations, sex ratios, ecosystem dynamics and ecological impacts in the various established global populations of green crabs.
... riddetective. For an example of the HYBRIDDETECTIVE workflow, see Jeffery et al. (2017) and Fig. S1. We chose to implement hybrid detection using the program NEWHYBRIDS (Anderson & Thompson, 2002) because it permits the assignment of individuals to hybrid class (i.e., pure-bred, F 1 , F 2 and backcrosses) and does not require a priori knowledge of the allele frequencies of the two populations being tested (Anderson & Thompson, 2002). ...
Article
The ability to detect and characterize hybridization in nature has long been of interest to many fields of biology and often has direct implications for wildlife management and conservation. The capacity to identify the presence of hybridization, and quantify the numbers of individuals belonging to different hybrid classes, permits inference on the magnitude of, and time scale over which, hybridization has been, or is occurring. Here we present an R package and associated workflow developed for the detection, with estimates of efficiency and accuracy, of multi-generational hybrid individuals using genetic or genomic data in conjunction with the program NEWHYBRIDS. This package includes functions for the identification and testing of diagnostic panels of markers, the simulation of multi-generational hybrids, and the quantification and visualization of the efficiency and accuracy with which hybrids can be detected. Overall, this package delivers a streamlined hybrid analysis platform, providing improvements in speed, ease of use and repeatability over current ad hoc approaches. The latest version of the package and associated documentation are available on GitHub (https://github.com/bwringe/hybriddetective).
... A notorious 100 exception is the European green crab (Carcinus maenas) in the Northwest Atlantic (Darling, et al. 101 2008). However, although the genome-wide genetic differentiation has been studied in the introduced 102 range (Jeffery, et al. 2017;Jeffery, et al. 2018), it has not been compared with the differentiation 103 observed in the native range to date. 104 ...
Preprint
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The Pacific cupped oyster is genetically subdivided into two sister taxa, Crassostrea gigas and C. angulata , which are in contact in the north-western Pacific. The nature and origin of their genetic and taxonomic differentiation remains controversial due the lack of known reproductive barriers and morphologic similarity. In particular, whether ecological and/or intrinsic isolating mechanisms participate to species divergence remains unknown. The recent co-introduction of both taxa into Europe offers a unique opportunity to test how genetic differentiation maintains under new environmental and demographic conditions. We generated a pseudo-chromosome assembly of the Pacific oyster genome using a combination of BAC-end sequencing and scaffold anchoring to a new high-density linkage map. We characterized genome-wide differentiation between C. angulata and C. gigas in both their native and introduced ranges, and showed that gene flow between species has been facilitated by their recent co-introductions in Europe. Nevertheless, patterns of genomic divergence between species remain highly similar in Asia and Europe, suggesting that the environmental transition caused by the co-introduction of the two species did not affect the genomic architecture of their partial reproductive isolation. Increased genetic differentiation was preferentially found in regions of low recombination. Using historical demographic inference, we show that the heterogeneity of differentiation across the genome is well explained by a scenario whereby recent gene flow has eroded past differentiation at different rates across the genome after a period of geographical isolation. Our results thus support the view that low-recombining regions help in maintaining intrinsic genetic differences between the two species.
... Entry of Indo-Pacific and Lessepsian migrants into the Eastern Mediterranean from the Suez Canal is one of the oldest maritime pathways of dispersal, transporting introduced species to a considerable number of marinas (Galil and Zenetos 2002). Further, popular maritime traffic highways between Northern European Seas and tropical ecosystems are strongly connected to the dispersal of invasive species (Seebens et al., 2013), and previous genetic studies demonstrate many Caribbean invasions originating from Europe (Gerlach, 1997;Besnier et al., 2014;Jeffery et al., 2017). ...
Thesis
Seagrasses occur worldwide, and are essential primary producers that uptake carbon dioxide, fix nutrients, stabilize sediments, prevent reef degradation, filter bacteria, provide food and nursery habitats to marine organisms. When seagrass meadows disappear, carbon is released back into the water column, sediments get stirred, water clarity decreases, and reefs become infected, with negative impacts on marine biodiversity and maritime economy. My thesis utilizes multidisciplinary ecology and evolutionary biology approaches to better understand the biology of seagrasses, particularly an invasive seagrass, to help improve management strategies for seagrass conservation. Seagrasses frequently display distinct depth distribution, although drivers of these patterns can be spatially and temporally variable. Chapter 1 examines the factors that influence the depth distribution of a circumtropical seagrass, Halophila decipiens. While H. decipiens can grow in waters as shallow as 1 m, in Moorea, French Polynesia we only found it in waters deeper than 6.4 m. To understand why H. decipiens did not grow in shallower habitats, we transplanted it into 3 habitats: the existing seagrass bed (control), just outside the seagrass bed, and shallower habitat adjacent to a fringing coral reef. Results showed that growth was not significantly different between the seagrass bed and just outside of the seagrass bed; however, its growth was significantly reduced when adjacent to the reef. We then transplanted seagrass into a shallower reef site with and without herbivore exclusion cages, and the results showed that H. decipiens grew best when herbivores were excluded, but lost growth when herbivores were allowed access. These results indicate that H. decipiens can grow in shallow habitats adjacent to reefs, but herbivory pressure from the reef limits its depth distribution. Seagrass meadows are in decline around the world. Biological invasions can magnify threats to seagrass ecosystems with detrimental consequences to seagrass biodiversity. In Chapter 2, I used mesocosm experiments to investigate the interactions between the invasive seagrass Halophila stipulacea and native seagrasses to determine whether species interactions can drive, prevent, or facilitate invasions in both the Mediterranean and Caribbean Sea. In the Caribbean, invasive H. stipulacea increased in growth when grown with the native Syringodium filiforme, and lost shoots when grown alone, while S. filiforme only increased in shoots when grown alone. This pattern was the same in the Mediterranean; when invasive H. stipulacea grew with the native Cymodocea nodosa, it gained more shoots than when grown alone, but C. nodosa only did better when grown alone. Results suggest that the invasive seagrass H. stipulacea can drive its own success by negatively affecting native seagrasses and benefiting from that negative interaction. This novel example of native species facilitating the success of an invasive provides one possible mechanism for the widespread success of this invasive species. Mechanisms that influence invasion success can further be understood by understanding how it was introduced to a specific region. In Chapter 3, I used genomic tools to reconstruct the origins of the globally invasive seagrass Halophila stipulacea in the Mediterranean and Caribbean Seas. While H. stipulacea almost certainly invaded the Mediterranean from native populations in the Red Sea through the Suez Canal, it is unclear whether the Caribbean invasion represents stepping stone colonization from the Mediterranean, an independent introduction from the native range, or an admixture from multiple native/invasive populations. To test these hypotheses, we examined population genetic structure and genetic diversity from multiple locations spanning across the native, historic, and recent invasive ranges of H. stipulacea, including the Indian Ocean and Red Sea, Mediterranean Sea, and the Caribbean Sea, respectively. Data from 524 SNP loci and restrictive, 45 SNP loci at >10x coverage revealed significant genetic structure among all five regions. The analyses revealed that the widespread invasion of H. stipulacea into the Caribbean Sea came from multiple introductions originating from the Mediterranean. This work provides a baseline for the distribution of the invasive H. stipulacea in the Caribbean and may help predict how to minimize detrimental impacts of a non-indigenous seagrass across its invaded ranges. Life history differences can provide a link in invasion potential and dispersal. In Chapter 4 I investigated the life history of seagrass Halophila stipulacea in the Caribbean. Reports of asexual and sexual reproduction are common in its native range, with sexual reproduction being less common in the Mediterranean Sea. Here we make the first report of H. stipulacea male flowers in the Caribbean and suggest that asexual fragmentation is the main strategy of expansion. These findings have important implications for the future dispersal, survival, and maintenance of the non-native populations in the Caribbean.
... There is genomic evidence for hybridization in Carcinus spp. invasions in Japan (Darling, 2011) and Canada (Jeffery et al., 2017), Japanese mitten crabs (Eriocheir japonica) in Europe (Hayer et al., 2019), and occurring naturally between two snow crab species: Chionoecetes japonicus and Chionoecetes opilio in Korea (Kim et al., 2012). At the edge of species' geographic ranges in particular, demographic factors and processes such as gene surfing and genetic stickiness may result in mean displacement of genes outpacing mean larval dispersal (Darling et al., 2014). ...
Article
Full-text available
Crustaceans are amongst the most reported invaders of coastal habitats, and predatory brachyuran crabs one of the most successful marine invasive groups. They hold high tolerance to abiotic stress and their genetic, life- history, and behavioural adaptation mechanisms prompt their invasive conspicuousness. However, there is a generalized ambiguity on the specific processes that make these bioinvasions successful. No trait-related patterns have yet been found, mostly since traits attributed solely to non-indigenous crab species lack confirmation by comparison with their native counterparts and across each other. Therefore, this review discusses the available literature on fitness and plasticity of brachyuran crabs under global changes, and advances the increasing importance of addressing native versus non-native invasive species comparisons in the annals of brachyura in- vasion dynamics. Further on, integrative approaches are highlighted and proposed as innovative tools to disentangle trait-related tolerance, overall crab phenotypic plasticity and further adaptation. These indicator tools will advance the knowledge on crabs’ invasive potential, which ultimately affects upcoming population dynamics and ecosystem services, adding value to an effective management of coastal bioinvasions.
... The European shore crab Carcinus maenas, an infamous global invader, provides another prominent example: initially introduced to the NW Atlantic in the early 1800s, a rapid northward expansion and population growth along the Canadian Atlantic coast was observed since the 1980s, presumably as a consequence of multiple introductions from the northern native range (Roman 2006). The two distinct introduced lineages of C. maenas are now hybridising in the Canadian maritimes, potentially leading to increased thermal tolerance and overall increasing invasive potential (Jeffery et al. 2017;Lehnert et al. 2018). Genetic data also indicated recurring introductions of the Asian shore crab Hemigrapsus sanguineus in the NW Atlantic, and high genetic diversity of expanding invasive populations (Lord and Williams 2016;Blakeslee et al. 2017). ...
Article
Full-text available
Genetic studies of introduced non-native species are a valuable tool to investigate invasion history and pathways, source populations and multiple introductions of alien species, as well as evolutionary genetic changes following establishment in a new environment. We used a set of nine polymorphic microsatellites to analyse the population genetic structure of the introduced Asian shore crab Hemigrapsus takanoi along European coasts. Our dataset covered the complete known European range of the species, including the most recent records from Great Britain and the southwestern Baltic Sea. The results showed a similarly high genetic diversity of H. takanoi throughout Europe, and no indication of genetic bottlenecks during secondary spread, even in the most recently established populations. Analyses for population structure along geographic regions gave support for a separation between the Bay of Seine populations (northern France) and all other populations. Genetic differentiation within the North and Baltic Seas was more subtle and patchy, hinting to potential unrecognised introduction events, dispersal barriers and anthropogenic vector activity. The populations from the Baltic Sea and Great Britain clustered with the Wadden Sea populations, suggesting secondary introductions from the southeastern North Sea as likely invasion pathways. In summary, we suggest that a combination of anthropogenic secondary spread and the species' reproductive biology have prevented a loss of genetic diversity during its ongoing expansion. We argue that genetic data depicting population status shortly after an introduction event-like the British and Baltic Sea populations of H. takanoi-may provide important baseline data for investigations of genetic changes during establishment and adaptation processes.
... Selkoe and Toonen 2011;Fuentes-Pardo and Ruzzante 2017;Jeffery et al. 2017;Van Wyngaarden et al. 2017b). ...
Technical Report
Full-text available
Canada has committed to developing effective and representative marine conservation networks. Guidance for the development of these networks focuses on core design features, including the incorporation of ecologically and biologically significant areas, ecological representation, replication, connectivity, and adequacy/viability. Network planning using these design features is currently underway in five priority bioregions: the Gulf of St. Lawrence, the Scotian Shelf, the Newfoundland-Labrador Shelves, the Western Arctic, and the Pacific Northern Shelf. To ensure these networks achieve their biodiversity protection goals and objectives, the extent to which the design features are being achieved must be evaluated and monitored over time. Practical advice on how to monitor and evaluate Marine Protected Area (MPA) networks is critical for identifying the key elements of (future) successful management plans. This paper focuses on approaches for evaluating and monitoring the core design features of the Canadian MPA Network. We describe the importance of these design features and detail tools and approaches relevant for evaluation and monitoring at the network level. We then present a detailed case study to show how marine conservation network planning in the Northern Shelf Bioregion (NSB) has incorporated the design features in evaluations of draft network designs and how those methods can direct future monitoring within the NSB and more broadly in the Canadian MPA Network.
... This invasion brought Green Crab propagules from northern Europe, which appeared better adapted to the colder temperatures in the Eastern Shore and north of Halifax. These cold-water adapted Green Crabs spread further north and began to hybridize with crabs from the southern invasion that had reached their northern limit (Audet et al. 2003, Jeffery et al. 2017a, Roman 2006. This genetic information is crucial, as it suggests that, had a second invasion not occurred, Green Crab would not likely have established stable populations on the Eastern Shore due to the colder temperatures relative to areas further south. ...
Technical Report
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The Biophysical and Ecological Overview of the Eastern Shore Islands Area of Interest (AOI) summarizes what is known about key physical and biological components of the Eastern Shore Islands ecosystem. These key attributes and description of their ecosystem function can be used to inform the development of Conservation Objectives and management measures, should the study area be established as a Marine Protected Area under Canada’s Oceans Act. The Eastern Shore Islands is a unique and complex archipelago system that has low human impact and a high degree of naturalness. Diverse habitat types consisting of bedrock, cobble, and sandy substrates, Eelgrass (Zostera marina), Rockweed (Ascophyllum nodosum), kelp beds, mud flats, and salt marshes are associated with the more than 200 nearshore islands encompassed within the AOI boundaries. These habitats provide important nesting, foraging, and overwintering habitat for large numbers of marine birds, including two endangered species – the Roseate Tern (Sterna dougalli) and Piping Plover (Charadrius melodus). Eelgrass and kelp beds provide important habitat for juvenile groundfish in this region, including Atlantic Cod (Gadus morhua) and Pollock (Pollachius virens). Subtidal Rockweed beds in the AOI have higher species richness and abundance of associated fish and invertebrates compared to southern Nova Scotia and areas devoid of Rockweed. The Eastern Shore Atlantic Herring (Clupea harengus) spawning area, an important component of the coastal spawning component, overlaps with the western portion of the AOI. Rivers and estuaries leading into the study area provide important migratory habitat for diadromous fishes including American Eel (Anguilla rostrata) and Atlantic Salmon (Salmo salar; assessed as Endangered by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC)), which migrate through the AOI to reach feeding and spawning areas. American Lobster (Homarus americanus), found throughout the study area, support an important commercial fishery in the Eastern Shore. Other invertebrates common to the area include molluscs, echinoderms, crustaceans, tunicates, and polychaetes that are associated with high habitat heterogeneity. Within the Eastern Shore Islands AOI, Harbour Seals are present and there are two inshore colonies of Grey Seal (Halichoerus grypus), but otherwise the area has no recorded significant habitat for other marine mammal species. The area is highly natural, with lower levels of contaminants in the water and sediments, lower human impacts, and fewer invasive species than southern Nova Scotia and the Bay of Fundy. The diversity and complexity of this highly natural habitat, in conjunction with juvenile fish nurseries and extensive marine bird foraging grounds, make this a unique and important ecosystem to the Scotian Shelf Bioregion. Though the full extent of biological diversity has yet to be quantified, it is likely that the unique habitat characteristics of the AOI are associated with a distinctive and diverse assemblage of bird, fish, and invertebrate species.
... Noncongruent patterns between mitochondrial and genomic DNA are expected due to recombination between nuclear markers but not mitochondrial sequences, consistent with patterns seen in more recently introduced species (Ayari et al., 2017; Jeffery et al., 2017). ...
Article
Full-text available
The same vectors that introduce species to new ranges could move them among native populations, but how human‐mediated dispersal impacts native ranges has been difficult to address because human‐mediated dispersal and natural dispersal can simultaneously shape patterns of gene flow. Here, we disentangle human‐mediated dispersal from natural dispersal by exploiting a system where the primary vector was once extensive but has since ceased. From 10th to 19th Centuries, ships in the North Atlantic exchanged sediments dredged from the intertidal for ballast, which ended when seawater ballast tanks were adopted. We investigate genetic patterns from RADseq‐derived SNPs in the amphipod Corophium volutator (n = 121; 4,870 SNPs) and the annelid Hediste diversicolor (n = 78; 3,820 SNPs), which were introduced from Europe to North America, have limited natural dispersal capabilities, are abundant in intertidal sediments, but not commonly found in modern water ballast tanks. We detect similar levels of genetic subdivision among introduced North American populations and among native European populations. Phylogenetic networks and clustering analyses reveal population structure between sites, a high degree of phylogenetic reticulation within ranges, and phylogenetic splits between European and North American populations. These patterns are inconsistent with phylogeographic structure expected to arise from natural dispersal alone, suggesting human activity eroded ancestral phylogeographic structure between native populations, but was insufficient to overcome divergent processes between naturalized populations and their sources. Our results suggest human activity may alter species' evolutionary trajectories on a broad geographic scale via regional homogenization and global diversification, in some cases precluding historical inference from genetic data.
... It has not yet been determined if physiological differences in crabs from different areas is correlated with the three different genetic lineages in the native range (northern Europe, western Europe, and off-shelf of the Faroe Islands and Iceland) [10,11]. Genome-wide studies are exposing the complexity of the genetic background of this species [12][13][14][15][16][17][18]. Whenever possible this review will provide the consensus view on a particular topic, but in most cases there is so much variability in published data that no consensus is possible and we will instead present a variety of results from different studies. ...
Article
Full-text available
Mule deer (Odocoileus hemionus) are endemic to a wide variety of habitats in western North America, many of which are shared in sympatry with their closely related sister-species white-tailed deer (Odocoileus virginianus), whom they hybridize with in wild populations. Although mule deer meet many ideal conditions for a molecular ecological research species, such as high abundance, ecological importance, and broad dispersal and gene flow, conservation genetic studies have been limited by a relative lack of existing genomic resources and inherent difficulties caused by introgression with white-tailed deer. Many molecular tools currently available for the study of cervids were designed using reference assemblies of divergent model species, specifically cattle (Bos taurus). Bovidae and Cervidae diverged approximately 28 million years ago, therefore, we sought to ameliorate the available resources by contributing the first mule deer whole genome sequence draft assembly with an average genome-wide read depth of 25X, using the white-tailed genome assembly (Ovir.te_1.0) as a reference. Comparing the two assemblies, we identified ∼33 million single nucleotide polymorphisms (SNPs) and insertion/deletion variants. We then verified fixed SNP differences between the two species and developed a 40-loci SNP assay capable of identifying pure mule deer, white-tailed deer, and interspecific hybrids. Assignment capacity of the panel, which was tested on simulated datasets, is reliable up to and including the third backcross hybrid generation. Identification of post-F1 hybrids will be necessary for hybrid zone population studies going forward, and the new mule deer assembly will be a valuable resource for genetic and comparative genomics studies.
Article
Most marine invertebrates disperse during a planktonic larval stage that may drift for weeks with ocean currents. A challenge for larvae of coastal species is to return to coastal nursery habitats. Shore crab (Carcinus maenas L.) larvae are known to show tidal rhythmicity in vertical migration in tidal areas and circadian rhythmicity in micro-tidal areas, which seems to increase successful coastal settlement. We studied genome-wide differentiation based on 24,000 SNPs of 12 native populations of shore crab sampled from a large tidal amplitude gradient from macro-tidal (ca. 8 m) to micro-tidal (ca. 0.2 m). Dispersal and recruitment success of larvae was assessed with a Lagrangian biophysical model, which showed a strong effect of larval behavior on long-term connectivity, and dispersal barriers that partly coincided with different tidal environments. The genetic population structure showed a subdivision of the samples into three clusters, which represent micro-, meso- and macro-tidal areas. The genetic differentiation was mostly driven by 0.5% outlier loci, which showed strong allelic clines located at the limits between the three tidal areas. Demographic modelling suggested that the two genetic barriers have different origins. Differential gene expression of two clock genes (cyc and pdp1) further highlighted phenotypic differences among genetic clusters that are potentially linked to the differences in larval behaviour. Taken together, our seascape genomic study suggest that tidal regime acts as a strong selection force on shore crab population structure, consistent with larval behaviour affecting dispersal and recruitment success.
Preprint
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The early detection of invasive species is essential to cease the spread of the species before it can cause irreversible damage to the environment. The analysis of environmental DNA (eDNA) has emerged as a non-harmful method to detect the presence of a species before visual detection and is a promising approach to monitor invasive species. Few studies have investigated the use of eDNA for arthropods, as their exoskeleton is expected to limit the release of eDNA into the environment. We tested published primers for the invasive European green crab, Carcinus maenas , in the Gulf of Maine and found them not species-specific enough for reliable use outside of the area for which they were designed for. We then designed new primers, tested them against a broad range of local faunal species, and validated these primers in a field study. We demonstrate that eDNA analyses can be used for crustaceans with an exoskeleton and suggest that primers and probe sequences must be tested on local fauna at each location of use to ensure no positive amplification of these other species.
Article
Human‐driven translocations of species have diverse evolutionary consequences such as promoting hybridization between previously geographically isolated taxa. This is well‐illustrated by the solitary tunicate, Ciona robusta, native to the North East Pacific and introduced in the North East Atlantic. It is now co‐occurring with its congener C. intestinalis in the English Channel, and C. roulei in the Mediterranean Sea. Despite their long allopatric divergence, first and second generation crosses showed a high hybridization success between the introduced and native taxa in the laboratory. However, previous genetic studies failed to provide evidence of recent hybridization between C. robusta and C. intestinalis in the wild. Using SNPs obtained from ddRAD‐sequencing of 397 individuals from 26 populations, we further explored the genome‐wide population structure of the native Ciona taxa. We first confirmed results documented in previous studies, notably i) a chaotic genetic structure at regional scale, and ii) a high genetic similarity between C. roulei and C. intestinalis, which is calling for further taxonomic investigation. More importantly, and unexpectedly, we also observed a genomic hotspot of long introgressed C. robusta tracts into C. intestinalis genomes at several locations of their contact zone. Both the genomic architecture of introgression, restricted to a 1.5 Mb region of chromosome 5, and its absence in allopatric populations suggest introgression is recent and occurred after the introduction of the non‐indigenous species. Overall, our study shows that anthropogenic hybridization can be effective in promoting introgression breakthroughs between species at a late stage of the speciation continuum.
Article
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Background Natural hybridization can influence the adaptive response to selection and accelerate species diversification. Understanding the composition and structure of hybrid zones may elucidate patterns of hybridization processes that are important to the formation and maintenance of species, especially for taxa that have experienced rapidly adaptive radiation. Here, we used morphological traits, ddRAD-seq and plastid DNA sequence data to investigate the structure of a Rhododendron hybrid zone and uncover the hybridization patterns among three sympatric and closely related species. Results Our results show that the hybrid zone is complex, where bi-directional hybridization takes place among the three sympatric parental species: R. spinuliferum , R. scabrifolium , and R. spiciferum . Hybrids between R. spinuliferum and R. spiciferum ( R. × duclouxii ) comprise multiple hybrid classes and a high proportion of F 1 generation hybrids, while a novel hybrid taxon between R. spinuliferum and R. scabrifolium dominated the F 2 generation, but no backcross individuals were detected. The hybrid zone showed basically coincident patterns of population structure between genomic and morphological data. Conclusions Natural hybridization exists among the three Rhododendron species in the hybrid zone, although patterns of hybrid formation vary between hybrid taxa, which may result in different evolutionary outcomes. This study represents a unique opportunity to dissect the ecological and evolutionary mechanisms associated with adaptive radiation of Rhododendron species in a biodiversity hotspot.
Article
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Carcinus maenas (European Green Crab) is an invasive marine portunid crab that has established populations globally outside of its native range and has been implicated in declines of benthic invertebrates in invaded ecosystems. Observations of Green Crab on intertidal mudflats in the upper Bay of Fundy have increased in recent years. We assessed the distribution and relative abundance of crab populations in Chignecto Bay, an arm of the upper Bay of Fundy, by trapping Green Crab and native Cancer irroratus (Say) (Rock Crab) at mudflats and in rocky intertidal zones in 2013 and 2014. Spatial distribution of Green Crabs indicated a preference for rocky intertidal habitats and greater abundance geographically lower in the Bay, which would correspond with an initial introduction at the mouth of the Bay and subsequent inward expansion. Abundance declined drastically from 2013 to 2014, suggesting that Green Crab may not yet be well established in Chignecto Bay. Carapace width indicated that crab age may be less variable further into the Bay, suggesting these sites may only be colonized in years with favorable environmental conditions. The population may be vulnerable under poorer conditions in other years, like 2014, when high overwintering mortality is a possible cause for the observed decline. There was not a corresponding decline in native Rock Crab. While Green Crab abundance is currently relatively low in Chignecto Bay, and their impact on mudflats likely minimal, prolonged favorable environmental conditions could lead to an increased presence.
Thesis
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One of the world's most successful marine invaders, the European green crab (Carcinus maenas), continues to spread and invade the coastlines of Atlantic Canada. In Prince Edward Island in particular, populations have continued to expand since the late 1990s. In areas like these, there is a distinct need to document this species' expansion into new habitats, to monitor its impacts on important native species, and to develop innovative mitigation strategies to control some of its effects. This thesis addressed the large information gap that still exists on this species' effect in the Atlantic Canadian region by focusing on four main areas: First, I explored over a decade of green crab population expansion records along Prince Edward Island's main shorelines. Second, I surveyed and examined the effects of green crabs on vulnerable size classes of an important shellfish species, the American oyster (Crassostrea virginica). Third, I performed a preliminary study into the occurrence and synchrony of molting in green crabs, identifying suitable physical features of pre-molting crabs as a first step for developing a soft-shell crab industry. And fourth, I developed and tested a novel bycatch reduction device to be used with fyke nets to facilitate the implementation of the aforementioned directed fishery for this species. Samples collected during the years 2000-2013 indicated that green crab expansion rates on Prince Edward Island vary spatially and temporarily. Expansion rates were higher along the south shore than the north shore of the island, and it was hypothesized that this dissimilarity was possibly related to the higher availability of suitable habitat along the south shore. The speed of the spread was such that it seemed more likely related to the benthic movement of juvenile and adult crabs than associated to larval spread or new anthropogenic vectors. With regards to green crab impacts, multiple oyster bed surveys conducted in 2014 measured mortality levels of vulnerable size classes of oysters. These surveys revealed that the probability of mortality of small oysters was higher in areas where green crabs were present. This probability decreased in the presence of other food sources (i.e. mussel beds), a result likely linked to green crab prey iii preferences. Field experiments using inclusion/exclusion cages indicated that the odds of oyster mortality was higher in inclusion cages than in the open environment and exclusion cages. These results suggested that at least some of the mortality of oysters could be attributed to green crab predation. With the recent implementation of a fishery for green crab as a potential mitigation strategy, there is a need for a marketable product to prompt fishermen to harvest green crabs. A soft-shell green crab product modelled after the Venetian "moleche" is expected to provide a lucrative incentive beyond the existing hard shell bait market. The examination of the timing and characteristics of molting revealed that synchronized "molting windows" or times of increased molting occur in the early summer for male green crabs. Recorded molting rates in the laboratory and the field were as high as 75% and 60%, respectively. External physical characteristics such as the presence of a "halo" on the episternites of the carapace, were deemed a reliable indicator that a crab would molt within 3 weeks. Although these results were preliminary in nature, they were promising and suggested that further studies be performed on the potential scaling up of these results. Fyke nets are a natural choice for a directed fishery of green crabs, as this type of gear is readily available and used locally, primarily for American eel (Anguilla rostrata). These nets are also a variant of the fyke net used in Italy to fish for a similar species of crab (Carcinus aestuarii) during its molting season. However, before fyke nets can be used in a directed fishery for green crab in Atlantic Canada, bycatch must be reduced. A novel Bycatch Reduction Device (BRD) for fyke nets was therefore developed and evaluated. Bycatch numbers and diversity, including three key commercial species, were significantly lower in the BRD equipped nets. Overall, the results of this thesis advance green crab research in the region, especially with regards to the quantification of impacts and development of mitigation measures. Further research questions as a result of my thesis work are identified and briefly discussed.
Article
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Hybridization and introgression can have complex consequences for both species evolution and conservation. Here, we investigated the origin and characteristics of a putative hybrid zone between two South American poison dart frog species, O. anchicayensis and the critically endangered O. lehmanni, which are heavily sought after on the illegal pet market. Using a combination of phenotypic (49 traits) and genomic (ddRADseq) data, we found that the putative hybrids are morphologically distinct from their parental species and confirmed genomic signatures of admixture in these populations. Several lines of evidence (hybrid indices, interspecific hybrid heterozygosity, genomic clines, comparisons with simulated hybrids and demographic modelling) support the conclusion that these populations are not comprised of early‐generation hybrids and thus, they likely did not arise as a result of illegal translocations associated with wildlife trafficking. Instead, they likely represent an independent lineage which has persisted through isolation and has only relatively recently re‐established gene flow with both parental species. Furthermore, we detected signals of differential introgression from parental species into these hybrid populations which suggest relaxed stabilizing selection on these aposematic color morphs, potentially via context‐dependent female choice. These populations thus provide a fascinating window into the role of hybridization, isolation and female choice in the diversification of South American poison dart frogs. In addition, our results underline the importance of landscape conservation measures to protect, not only known localities of nominal species, but also the phenotypic and genomic variation harbored by admixed lineages which represent crucial repositories for the impressive diversity in this system.
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Hybridization among populations and species is a central theme in many areas of biology, and the study of hybridization has direct applicability to testing hypotheses about evolution, speciation, and genetic recombination, as well as having conservation, legal and regulatory implications. Yet, despite being a topic of considerable interest, the identification of hybrid individuals, and quantification of the (un)certainty surrounding the identifications remains difficult. Unlike other programs that exist to identify hybrids based on genotypic information, NEWHYBRIDS is able to assign individuals to specific hybrid classes (e.g. F1, F2) because it makes use of patterns of gene inheritance within each locus, rather than just the proportions of gene inheritance within each individual. For each comparison and set of markers, multiple independent runs of each dataset should be used to develop an estimate of the hybrid class assignment accuracy. The necessity of analyzing multiple simulated datasets, constructed from large genome-wide datasets presents significant computational challenges. To address these challenges we present parallelnewhybrid, an R package designed to decrease user burden when undertaking multiple NEWHYBRIDS analyses. parallelnewhybrid does so by taking advantage of the parallel computational capabilities inherent in modern computers to efficiently and automatically execute separate NEWHYBRIDS runs in parallel. We show that parallelization of analyses using this package affords users several-fold reductions in time over a traditional serial analysis. parallelnewhybrid consists of an example dataset, a README and three operating system-specific functions to execute parallel NEWHYBRIDS analyses on each of a computer's c cores. parallelnewhybrid is freely available on the long-term software hosting site GitHub (w w w . github. com/bwringe/parallelnewhybrid) This article is protected by copyright. All rights reserved.
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Advances in genetic sequencing technologies and techniques have made large, genome-wide datasets comprised of hundreds or even thousands of individuals and loci the norm rather than the exception even for non-model organisms. While such data presents new opportunities for evaluating population structure and demographic processes, the large size of these genomic datasets brings new computational challenges for researchers needing to parse, convert, and manipulate data often into a variety of software-specific formats required of genomic analyses. We developed genepopedit as a flexible tool for the manipulation of multilocus molecular datasets. Functionality can be divided among diagnostic, manipulation, sampling, and transformation-based tools. Metadata from large genomic datasets can be efficiently extracted, without the need to view data in a text editing program. genepopedit provides tools to manipulate loci, individual samples, and populations included in genomic datasets, in addition to the ability to convert directly to a variety of analysis formats. Functions are compiled as an R package, which can integrate into existing analysis workflows. Importantly, genepopedit provides a simple yet robust code-based tool for repeatable genomic data manipulation, which has been proven to be stable for datasets in excess of 200,000 SNPs. The latest version of the package and associated documentation are available on Github (github . com/rystanley/genepopedit). This article is protected by copyright. All rights reserved.
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The expanding scale and increasing rate of marine biological invasions has been documented since the early 20th century. Besides their global ecological and economic impacts, non-indigenous species (NIS) also have attracted much attention as opportunities to explore important eco-evolutionary processes such as rapid adaptation, long-distance dispersal and range expansion, and secondary contacts between divergent evolutionary lineages. In this context, genetic tools have been extensively used in the past twenty years. Three important issues appear to have emerged from such studies. First, the study of NIS has revealed unexpected cryptic diversity in what had previously been assumed homogeneous entities. Second, there has been surprisingly little evidence of strong founder events accompanying marine introductions, a pattern possibly driven by large propagule loads. Third, the evolutionary processes leading to successful invasion have been difficult to ascertain due to faint genetic signals. Here we explore the potential of novel tools associated with High-Throughput DNA Sequencing (HTS) to address these still pressing issues. Dramatic increase in the number of loci accessible via HTS has the potential to radically increase the power of analyses aimed at species delineation, exploring the population genomic consequences of range expansions, and examining evolutionary processes such as admixture, introgression, and adaptation. Nevertheless, the value of this new wealth of genomic data will ultimately depend on the ability to couple it with expanded “traditional” efforts, including exhaustive sampling of marine populations over large geographic scales, integrated taxonomic analyses, and population level exploration of quantitative trait differentiation through common-garden and other laboratory experiments.
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Understanding the population structure and patterns of gene flow within species is of fundamental importance to the study of evolution. In the fields of population and evolutionary genetics, measures of genetic differentiation are commonly used to gather this information. One potential caveat is that these measures assume gene flow to be symmetric. However, asymmetric gene flow is common in nature, especially in systems driven by physical processes such as wind or water currents. As information about levels of asymmetric gene flow among populations is essential for the correct interpretation of the distribution of contemporary genetic diversity within species, this should not be overlooked. To obtain information on asymmetric migration patterns from genetic data, complex models based on maximum-likelihood or Bayesian approaches generally need to be employed, often at great computational cost. Here, a new simpler and more efficient approach for understanding gene flow patterns is presented. This approach allows the estimation of directional components of genetic divergence between pairs of populations at low computational effort, using any of the classical or modern measures of genetic differentiation. These directional measures of genetic differentiation can further be used to calculate directional relative migration and to detect asymmetries in gene flow patterns. This can be done in a user-friendly web application called divMigrate-online introduced in this study. Using simulated data sets with known gene flow regimes, we demonstrate that the method is capable of resolving complex migration patterns under a range of study designs.
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Little attention has been paid to the evolutionary consequences of the colonizing dynamics and succession processes following glacier retreat. Here we studied hybrid populations that have recently formed and established on glacier forefields of the European Alps owing to secondary contact of a lowland colonizer with a subalpine species. We analyzed the composition of two hybrid populations between Salix purpurea and Salix helvetica with nine microsatellite markers by using Bayesian methods (structure and NewHybrids), and simulations. We also studied niche differentiation between the hybrids and the parental species based on indicator values, soil pH and water retention potential measurements. Allelic structure of hybrids confirms the assumed parentage and in situ origin of the crosses on two independent sites within the last decades. Both hybrid populations comprised F1 and later generation hybrids (F2 and backcrosses), confirming hybrid fertility. The parental species showed significant differences in niche characteristics for temperature, soil pH, nutrients and moisture. Remarkably, the hybrids exhibited a higher tolerance to cold temperatures, nutrient-poor and acidic soils than either parent. Our results show that willow hybrids originated after glacier retreat and have established persistent populations within a few decades. One factor contributing to hybrid establishment in sympatry with their parents is their ability to occupy more extreme niches than either parental species within a mosaic-like pattern of microhabitats on the forefield. Introgression and/or transgressive segregation may have resulted in novel genotypes that are able to expand the ecological spectrum of either parent.Heredity advance online publication, 16 March 2016; doi:10.1038/hdy.2016.14.
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Hybridization may drive rare taxa to extinction through genetic swamping, where the rare form is replaced by hybrids, or by demographic swamping, where population growth rates are reduced due to the wasteful production of maladaptive hybrids. Conversely, hybridization may rescue the viability of small, inbred populations. Understanding the factors that contribute to destructive versus constructive outcomes of hybridization is key to managing conservation concerns. Here we survey the literature for studies of hybridization and extinction to identify the ecological, evolutionary, and genetic factors that critically affect extinction risk through hybridization. We find that while extinction risk is highly situation dependent, genetic swamping is much more frequent than demographic swamping. In addition, human involvement is associated with increased risk and high reproductive isolation with reduced risk. Although climate change is predicted to increase the risk of hybridization-induced extinction, we find little empirical support for this prediction. Similarly, theoretical and experimental studies imply that genetic rescue through hybridization may be equally or more probable than demographic swamping, but our literature survey failed to support this claim. We conclude that halting the introduction of hybridization-prone exotics and restoring mature and diverse habitats that are resistant to hybrid establishment should be management priorities. This article is protected by copyright. All rights reserved.
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Studies of hybridization and introgression and, in particular, the identification of admixed individuals in natural populations benefit from the use of diagnostic genetic markers that reliably differentiate pure species from each other and their hybrid forms. Such diagnostic markers are often infrequent in the genomes of closely related species, and genomewide data facilitate their discovery. We used whole-genome data from Illumina HiSeqS2000 sequencing of two recently diverged (600,000 years) and hybridizing, avian, sister species, the Saltmarsh (Ammodramus caudacutus) and Nelson's (A. nelsoni) Sparrow, to develop a suite of diagnostic markers for high-resolution identification of pure and admixed individuals. We compared the microsatellite repeat regions identified in the genomes of the two species and selected a subset of 37 loci that differed between the species in repeat number. We screened these loci on 12 pure individuals of each species and report on the 34 that successfully amplified. From these, we developed a panel of the 12 most diagnostic loci, which we evaluated on 96 individuals, including individuals from both allopatric populations and sympatric individuals from the hybrid zone. Using simulations, we evaluated the power of the marker panel for accurate assignments of individuals to their appropriate pure species and hybrid genotypic classes (F1, F2, and backcrosses). The markers proved highly informative for species discrimination and had high accuracy for classifying admixed individuals into their genotypic classes. These markers will aid future investigations of introgressive hybridization in this system and aid conservation efforts aimed at monitoring and preserving pure species. Our approach is transferable to other study systems consisting of closely related and incipient species.
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A diverse array of molecular markers and constantly evolving analytical approaches have been employed to reconstruct the invasion histories of the most notorious invasions. Detailed information on the source(s) of introduction, invasion route, type of vectors, number of independent introductions, and pathways of secondary spread has been corroborated for a large number of biological invasions. In this review, I present the promises and limitations of current techniques while discussing future directions. Broad phylogeographic surveys of native and introduced populations have traced back invasion routes with surprising precision. These approaches often further clarify species boundaries and reveal complex patterns of genetic relationships with non-invasive relatives. Moreover, fine scale analyses of population genetics or genomics allow deep inferences on the colonization dynamics across invaded ranges, and can reveal the extent of gene flow among populations across various geographical scales, major demographic events such as genetic bottlenecks as well as other important evolutionary events such as hybridization with native taxa, inbreeding, and selective sweeps. Genetic data has been often corroborated successfully with historical, geographical and ecological data to enable a comprehensive reconstruction of the invasion process. The advent of next generation sequencing, along with the availability of extensive databases of repository sequences generated by barcoding projects opens the opportunity to broadly monitor biodiversity, to identify early invasions, and to quantify failed invasions that would otherwise remain inconspicuous to the human eye. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
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Biological invasions offer unique opportunities to investigate evolutionary dynamics at the peripheries of expanding pop- ulations. Here, we examine genetic patterns associated with admixture between two distinct invasive lineages of the European green crab, Carcinus maenas L., independently introduced to the northwest Atlantic. Previous investigations based on mito- chondrial DNA sequences demonstrated that larval dispersal driven by advective currents could explain observed southward displacement of an admixture zone between the two invasions. Comparison of published mitochondrial results with new nuclear data from nine microsatellite loci, however, reveals striking discordance in their introgression patterns. Specifically, introgression of mitochondrial genomes relative to nuclear background suggests that demographic processes such as sex- biased reproductive dynamics and population size imbalances— and not solely larval dispersal—play an important role in driving the evolution of the genetic cline. In particular, the unpredicted introgression of mitochondrial alleles against the direction of mean larval dispersal in the region is consistent with recent models invoking similar demographic processes to explain movements of genes into invading populations. These observations have important implications for understanding historical shifts in C. maenas range limits, and more generally for inferences of larval dispersal based on genetic data.
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Hybrid zones provide unprecedented opportunity for the study of the evolution of reproductive isolation, and the extent of hybridization across individuals and genomes can illuminate the degree of isolation. We examine patterns of interchromosomal linkage disequilibrium (ILD) and the presence of hybridization in Atlantic cod, Gadus morhua, in previously identified hybrid zones in the North Atlantic. Here, previously identified clinal loci were mapped to the cod genome with most (∼70%) occurring in or associated with (<5 kb) coding regions representing a diverse array of possible functions and pathways. Despite the observation that clinal loci were distributed across three linkage groups, elevated ILD was observed among all groups of clinal loci and strongest in comparisons involving a region of low recombination along linkage group 7. Evidence of ILD supports a hypothesis of divergence hitchhiking transitioning to genome hitchhiking consistent with reproductive isolation. This hypothesis is supported by Bayesian characterization of hybrid classes present and we find evidence of common F1 hybrids in several regions consistent with frequent interbreeding, yet little evidence of F2 or backcrossed individuals. This work suggests that significant barriers to hybridization and introgression exist among these co-occurring groups of cod either through strong selection against hybrid individuals, or genetic incompatibility and intrinsic barriers to hybridization. In either case, the presence of strong clinal trends, and little gene flow despite extensive hybridization supports a hypothesis of reproductive isolation and cryptic speciation in Atlantic cod. Further work is required to test the degree and nature of reproductive isolation in this species.
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The hypothesis that interspecific hybridisation promotes invasiveness has received much recent attention, but tests of the hypothesis can suffer from important limitations. Here, we provide the first systematic review of studies experimentally testing the hybridisation-invasion (H-I) hypothesis in plants, animals and fungi. We identified 72 hybrid systems for which hybridisation has been putatively associated with invasiveness, weediness or range expansion. Within this group, 15 systems (comprising 34 studies) experimentally tested performance of hybrids vs. their parental species and met our other criteria. Both phylogenetic and non-phylogenetic meta-analyses demonstrated that wild hybrids were significantly more fecund and larger than their parental taxa, but did not differ in survival. Resynthesised hybrids (which typically represent earlier generations than do wild hybrids) did not consistently differ from parental species in fecundity, survival or size. Using meta-regression, we found that fecundity increased (but survival decreased) with generation in resynthesised hybrids, suggesting that natural selection can play an important role in shaping hybrid performance – and thus invasiveness – over time. We conclude that the available evidence supports the H-I hypothesis, with the caveat that our results are clearly driven by tests in plants, which are more numerous than tests in animals and fungi.
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Genetic admixture of divergent intraspecific lineages is increasingly suspected to have an important role in the success of colonising populations. However, admixture is not a universally beneficial genetic phenomenon. Selection is typically expected to favour locally adapted genotypes and can act against admixed individuals, suggesting that there are some conditions under which admixture will have negative impacts on population fitness. Therefore, it remains unclear how often admixture acts as a true driver of colonisation success. Here, we review the population consequences of admixture and discuss its costs and benefits across a broad spectrum of ecological contexts. We critically evaluate the evidence for a causal role of admixture in successful colonisation, and consider that role more generally in driving population range expansion.
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This software package provides an R-based framework to make use of multi-core computers when running analyses in the population genetics program STRUCTURE. It is especially addressed to those users of STRUCTURE dealing with numerous and repeated data analyses, and who could take advantage of an efficient script to automatically distribute STRUCTURE jobs among multiple processors. It also consists of additional functions to divide analyses among combinations of populations within a single data set without the need to manually produce multiple projects, as it is currently the case in STRUCTURE. The package consists of two main functions: MPI_structure() and parallel_structure() as well as an example data file. We compared the performance in computing time for this example data on two computer architectures and showed that the use of the present functions can result in several-fold improvements in terms of computation time. ParallelStructure is freely available at https://r-forge.r-project.org/projects/parallstructure/.
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Massively parallel short-read sequencing technologies, coupled with powerful software platforms, are enabling investigators to analyse tens of thousands of genetic markers. This wealth of data is rapidly expanding and allowing biological questions to be addressed with unprecedented scope and precision. The sizes of the data sets are now posing significant data processing and analysis challenges. Here we describe an extension of the Stacks software package to efficiently use genotype-by-sequencing data for studies of populations of organisms. Stacks now produces core population genomic summary statistics and SNP-by-SNP statistical tests. These statistics can be analysed across a reference genome using a smoothed sliding window. Stacks also now provides several output formats for several commonly used downstream analysis packages. The expanded population genomics functions in Stacks will make it a useful tool to harness the newest generation of massively parallel genotyping data for ecological and evolutionary genetics.
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We present a new R package, diveRsity, for the calculation of various diversity statistics, including common diversity partitioning statistics (θ, GST) and population differentiation statistics (DJost, , χ2 test for population heterogeneity), among others. The package calculates these estimators along with their respective bootstrapped confidence intervals for loci, sample population pairwise and global levels. Various plotting tools are also provided for a visual evaluation of estimated values, allowing users to critically assess the validity and significance of statistical tests from a biological perspective.diveRsity has a set of unique features, which facilitate the use of an informed framework for assessing the validity of the use of traditional F-statistics for the inference of demography, with reference to specific marker types, particularly focusing on highly polymorphic microsatellite loci. However, the package can be readily used for other co-dominant marker types (e.g. allozymes, SNPs).Detailed examples of usage and descriptions of package capabilities are provided. The examples demonstrate useful strategies for the exploration of data and interpretation of results generated by diveRsity. Additional online resources for the package are also described, including a GUI web app version intended for those with more limited experience using R for statistical analysis.
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Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near-instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky–Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization.
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Many aspects of the historical relationships between populations in a species are reflected in genetic data. Inferring these relationships from genetic data, however, remains a challenging task. In this paper, we present a statistical model for inferring the patterns of population splits and mixtures in multiple populations. In our model, the sampled populations in a species are related to their common ancestor through a graph of ancestral populations. Using genome-wide allele frequency data and a Gaussian approximation to genetic drift, we infer the structure of this graph. We applied this method to a set of 55 human populations and a set of 82 dog breeds and wild canids. In both species, we show that a simple bifurcating tree does not fully describe the data; in contrast, we infer many migration events. While some of the migration events that we find have been detected previously, many have not. For example, in the human data, we infer that Cambodians trace approximately 16% of their ancestry to a population ancestral to other extant East Asian populations. In the dog data, we infer that both the boxer and basenji trace a considerable fraction of their ancestry (9% and 25%, respectively) to wolves subsequent to domestication and that East Asian toy breeds (the Shih Tzu and the Pekingese) result from admixture between modern toy breeds and "ancient" Asian breeds. Software implementing the model described here, called TreeMix, is available at http://treemix.googlecode.com.
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We present STRUCTURE HARVESTER (available at http://taylor0.biology.ucla.edu/structureHarvester/), a web-based program for collating results generated by the program STRUCTURE. The program provides a fast way to assess and visualize likelihood values across multiple values of K and hundreds of iterations for easier detection of the number of genetic groups that best fit the data. In addition, STRUCTURE HARVESTER will reformat data for use in downstream programs, such as CLUMPP. KeywordsStructure–Population structure–Population genetics–Evanno method–Visualization–Clustering
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The evolutionary genetics of invasive species has been relatively unexplored, but could offer insights into mechanisms of invasions. Recent studies suggest that the invasion success of many species might depend more heavily on their ability to respond to natural selection than on broad physiological tolerance or plasticity. Thus, these studies stress the importance of genetic architecture, selection upon which could result in evolutionary adaptations and possibly speciation. For instance, epistatic interactions and the action of a few genes could facilitate invasion success. These findings emphasize the utility of genomic approaches for determining invasion mechanisms, through analysis of gene expression, gene interactions, and genomic rearrangements that are associated with invasion events.
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Next-generation sequencing technologies are revolutionizing the field of evolutionary biology, opening the possibility for genetic analysis at scales not previously possible. Research in population genetics, quantitative trait mapping, comparative genomics, and phylogeography that was unthinkable even a few years ago is now possible. More importantly, these next-generation sequencing studies can be performed in organisms for which few genomic resources presently exist. To speed this revolution in evolutionary genetics, we have developed Restriction site Associated DNA (RAD) genotyping, a method that uses Illumina next-generation sequencing to simultaneously discover and score tens to hundreds of thousands of single-nucleotide polymorphism (SNP) markers in hundreds of individuals for minimal investment of resources. In this chapter, we describe the core RAD-seq protocol, which can be modified to suit a diversity of evolutionary genetic questions. In addition, we discuss bioinformatic considerations that arise from unique aspects of next-generation sequencing data as compared to traditional marker-based approaches, and we outline some general analytical approaches for RAD-seq and similar data. Despite considerable progress, the development of analytical tools remains in its infancy, and further work is needed to fully quantify sampling variance and biases in these data types.
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Despite the great utility of mitochondrial DNA (mtDNA) sequence data in population genetics and phylogenetics, key parameters describing the process of mitochondrial mutation (e.g., the rate and spectrum of mutational change) are based on few direct estimates. Furthermore, the variation in the mtDNA mutation process within species or between lineages with contrasting reproductive strategies remains poorly understood. In this study, we directly estimate the mtDNA mutation rate and spectrum using Daphnia pulex mutation-accumulation (MA) lines derived from sexual (cyclically parthenogenetic) and asexual (obligately parthenogenetic) lineages. The nearly complete mitochondrial genome sequences of 82 sexual and 47 asexual MA lines reveal high mtDNA mutation rate of 1.37 × 10(-7) and 1.73 × 10(-7) per nucleotide per generation, respectively. The Daphnia mtDNA mutation rate is among the highest in eukaryotes, and its spectrum is dominated by insertions and deletions (70%), largely due to the presence of mutational hotspots at homopolymeric nucleotide stretches. Maximum likelihood estimates of the Daphnia mitochondrial effective population size reveal that between five and ten copies of mitochondrial genomes are transmitted per female per generation. Comparison between sexual and asexual lineages reveals no statistically different mutation rates and highly similar mutation spectra.
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Hybridization has a major role in evolution-from the introgression of important phenotypic traits between species, to the creation of new species through hybrid speciation. Molecular studies of hybridization aim to understand the class of hybrids and the frequency of introgression, detect the signature of ancient hybridization, and understand the behaviour of introgressed loci in their new genomic background. This often involves a large investment in the design and application of molecular markers, leading to a compromise between the depth and breadth of genomic data. New techniques designed to assay a large sub-section of the genome, in association with next-generation sequencing (NGS) technologies, will allow genome-wide hybridization and introgression studies in organisms with no prior sequence data. These detailed genotypic data will unite the breadth of sampling of loci characteristic of population genetics with the depth of sequence information associated with molecular phylogenetics. In this review, we assess the theoretical and methodological constraints that limit our understanding of natural hybridization, and promote the use of NGS for detecting hybridization and introgression between non-model organisms. We also make recommendations for the ways in which emerging techniques, such as pooled barcoded amplicon sequencing and restriction site-associated DNA tags, should be used to overcome current limitations, and enhance our understanding of this evolutionary significant process.
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In a single well-mixed population, equally abundant neutral alleles are equally likely to persist. However, in spatially complex populations structured by an asymmetric dispersal mechanism, such as a coastal population where larvae are predominantly moved downstream by currents, the eventual frequency of neutral haplotypes will depend on their initial spatial location. In our study of the progression of two spatially separate, genetically distinct introductions of the European green crab (Carcinus maenas) along the coast of eastern North America, we captured this process in action. We documented the shift of the genetic cline in this species over 8 y, and here we detail how the upstream haplotypes are beginning to dominate the system. This quantification of an evolving genetic boundary in a coastal system demonstrates that novel genetic alleles or haplotypes that arise or are introduced into upstream retention zones (regions whose export of larvae is not balanced by import from elsewhere) will increase in frequency in the entire system. This phenomenon should be widespread when there is asymmetrical dispersal, in the oceans or on land, suggesting that the upstream edge of a species' range can influence genetic diversity throughout its distribution. Efforts to protect the upstream edge of an asymmetrically dispersing species' range are vital to conserving genetic diversity in the species.
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Despite the power of massively parallel sequencing platforms, a drawback is the short length of the sequence reads produced. We demonstrate that short reads can be locally assembled into longer contigs using paired-end sequencing of restriction-site associated DNA (RAD-PE) fragments. We use this RAD-PE contig approach to identify single nucleotide polymorphisms (SNPs) and determine haplotype structure in threespine stickleback and to sequence E. coli and stickleback genomic DNA with overlapping contigs of several hundred nucleotides. We also demonstrate that adding a circularization step allows the local assembly of contigs up to 5 kilobases (kb) in length. The ease of assembly and accuracy of the individual contigs produced from each RAD site sequence suggests RAD-PE sequencing is a useful way to convert genome-wide short reads into individually-assembled sequences hundreds or thousands of nucleotides long.
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Interspecific hybridization plays an important role in facilitating adaptive evolutionary change. More specifically, recent studies have demonstrated that hybridization may dramatically influence the establishment, spread, and impact of invasive populations. In Japan, previous genetic evidence for the presence of two non-native congeners, the European green crab Carcinus maenas and the Mediterranean green crab C. aestuarii, has raised questions regarding the possibility of hybridization between these sister species. Here I present analysis based on both nuclear microsatellites and the mitochondrial cytochrome C oxidase subunit I (COI) gene which unambiguously argues for a hybrid origin of Japanese Carcinus. Despite the presence of mitochondrial lineages derived from both C. maenas and C. aestuarii, the Japanese population is panmictic at nuclear loci and has achieved cytonuclear equilibrium throughout the sampled range in Japan. Furthermore, analysis of admixture at nuclear loci indicates dramatic introgression of the C. maenas mitochondrial genome into a predominantly C. aestuarii nuclear background. These patterns, along with inferences drawn from the observational record, argue for a hybridization event pre-dating the arrival of Carcinus in Japan. The clarification of both invasion history and evolutionary history afforded by genetic analysis provides information that may be critically important to future studies aimed at assessing risks posed by invasive Carcinus populations to Japan and the surrounding region.
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Next-generation sequencing technology provides novel opportunities for gathering genome-scale sequence data in natural populations, laying the empirical foundation for the evolving field of population genomics. Here we conducted a genome scan of nucleotide diversity and differentiation in natural populations of threespine stickleback (Gasterosteus aculeatus). We used Illumina-sequenced RAD tags to identify and type over 45,000 single nucleotide polymorphisms (SNPs) in each of 100 individuals from two oceanic and three freshwater populations. Overall estimates of genetic diversity and differentiation among populations confirm the biogeographic hypothesis that large panmictic oceanic populations have repeatedly given rise to phenotypically divergent freshwater populations. Genomic regions exhibiting signatures of both balancing and divergent selection were remarkably consistent across multiple, independently derived populations, indicating that replicate parallel phenotypic evolution in stickleback may be occurring through extensive, parallel genetic evolution at a genome-wide scale. Some of these genomic regions co-localize with previously identified QTL for stickleback phenotypic variation identified using laboratory mapping crosses. In addition, we have identified several novel regions showing parallel differentiation across independent populations. Annotation of these regions revealed numerous genes that are candidates for stickleback phenotypic evolution and will form the basis of future genetic analyses in this and other organisms. This study represents the first high-density SNP-based genome scan of genetic diversity and differentiation for populations of threespine stickleback in the wild. These data illustrate the complementary nature of laboratory crosses and population genomic scans by confirming the adaptive significance of previously identified genomic regions, elucidating the particular evolutionary and demographic history of such regions in natural populations, and identifying new genomic regions and candidate genes of evolutionary significance.
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Demographic models built from genetic data play important roles in illuminating prehistorical events and serving as null models in genome scans for selection. We introduce an inference method based on the joint frequency spectrum of genetic variants within and between populations. For candidate models we numerically compute the expected spectrum using a diffusion approximation to the one-locus, two-allele Wright-Fisher process, involving up to three simultaneous populations. Our approach is a composite likelihood scheme, since linkage between neutral loci alters the variance but not the expectation of the frequency spectrum. We thus use bootstraps incorporating linkage to estimate uncertainties for parameters and significance values for hypothesis tests. Our method can also incorporate selection on single sites, predicting the joint distribution of selected alleles among populations experiencing a bevy of evolutionary forces, including expansions, contractions, migrations, and admixture. We model human expansion out of Africa and the settlement of the New World, using 5 Mb of noncoding DNA resequenced in 68 individuals from 4 populations (YRI, CHB, CEU, and MXL) by the Environmental Genome Project. We infer divergence between West African and Eurasian populations 140 thousand years ago (95% confidence interval: 40-270 kya). This is earlier than other genetic studies, in part because we incorporate migration. We estimate the European (CEU) and East Asian (CHB) divergence time to be 23 kya (95% c.i.: 17-43 kya), long after archeological evidence places modern humans in Europe. Finally, we estimate divergence between East Asians (CHB) and Mexican-Americans (MXL) of 22 kya (95% c.i.: 16.3-26.9 kya), and our analysis yields no evidence for subsequent migration. Furthermore, combining our demographic model with a previously estimated distribution of selective effects among newly arising amino acid mutations accurately predicts the frequency spectrum of nonsynonymous variants across three continental populations (YRI, CHB, CEU).
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We describe a model-based clustering method for using multilocus genotype data to infer population structure and assign individuals to populations. We assume a model in which there are K populations (where K may be unknown), each of which is characterized by a set of allele frequencies at each locus. Individuals in the sample are assigned (probabilistically) to populations, or jointly to two or more populations if their genotypes indicate that they are admixed. Our model does not assume a particular mutation process, and it can be applied to most of the commonly used genetic markers, provided that they are not closely linked. Applications of our method include demonstrating the presence of population structure, assigning individuals to populations, studying hybrid zones, and identifying migrants and admixed individuals. We show that the method can produce highly accurate assignments using modest numbers of loci—e.g., seven microsatellite loci in an example using genotype data from an endangered bird species. The software used for this article is available from http://www.stats.ox.ac.uk/~pritch/home.html.
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Hybrid zones formed between recently diverged populations offer an opportunity to study the mechanisms underlying reproductive isolation and the process of speciation. Here, we use a combination of analytical theory and explicit forward simulations to describe how selection against hybrid genotypes impacts patterns of introgression across genomic and geographic space. By describing how lineages move across the hybrid zone, in a model without coalescence, we add to modern understanding of how clines form and how parental haplotypes are broken up during introgression. Working with lineages makes it easy to see that clines form in about 1/s generations, where s is the strength of selection against hybrids,and linked clines persist over a genomic scale of 1/T, where T is the age, in generations,of the hybrid zone.Locally disadvantageous alleles tend to exist as small families, whose lineages trace back to the side from which they originated at speed √(s) dispersal distances per generation.The lengths of continuous tracts of ancestry provide an additional source of information:blocks of ancestry surrounding incompatibilities can be substantially longer than the genome-wide average block length at the same spatial location, an observation that might be used to identify candidate targets of selection. This article is protected by copyright. All rights reserved.
Article
Ecophenotypic differentiation among replicate ecotype pairs within a species complex is often attributed to independent outcomes of parallel divergence driven by adaptation to similar environmental contrasts. However, the extent to which parallel phenotypic and genetic divergence patterns have emerged independently is increasingly questioned by population genomic studies. Here we document the extent of genetic differentiation within and among two geographical replicates of the coastal and marine ecotypes of the European anchovy (Engraulis encrasicolus) gathered from Atlantic and Mediterranean locations. Using a genome-wide dataset of RAD-derived SNPs, we show that habitat type (marine vs. coastal) is the most important component of genetic differentiation among populations of anchovy. By analyzing the joint allele frequency spectrum of each coastal-marine ecotype pair, we show that genomic divergence patterns between ecotypes can be explained by a post-glacial secondary contact following a long period of allopatric isolation (ca. 300 kyrs). We found strong support for a model including heterogeneous migration among loci, suggesting that secondary gene flow has eroded past differentiation at different rates across the genome. Markers experiencing reduced introgression exhibited strongly correlated differentiation levels among Atlantic and Mediterranean regions. These results support that partial reproductive isolation and parallel genetic differentiation among replicate pairs of anchovy ecotypes are largely due to a common divergence history prior to secondary contact. They moreover provide comprehensive insights into the origin of a surprisingly strong fine-scale genetic structuring in a high gene flow marine fish, which should improve stock management and conservation actions. This article is protected by copyright. All rights reserved.
Article
Haplotype networks are an intuitive method for visualising relationships between individual genotypes at the population level. Here, we present popart, an integrated software package that provides a comprehensive implementation of haplotype network methods, phylogeographic visualisation tools and standard statistical tests, together with publication-ready figure production. popart also provides a platform for the implementation and distribution of new network-based methods – we describe one such new method, integer neighbour-joining. The software is open source and freely available for all major operating systems.
Article
The European green crab, Carcinus maenas, was first observed in the western Atlantic in the 19th century (from New Jersey to Massachusetts, USA). A northward expansion along the coast of New England has been observed in the first half of the second century. The green crab was observed in Canadian waters in Passamoquoddy Bay in 1951. The species has gradually invaded the Bay of Fundy in the 1950s, and the Atlantic coast of Nova Scotia from the 1960s to the mid 1990s, and reached the southern Gulf of St. Lawrence in the mid 1990s. Further westward expansion in the southern Gulf of St. Lawrence has been confirmed along the eastern coast of Prince Edward Island in 1997 and more recently in the Northumberland Strait at the border between Nova Scotia and New Brunswick.
Article
Species invasions cause significant ecological and economic damage, and genetic information is important to understanding and managing invasive species. In the ocean, many invasive species have high dispersal and gene flow, lowering the discriminatory power of traditional genetic approaches. High-throughput sequencing holds tremendous promise for increasing resolution and illuminating the relative contributions of selection and drift in marine invasion, but has not yet been used to compare the diversity and dynamics of a high-dispersal invader in its native and invaded ranges. We test a transcriptome-based approach in the European green crab (Carcinus maenas), a widespread invasive species with high gene flow and a well-known invasion history, in two native and five invasive populations. A panel of 10,809 transcriptome-derived nuclear SNPs identified significant population structure among highly bottlenecked invasive populations that were previously undifferentiated with traditional markers. Comparing the full data set and a subset of 9,246 putatively neutral SNPs strongly suggested that non-neutral processes are the primary driver of population structure within the species' native range, while neutral processes appear to dominate in the invaded range. Non-neutral native range structure coincides with significant differences in intraspecific thermal tolerance, suggesting temperature as a potential selective agent. These results underline the importance of adaptation in shaping intraspecific differences even in high-gene flow marine invasive species. They also demonstrate that high-throughput approaches have broad utility in determining neutral structure in recent invasions of such species. Together, neutral and non-neutral data derived from high-throughput approaches may increase understanding of invasion dynamics in high-dispersal species. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
Article
Genetic adaptation—heritable changes that alter an organism’s performance—may facilitate invasion at several scales, but is seldom considered in predicting and managing marine invasions. However, a growing body of research—largely based on emerging genetic approaches—suggests that adaptation is possible and potentially widespread in the marine realm. Here, I review evidence for adaptation in marine invasion, considering both quantitative and genetic studies. Quantitative studies, which consider trait-based differences between populations or individuals without directly examining genetic makeup, have suggested local adaptation in several high-profile species. This implies that invasion risk may not be constant from population to population within a species, a key assumption of most invasion models. However, in many quantitative studies, the effects of heritable adaptive changes may be confounded with the effects of plasticity. Molecular approaches can help disentangle these effects, and studies at the genomic level are beginning to elucidate the specific genetic patterns and pathways underlying adaptation in invasion. While studies at this scale are currently rare in the marine invasion literature, they are likely to become increasingly prevalent—and useful—now that next-generation sequencing approaches have become tractable in non-model systems. Both traditional and emerging genetic approaches can improve our understanding of adaptation in marine invasions, and can aid managers in making accurate predictions of invasion spread and risk.
Article
The identification of the genetic structure of populations from multilocus genotype data has become a central component of modern population-genetic data analysis. Application of model-based clustering programs often entails a number of steps, in which the user considers different modeling assumptions, compares results across different pre-determined values of the number of assumed clusters (a parameter typically denoted K), examines multiple independent runs for each fixed value of K, and distinguishes among runs belonging to substantially distinct clustering solutions. Here, we present Clumpak (Cluster Markov Packager Across K), a method that automates the post-processing of results of model-based population structure analyses. For analyzing multiple independent runs at a single K value, Clumpak identifies sets of highly similar runs, separating distinct groups of runs that represent distinct modes in the space of possible solutions. This procedure, which generates a consensus solution for each distinct mode, is performed by the use of a Markov clustering algorithm that relies on a similarity matrix between replicate runs, as computed by the software Clumpp. Next, Clumpak identifies an optimal alignment of inferred clusters across different values of K, extending a similar approach implemented for a fixed K in Clumpp, and simplifying the comparison of clustering results across different K values. Clumpak incorporates additional features, such as implementations of methods for choosing K and comparing solutions obtained by different programs, models, or data subsets. Clumpak, available at http://clumpak.tau.ac.il, simplifies the use of model-based analyses of population structure in population genetics and molecular ecology. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
Article
Along the central coast of Maine most female Carcinus maenas extruded their eggs in spring. The smallest ovigerous female was 34 mm in carapace width. Mating occurred from July to October, and in all mating pairs the male was larger than the female. Megalopae and Stage 1 crabs did not settle until late August, growing only to a mean of 5.5 mm carapace width (Stage 5) before winter. Renewed growth began the following June, and juveniles grew to 13-25 mm carapace width by their second winter. Most mature males molted by the end of July, whereas mature females molted from July to October, while guarded by males waiting to mate with them. On the central coast of Maine, therefore, C. maenas matures when 2-3 years old, breeds 2-3 times, and generation time is a minimum of 3 years. Compared with warmer water populations in southern Britain and Holland, the Maine coast population of C. maenas has later settlement of megalopae, slower growth, delayed maturity, longer generation time, and a longer life span. Such differences may account for the inability of populations to establish themselves in waters much colder than those of the central coast of Maine.
Article
As global warming accelerates, there is increasing concern about how ecosystems may change as a result of species loss and replacement. Here, we examined the thermal physiology of the European green crab (Carcinus maenas Linnaeus 1758), a globally invasive species, along three parallel thermal gradients in its native and invasive ranges. At each site, we assessed cardiac physiology to determine heat and cold tolerance and acclimatory plasticity. We found that, overall, the species is highly tolerant of both heat and cold, and that it survives higher temperatures than co-occurring native marine crustaceans. Further, we found that both heat and cold tolerance are plastic in response to short-term acclimation (18-31 days at either 5 or 25°C). Comparing patterns within ranges, we found latitudinal gradients in thermal tolerance in the native European range and in the invasive range in eastern North America. This pattern is strongest in the native range, and likely evolved there. Because of a complicated invasion history, the latitudinal pattern in the eastern North American invasive range may be due either to rapid adaptation post-invasion or to adaptive differences between the ancestral populations that founded the invasion. Overall, the broad thermal tolerance ranges of green crabs, which may facilitate invasion of novel habitats, derive from high inherent eurythermality and acclimatory plasticity and potentially adaptive differentiation among populations. The highly flexible physiology that results from these capacities may represent the hallmark of a successful invasive species, and may provide a model for success in a changing world.
Article
Abstract In order to improve the yield of bay scallop Argopecten irradians by exploiting geographic subspecies heterosis, crosses between and within two subspecies, the northern A. i. irradians (Lamarck) and the southern A. i. concentricus (Say), were created and the offspring were cultured under the same environmental conditions. The two parental populations were collected from Bohai Bay in northern China and Beibu Bay in southern China, which were distinct in particular shell colours. The results indicated that the shell colour of bay scallop was inheritable and could be used as a morphological mark to distinguish hybrid and purebred individuals. At harvest, hybrid offspring always produced a significantly higher yield than purebred offspring. Positive heterosis was achieved for shell length, shell height, shell width, total weight and adductor weight, which was 5.02, 5.22, 3.88, 7.53 and 9.47 respectively. Hybrid gain was 10.86% for shell length, 10.48% for shell height, 9.77% for shell width, 34.90% for total weight and 41.69% for adductor weight, respectively, and all were significantly >5%. The present study reveals that it is effective for improving yield by hybridization between different geographic subspecies in the bay scallop.
Article
This paper elaborates on a hybrid index that utilizes information from genetic markers to quantify the genetic contribution of hybridizing species to individuals of unknown ancestry. Dominant markers will only lead to reliable and accurate estimates of hybrid index in later generation hybrids. In contrast, codominant markers can be fully resolved and their use is unproblematic. For both types of markers and allele frequencies that differ substantially between parental species (FST ≥ 0.17), a hybrid index based on 35–45 loci will have a nearly minimal confidence interval. Estimates of hybrid index are robust to modest errors in estimates of parental allele frequencies.
Article
Aim To determine timing, source and vector for the recent introduction of the European green crab, Carcinus maenas (Linnaeus, 1758), to Newfoundland using multiple lines of evidence. Location Founding populations in Placentia Bay, Newfoundland, Canada and potential source populations in the north-west Atlantic (NWA) and Europe. Methods We analysed mitochondrial and microsatellite genetic data from European and NWA populations sampled during 1999–2002 to determine probable source locations and vectors for the Placentia Bay introduction discovered in 2007. We also analysed Placentia Bay demographic data and shipping records to look for congruent patterns with genetic analyses. Results Demographic data and surveys suggested that C. maenas populations are established and were in Placentia Bay for several years (c. 2002) prior to discovery. Genetic data corroboratively suggested central/western Scotian Shelf populations (e.g., Halifax) as the likely source area for the anthropogenic introduction. These Scotian Shelf populations were within an admixture zone made up of genotypes from both the earlier (early 1800s) and later (late 1900s) introductions of the crab to the NWA from Europe. Placentia Bay also exhibited this mixed ancestry. Probable introduction vectors included vessel traffic and shipping, especially vessels carrying ballast water. Main conclusions Carcinus maenas overcame considerable natural barriers (i.e., coastal and ocean currents) via anthropogenic transport to become established and abundant in Newfoundland. Our study thus demonstrates how non-native populations can be important secondary sources of introduction especially when aided by human transport. Inference of source populations was possible owing to the existence of an admixture zone in central/western Nova Scotia made up of southern and northern genotypes corresponding with the crab’s two historical introductions. Coastal vessel traffic was found to be a likely vector for the crab’s spread to Newfoundland. Our study demonstrates that there is considerable risk for continued introduction or reintroduction of C. maenas throughout the NWA.
Article
Investigating diversity in asexual organisms using molecular markers involves the assignment of individuals to clonal lineages and the subsequent analysis of clonal diversity. Assignment is possible using a distance matrix in combination with a user-specified threshold, defined as the maximum distance between two individuals that are considered to belong to the same clonal lineage. Analysis of clonal diversity requires tests for differences in diversity and clonal composition between populations. We developed two programs, genotype and genodive for such analyses of clonal diversity in asexually reproducing organisms. Additionally, genotype can be used for detecting genotyping errors in studies of sexual organisms.
Article
The emerging field of speciation genomics is advancing our understanding of the evolution of reproductive isolation from the individual gene to a whole-genome perspective. In this new view it is important to understand the conditions under which 'divergence hitchhiking' associated with the physical linkage of gene regions, versus 'genome hitchhiking' associated with reductions in genome-wide rates of gene flow caused by selection, can enhance speciation-with-gene-flow. We describe here a theory predicting four phases of speciation, defined by changes in the relative effectiveness of divergence and genome hitchhiking, and review empirical data in light of the theory. We outline future directions, emphasizing the need to couple next-generation sequencing with selection, transplant, functional genomics, and mapping studies. This will permit a natural history of speciation genomics that will help to elucidate the factors responsible for population divergence and the roles that genome structure and different forms of hitchhiking play in facilitating the genesis of new biodiversity.
Article
The package hierfstat for the statistical software r , created by the R Development Core Team, allows the estimate of hierarchical F -statistics from a hierarchy with any numbers of levels. In addition, it allows testing the statistical significance of population differentiation for these different levels, using a generalized likelihood-ratio test. The package hierfstat is available at http://www.unil.ch/popgen/softwares/hierfstat.htm.
Article
India has been underrepresented in genome-wide surveys of human variation. We analyse 25 diverse groups in India to provide strong evidence for two ancient populations, genetically divergent, that are ancestral to most Indians today. One, the 'Ancestral North Indians' (ANI), is genetically close to Middle Easterners, Central Asians, and Europeans, whereas the other, the 'Ancestral South Indians' (ASI), is as distinct from ANI and East Asians as they are from each other. By introducing methods that can estimate ancestry without accurate ancestral populations, we show that ANI ancestry ranges from 39-71% in most Indian groups, and is higher in traditionally upper caste and Indo-European speakers. Groups with only ASI ancestry may no longer exist in mainland India. However, the indigenous Andaman Islanders are unique in being ASI-related groups without ANI ancestry. Allele frequency differences between groups in India are larger than in Europe, reflecting strong founder effects whose signatures have been maintained for thousands of years owing to endogamy. We therefore predict that there will be an excess of recessive diseases in India, which should be possible to screen and map genetically.