Publications by authors named "P Bentzen"

98 Publications

Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic.

Proc Natl Acad Sci U S A 2021 Apr;118(15)

Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Blindern, NO-0316 Oslo, Norway;

The mode and extent of rapid evolution and genomic change in response to human harvesting are key conservation issues. Although experiments and models have shown a high potential for both genetic and phenotypic change in response to fishing, empirical examples of genetic responses in wild populations are rare. Here, we compare whole-genome sequence data of Atlantic cod () that were collected before (early 20th century) and after (early 21st century) periods of intensive exploitation and rapid decline in the age of maturation from two geographically distinct populations in Newfoundland, Canada, and the northeast Arctic, Norway. Our temporal, genome-wide analyses of 346,290 loci show no substantial loss of genetic diversity and high effective population sizes. Moreover, we do not find distinct signals of strong selective sweeps anywhere in the genome, although we cannot rule out the possibility of highly polygenic evolution. Our observations suggest that phenotypic change in these populations is not constrained by irreversible loss of genomic variation and thus imply that former traits could be reestablished with demographic recovery.
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http://dx.doi.org/10.1073/pnas.2025453118DOI Listing
April 2021

Chromosome level reference of Atlantic halibut Hippoglossus hippoglossus provides insight into the evolution of sexual determination systems.

Mol Ecol Resour 2021 Mar 2. Epub 2021 Mar 2.

Biology Department, Dalhousie University, Halifax, NS, Canada.

Changes in the genetic mechanisms that control sexual determination have occurred independently across the tree of life, and with exceptional frequency in teleost fishes. To investigate the genomic changes underlying the evolution of sexual determination, we sequenced a chromosome-level genome, multitissue transcriptomes, and reduced representation population data for the Atlantic halibut (Hippoglossus hippoglossus), which has an XY/XX sex determination mechanism and has recently diverged (0.9-3.8 Ma) from the Pacific halibut (Hippoglossus stenolepis), which has a ZZ/ZW system. We used frequency and coverage-based population approaches to identify a putative sex-determining factor, GSDF. We characterized regions with elevated heterozygosity and linkage disequilibrium indicating suppression of recombination across a nascent sex chromosome. We detected testis-specific expression of GSDF, the sequence of which is highly conserved across flatfishes. Based on evidence from genome-wide association, coverage, linkage disequilibrium, testis and brain transcriptomes, and sequence conservation with other flatfishes, we propose a mechanism for the recent evolution of an XY sex-determination mechanism in Atlantic halibut. Changes to the ancestral sex-determining gene DMRT1 in regulating the downstream gene GSDF probably coincided with GSDF, or a proximal regulatory element of it, becoming the primary sex-determining factor. Our results suggest changes to a small number of elements can have drastic repercussions for the genomic substrate available to sex-specific evolutionary forces, providing insight into how certain elements repeatedly evolve to control sex across taxa. Our chromosome-level assembly, multitissue transcriptomes, and population genomic data provide a valuable resource and understanding of the evolution of sexual systems in fishes.
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http://dx.doi.org/10.1111/1755-0998.13369DOI Listing
March 2021

Environmental Change, If Unaccounted, Prevents Detection of Cryptic Evolution in a Wild Population.

Am Nat 2021 01 25;197(1):29-46. Epub 2020 Nov 25.

AbstractDetecting contemporary evolution requires demonstrating that genetic change has occurred. Mixed effects models allow estimation of quantitative genetic parameters and are widely used to study evolution in wild populations. However, predictions of evolution based on these parameters frequently fail to match observations. Here, we applied three commonly used quantitative genetic approaches to predict the evolution of size at maturity in a wild population of Trinidadian guppies. Crucially, we tested our predictions against evolutionary change observed in common-garden experiments performed on samples from the same population. We show that standard quantitative genetic models underestimated or failed to detect the cryptic evolution of this trait as demonstrated by the common-garden experiments. The models failed because (1) size at maturity and fitness both decreased with increases in population density, (2) offspring experienced higher population densities than their parents, and (3) selection on size was strongest at high densities. When we accounted for environmental change, predictions better matched observations in the common-garden experiments, although substantial uncertainty remained. Our results demonstrate that predictions of evolution are unreliable if environmental change is not appropriately captured in models.
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http://dx.doi.org/10.1086/711874DOI Listing
January 2021

Resistance and resilience of genetic and phenotypic diversity to "black swan" flood events: A retrospective analysis with historical samples of guppies.

Mol Ecol 2021 02 7;30(4):1017-1028. Epub 2021 Jan 7.

Redpath Museum and Department of Biology, McGill University, Montreal, QC, Canada.

Rare extreme "black swan" disturbances can impact ecosystems in many ways, such as destroying habitats, depleting resources, and causing high mortality. In rivers, for instance, exceptional floods that occur infrequently (e.g., so-called "50-year floods") can strongly impact the abundance of fishes and other aquatic organisms. Beyond such ecological effects, these floods could also impact intraspecific diversity by elevating genetic drift or dispersal and by imposing strong selection, which could then influence the population's ability to recover from disturbance. And yet, natural systems might be resistant (show little change) or resilient (show rapid recovery) even to rare extreme events - perhaps as a result of selection due to past events. We considered these possibilities in two rivers where native guppies experienced two extreme floods - one in 2005 and another in 2016. For each river, we selected four sites and used archived "historical" samples to compare levels of genetic and phenotypic diversity before vs. after floods. Genetic diversity was represented by 33 neutral microsatellite markers, and phenotypic diversity was represented by body length and male melanic (black) colour. We found that genetic diversity and population structure was mostly "resistant" to even these extreme floods; whereas the larger impacts on phenotypic diversity were short-lived, suggesting additional "resilience". We discuss the determinants of these two outcomes for guppies facing floods, and then consider the general implications for the resistance and resilience of intraspecific variation to black swan disturbances.
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http://dx.doi.org/10.1111/mec.15782DOI Listing
February 2021

Divergent and linked selection shape patterns of genomic differentiation between European and North American Atlantic salmon (Salmo salar).

Mol Ecol 2020 06 21;29(12):2160-2175. Epub 2020 Jun 21.

Fisheries and Oceans Canada, Northwest Atlantic Fisheries Centre, St. John's, NL, Canada.

As populations diverge many processes can shape genomic patterns of differentiation. Regions of high differentiation can arise due to divergent selection acting on selected loci, genetic hitchhiking of nearby loci, or through repeated selection against deleterious alleles (linked background selection); this divergence may then be further elevated in regions of reduced recombination. Atlantic salmon (Salmo salar) from Europe and North America diverged >600,000 years ago and despite some evidence of secondary contact, the majority of genetic data indicate substantial divergence between lineages. This deep divergence with potential gene flow provides an opportunity to investigate the role of different mechanisms that shape the genomic landscape during early speciation. Here, using 184,295 single nucleotide polymorphisms (SNPs) and 80 populations, we investigate the genomic landscape of differentiation across the Atlantic Ocean with a focus on highly differentiated regions and the processes shaping them. We found evidence of high (mean F  = 0.26) and heterogeneous genomic differentiation between continents. Genomic regions associated with high trans-Atlantic differentiation ranged in size from single loci (SNPs) within important genes to large regions (1-3 Mbp) on four chromosomes (Ssa06, Ssa13, Ssa16 and Ssa19). These regions showed signatures consistent with selection, including high linkage disequilibrium, despite no significant reduction in recombination. Genes and functional enrichment of processes associated with differentiated regions may highlight continental differences in ocean navigation and parasite resistance. Our results provide insight into potential mechanisms underlying differences between continents, and evidence of near-fixed and potentially adaptive trans-Atlantic differences concurrent with a background of high genome-wide differentiation supports subspecies designation in Atlantic salmon.
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http://dx.doi.org/10.1111/mec.15480DOI Listing
June 2020

Multiple decades of stocking has resulted in limited hatchery introgression in wild brook trout () populations of Nova Scotia.

Evol Appl 2020 May 20;13(5):1069-1089. Epub 2020 Feb 20.

Marine Gene Probe Lab Biology Department Dalhousie University Halifax NS Canada.

Many populations of freshwater fishes are threatened with losses, and increasingly, the release of hatchery individuals is one strategy being implemented to support wild populations. However, stocking of hatchery individuals may pose long-term threats to wild populations, particularly if genetic interactions occur between wild and hatchery individuals. One highly prized sport fish that has been heavily stocked throughout its range is the brook trout (). In Nova Scotia, Canada, hatchery brook trout have been stocked since the early 1900s, and despite continued stocking efforts, populations have suffered declines in recent decades. Before this study, the genetic structure of brook trout populations in the province was unknown; however, given the potential negative consequences associated with hatchery stocking, it is possible that hatchery programs have adversely affected the genetic integrity of wild populations. To assess the influence of hatchery supplementation on wild populations, we genotyped wild brook trout from 12 river systems and hatchery brook trout from two major hatcheries using 100 microsatellite loci. Genetic analyses of wild trout revealed extensive population genetic structure among and within river systems and significant isolation-by-distance. Hatchery stocks were genetically distinct from wild populations, and most populations showed limited to no evidence of hatchery introgression (<5% hatchery ancestry). Only a single location had a substantial number of hatchery-derived trout and was located in the only river where a local strain is used for supplementation. The amount of hatchery stocking within a watershed did not influence the level of hatchery introgression. Neutral genetic structure of wild populations was influenced by geography with some influence of climate and stocking indices. Overall, our study suggests that long-term stocking has not significantly affected the genetic integrity of wild trout populations, highlighting the variable outcomes of stocking and the need to evaluate the consequences on a case-by-case basis.
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http://dx.doi.org/10.1111/eva.12923DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7232767PMC
May 2020

Resolving fine-scale population structure and fishery exploitation using sequenced microsatellites in a northern fish.

Evol Appl 2020 May 20;13(5):1055-1068. Epub 2020 Feb 20.

Department of Ocean Sciences Memorial University of Newfoundland St. John's NL Canada.

The resiliency of populations and species to environmental change is dependent on the maintenance of genetic diversity, and as such, quantifying diversity is central to combating ongoing widespread reductions in biodiversity. With the advent of next-generation sequencing, several methods now exist for resolving fine-scale population structure, but the comparative performance of these methods for genetic assignment has rarely been tested. Here, we evaluate the performance of sequenced microsatellites and a single nucleotide polymorphism (SNP) array to resolve fine-scale population structure in a critically important salmonid in north eastern Canada, Arctic Charr (). We also assess the utility of sequenced microsatellites for fisheries applications by quantifying the spatial scales of movement and exploitation through genetic assignment of fishery samples to rivers of origin and comparing these results with a 29-year tagging dataset. Self-assignment and simulation-based analyses of 111 genome-wide microsatellite loci and 500 informative SNPs from 28 populations of Arctic Charr in north-eastern Canada identified largely river-specific genetic structure. Despite large differences (~4X) in the number of loci surveyed between panels, mean self-assignment accuracy was similar with the microsatellite loci and the SNP panel (>90%). Subsequent analysis of 996 fishery-collected samples using the microsatellite panel revealed that larger rivers contribute greater numbers of individuals to the fishery and that coastal fisheries largely exploit individuals originating from nearby rivers, corroborating results from traditional tagging experiments. Our results demonstrate the efficacy of sequence-based microsatellite genotyping to advance understanding of fine-scale population structure and harvest composition in northern and understudied species.
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http://dx.doi.org/10.1111/eva.12922DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7232759PMC
May 2020

Parasite diversity and ecology in a model species, the guppy () in Trinidad.

R Soc Open Sci 2020 Jan 22;7(1):191112. Epub 2020 Jan 22.

Biosciences, University of Exeter, Stocker Road, Exeter EX4 4PY, UK.

The guppy () is a model species in ecology and evolution. Many studies have examined effects of predators on guppy behaviour, reproduction, survival strategies, feeding and other life-history traits, but few have studied variation in their parasite diversity. We surveyed parasites of 18 Trinidadian populations of guppy, to provide insight on the geographical mosaic of parasite variability, which may act as a source of natural selection acting on guppies. We found 21 parasite species, including five new records for Trinidad. Spatial variation in parasite diversity was significantly higher than that of piscine predators, and significant variation in parasite richness among individuals and populations was correlated with: (i) host size, (ii) snail species richness, and (iii) the distance between populations. Differences in parasite species richness are likely to play an important, yet underestimated role in the biology of this model species of vertebrate ecology and evolution.
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http://dx.doi.org/10.1098/rsos.191112DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7029902PMC
January 2020

Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish.

Ecol Evol 2020 Jan 11;10(2):638-653. Epub 2020 Jan 11.

Fisheries and Oceans Canada Northwest Atlantic Fisheries Centre St. John's NL Canada.

Genomic architecture and standing variation can play a key role in ecological adaptation and contribute to the predictability of evolution. In Atlantic cod (), four large chromosomal rearrangements have been associated with ecological gradients and migratory behavior in regional analyses. However, the degree of parallelism, the extent of independent inheritance, and functional distinctiveness of these rearrangements remain poorly understood. Here, we use a 12K single nucleotide polymorphism (SNP) array to demonstrate extensive individual variation in rearrangement genotype within populations across the species range, suggesting that local adaptation to fine-scale ecological variation is enabled by rearrangements with independent inheritance. Our results demonstrate significant association of rearrangements with migration phenotype and environmental gradients across the species range. Individual rearrangements exhibit functional modularity, but also contain loci showing multiple environmental associations. Clustering in genetic distance trees and reduced differentiation within rearrangements across the species range are consistent with shared variation as a source of contemporary adaptive diversity in Atlantic cod. Conversely, we also find that haplotypes in the LG12 and LG1 rearranged region have diverged across the Atlantic, despite consistent environmental associations. Exchange of these structurally variable genomic regions, as well as local selective pressures, has likely facilitated individual diversity within Atlantic cod stocks. Our results highlight the importance of genomic architecture and standing variation in enabling fine-scale adaptation in marine species.
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http://dx.doi.org/10.1002/ece3.5828DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6988541PMC
January 2020

Evolutionary impacts differ between two exploited populations of northern bottlenose whale ().

Ecol Evol 2019 Dec 19;9(23):13567-13584. Epub 2019 Nov 19.

Biology Department Dalhousie University Halifax NS Canada.

Interpretation of conservation status should be informed by an appreciation of genetic diversity, past demography, and overall trends in population size, which contribute to a species' evolutionary potential and resilience to genetic risks. Low genetic diversity can be symptomatic of rapid demographic declines and impose genetic risks to populations, but can also be maintained by natural processes. The northern bottlenose whale has the lowest known mitochondrial diversity of any cetacean and was intensely whaled in the Northwest Atlantic over the last century, but whether exploitation imposed genetic risks that could limit recovery is unknown. We sequenced full mitogenomes and genotyped 37 novel microsatellites for 128 individuals from known areas of abundance in the Scotian Shelf, Northern and Southern Labrador, Davis Strait, and Iceland, and a newly discovered group off Newfoundland. Despite low diversity and shared haplotypes across all regions, both markers supported the Endangered Scotian Shelf population as distinct from the combined northern regions. The genetic affinity of Newfoundland was uncertain, suggesting an area of mixing with no clear population distinction for the region. Demographic reconstruction using mitogenomes suggests that the northern region underwent population expansion following the last glacial maximum, but for the peripheral Scotian Shelf population, a stable demographic trend was followed by a drastic decline over a temporal scale consistent with increasing human activity in the Northwest Atlantic. Low connectivity between the Scotian Shelf and the rest of the Atlantic likely compounded the impact of intensive whaling for this species, potentially imposing genetic risks affecting recovery of this population. We highlight how the combination of historical environmental conditions and modern exploitation of this species has had very different evolutionary impacts on structured populations of northern bottlenose whales across the western North Atlantic.
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http://dx.doi.org/10.1002/ece3.5813DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6912904PMC
December 2019

Eco-Evolutionary Feedbacks Predict the Time Course of Rapid Life-History Evolution.

Am Nat 2019 11 9;194(5):671-692. Epub 2019 Sep 9.

Organisms can change their environment and in doing so change the selection they experience and how they evolve. Population density is one potential mediator of such interactions because high population densities can impact the ecosystem and reduce resource availability. At present, such interactions are best known from theory and laboratory experiments. Here we quantify the importance of such interactions in nature by transplanting guppies from a stream where they co-occur with predators into tributaries that previously lacked both guppies and predators. If guppies evolve solely because of the immediate reduction in mortality rate, the strength of selection and rate of evolution should be greatest at the outset and then decline as the population adapts to its new environment. If indirect effects caused by the increase in guppy population density in the absence of predation prevail, then there should be a lag in guppy evolution because time is required for them to modify their environment. The duration of this lag is predicted to be associated with the environmental modification caused by guppies. We observed a lag in life-history evolution associated with increases in population density and altered ecology. How guppies evolved matched predictions derived from evolutionary theory that incorporates such density effects.
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http://dx.doi.org/10.1086/705380DOI Listing
November 2019

Genomic signatures and correlates of widespread population declines in salmon.

Nat Commun 2019 07 5;10(1):2996. Epub 2019 Jul 5.

Fisheries and Oceans Canada, Northwest Atlantic Fisheries Centre, 80 E White Hills Rd, St. John's, Newfoundland, A1C 5X1, Canada.

Global losses of biodiversity are occurring at an unprecedented rate, but causes are often unidentified. Genomic data provide an opportunity to isolate drivers of change and even predict future vulnerabilities. Atlantic salmon (Salmo salar) populations have declined range-wide, but factors responsible are poorly understood. Here, we reconstruct changes in effective population size (N) in recent decades for 172 range-wide populations using a linkage-based method. Across the North Atlantic, N has significantly declined in >60% of populations and declines are consistently temperature-associated. We identify significant polygenic associations with decline, involving genomic regions related to metabolic, developmental, and physiological processes. These regions exhibit changes in presumably adaptive diversity in declining populations consistent with contemporary shifts in body size and phenology. Genomic signatures of widespread population decline and associated risk scores allow direct and potentially predictive links between population fitness and genotype, highlighting the power of genomic resources to assess population vulnerability.
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http://dx.doi.org/10.1038/s41467-019-10972-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6611788PMC
July 2019

A migration-associated supergene reveals loss of biocomplexity in Atlantic cod.

Sci Adv 2019 06 26;5(6):eaav2461. Epub 2019 Jun 26.

Fisheries and Oceans Canada, Northwest Atlantic Fisheries Centre, St. John's, Newfoundland, Canada.

Chromosome structural variation may underpin ecologically important intraspecific diversity by reducing recombination within supergenes containing linked, coadapted alleles. Here, we confirm that an ancient chromosomal rearrangement is strongly associated with migratory phenotype and individual genetic structure in Atlantic cod () across the Northwest Atlantic. We reconstruct trends in effective population size over the last century and reveal declines in effective population size matching onset of industrialized harvest (after 1950). We find different demographic trajectories between individuals homozygous for the chromosomal rearrangement relative to heterozygous or homozygous individuals for the noninverted haplotype, suggesting different selective histories across the past 150 years. These results illustrate how chromosomal structural diversity can mediate fine-scale genetic, phenotypic, and demographic variation in a highly connected marine species and show how overfishing may have led to loss of biocomplexity within Northern cod stock.
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http://dx.doi.org/10.1126/sciadv.aav2461DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6594766PMC
June 2019

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

Ecol Evol 2019 Apr 29;9(8):4504-4517. Epub 2019 Mar 29.

Department of Biology Dalhousie University Halifax Nova Scotia Canada.

In dendritic river systems, gene flow is expected to occur primarily within watersheds. Yet, rare cross-watershed transfers can also occur, whether mediated by (often historical) geological events or (often contemporary) human activities. We explored these events and their potential evolutionary consequences by analyzing patterns of neutral genetic variation (microsatellites) and adaptive phenotypic variation (male color) in wild guppies () distributed across two watersheds in northern Trinidad. We found the expected signatures of within-watershed gene flow; yet we also inferred at least two instances of cross-watershed gene flow-one in the upstream reaches and one further downstream. The upstream cross-watershed event appears to be very recent (41 ± 13 years), suggesting dispersal via recent flooding or undocumented human-mediated transport. The downstream cross-watershed event appears to be considerably older (577 ± 265 years), suggesting a role for rare geological or climatological events. Alongside these strong signatures of both contemporary and historical gene flow, we found little evidence of impacts on presumably adaptive phenotypic differentiation, except perhaps in the one instance of very recent cross-watershed gene flow. Selection in this system seems to overpower gene flow-at least on the spatiotemporal scales investigated here.
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http://dx.doi.org/10.1002/ece3.5033DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6476793PMC
April 2019

Estimating the relative fitness of escaped farmed salmon offspring in the wild and modelling the consequences of invasion for wild populations.

Evol Appl 2019 Apr 28;12(4):705-717. Epub 2019 Jan 28.

Science Branch, Fisheries and Oceans Canada St. John's Newfoundland and Labrador Canada.

Throughout their native range, wild Atlantic salmon populations are threatened by hybridization and introgression with escapees from net-pen salmon aquaculture. Although domestic-wild hybrid offspring have shown reduced fitness in laboratory and field experiments, consequential impacts on population abundance and genetic integrity remain difficult to predict in the field, in part because the strength of selection against domestic offspring is often unknown and context-dependent. Here, we follow a single large escape event of farmed Atlantic salmon in southern Newfoundland and monitor changes in the in-river proportions of hybrids and feral individuals over time using genetically based hybrid identification. Over a three-year period following the escape, the overall proportion of wild parr increased consistently (total wild proportion of 71.6%, 75.1% and 87.5% each year, respectively), with subsequent declines in feral (genetically pure farmed individuals originating from escaped, farmed adults) and hybrid parr. We quantify the strength of selection against parr of aquaculture ancestry and explore the genetic and demographic consequences for populations in the region. Within-cohort changes in the relative proportions of feral and F1 parr suggest reduced relative survival compared to wild individuals over the first (0.15 and 0.81 for feral and F1, respectively) and second years of life (0.26, 0.83). These relative survivorship estimates were used to inform an individual-based salmon eco-genetic model to project changes in adult abundance and overall allele frequency across three invasion scenarios ranging from short-term to long-term invasion and three relative survival scenarios. Modelling results indicate that total population abundance and time to recovery were greatly affected by relative survivorship and predict significant declines in wild population abundance under continued large escape events and calculated survivorship. Overall, this work demonstrates the importance of estimating the strength of selection against domestic offspring in the wild to predict the long-term impact of farmed salmon escape events on wild populations.
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http://dx.doi.org/10.1111/eva.12746DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6439497PMC
April 2019

Chromosome polymorphisms track trans-Atlantic divergence and secondary contact in Atlantic salmon.

Mol Ecol 2019 04 29;28(8):2074-2087. Epub 2019 Apr 29.

Fisheries and Oceans Canada, Northwest Atlantic Fisheries Centre, St. John's, Newfoundland, Canada.

Pleistocene glaciations drove repeated range contractions and expansions shaping contemporary intraspecific diversity. Atlantic salmon (Salmo salar) in the western and eastern Atlantic diverged >600,000 years before present, with the two lineages isolated in different southern refugia during glacial maxima, driving trans-Atlantic genomic and karyotypic divergence. Here, we investigate the genomic consequences of glacial isolation and trans-Atlantic secondary contact using 108,870 single nucleotide polymorphisms genotyped in 80 North American and European populations. Throughout North America, we identified extensive interindividual variation and discrete linkage blocks within and between chromosomes with known trans-Atlantic differences in rearrangements: Ssa01/Ssa23 translocation and Ssa08/Ssa29 fusion. Spatial genetic analyses suggest independence of rearrangements, with Ssa01/Ssa23 showing high European introgression (>50%) in northern populations indicative of post-glacial trans-Atlantic secondary contact, contrasting with low European ancestry genome-wide (3%). Ssa08/Ssa29 showed greater intrapopulation diversity, suggesting a derived chromosome fusion polymorphism that evolved within North America. Evidence of potential selection on both genomic regions suggests that the adaptive role of rearrangements warrants further investigation in Atlantic salmon. Our study highlights how Pleistocene glaciations can influence large-scale intraspecific variation in genomic architecture of northern species.
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http://dx.doi.org/10.1111/mec.15065DOI Listing
April 2019

Spatio-temporal dynamics of density-dependent dispersal during a population colonisation.

Ecol Lett 2019 Apr 4;22(4):634-644. Epub 2019 Feb 4.

University of Jyväskylä, Centre of Excellence in Biological Interactions, Department of Biological and Environmental Science, Jyväskylä, Finland.

Predicting population colonisations requires understanding how spatio-temporal changes in density affect dispersal. Density can inform on fitness prospects, acting as a cue for either habitat quality, or competition over resources. However, when escaping competition, high local density should only increase emigration if lower-density patches are available elsewhere. Few empirical studies on dispersal have considered the effects of density at the local and landscape scale simultaneously. To explore this, we analyze 5 years of individual-based data from an experimental introduction of wild guppies Poecilia reticulata. Natal dispersal showed a decrease in local density dependence as density at the landscape level increased. Landscape density did not affect dispersal among adults, but local density-dependent dispersal switched from negative (conspecific attraction) to positive (conspecific avoidance), as the colonisation progressed. This study demonstrates that densities at various scales interact to determine dispersal, and suggests that dispersal trade-offs differ across life stages.
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http://dx.doi.org/10.1111/ele.13205DOI Listing
April 2019

Range-wide genomic data synthesis reveals transatlantic vicariance and secondary contact in Atlantic cod.

Ecol Evol 2018 Dec 16;8(23):12140-12152. Epub 2018 Nov 16.

School of Biological Sciences Bangor University Bangor UK.

Recent advances in genetic and genomic analysis have greatly improved our understanding of spatial population structure in marine species. However, studies addressing phylogeographic patterns at oceanic spatial scales remain rare. In Atlantic cod (), existing range-wide examinations suggest significant transatlantic divergence, although the fine-scale contemporary distribution of populations and potential for secondary contact are largely unresolved. Here, we explore transatlantic phylogeography in Atlantic cod using a data-synthesis approach, integrating multiple genome-wide single-nucleotide polymorphism (SNP) datasets representative of different regions to create a single range-wide dataset containing 1,494 individuals from 54 locations and genotyped at 796 common loci. Our analysis highlights significant transatlantic divergence and supports the hypothesis of westward post-glacial colonization of Greenland from the East Atlantic. Accordingly, our analysis suggests the presence of transatlantic secondary contact off eastern North America and supports existing perspectives on the phylogeographic history of Atlantic cod with an unprecedented combination of genetic and geographic resolution. Moreover, we demonstrate the utility of integrating distinct SNP databases of high comparability.
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http://dx.doi.org/10.1002/ece3.4672DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6303715PMC
December 2018

RADProc: A computationally efficient de novo locus assembler for population studies using RADseq data.

Mol Ecol Resour 2019 Jan 21;19(1):272-282. Epub 2018 Dec 21.

Faculty of Computer Science, Dalhousie University, Halifax, Nova Scotia, Canada.

Restriction site-associated DNA sequencing (RADseq) is a powerful tool for genotyping of individuals, but the identification of loci and assignment of sequence reads is a crucial and often challenging step. The optimal parameter settings for a given de novo RADseq assembly vary between data sets and can be difficult and computationally expensive to determine. Here, we introduce RADProc, a software package that uses a graph data structure to represent all sequence reads and their similarity relationships. Storing sequence-comparison results in a graph eliminates unnecessary and redundant sequence similarity calculations. De novo locus formation for a given parameter set can be performed on the precomputed graph, making parameter sweeps far more efficient. RADProc also uses a clustering approach for faster nucleotide-distance calculation. The performance of RADProc compares favourably with that of the widely used Stacks software. The run-time comparisons between RADProc and Stacks for 32 different parameter settings using 20 green-crab (Carcinus maenas) samples showed that RADProc took as little as 2 hr 40 min compared to 78 hr by Stacks, while 16 brown trout (Salmo trutta L.) samples were processed by RADProc and Stacks in 23 and 263 hr, respectively. Comparisons of the de novo loci formed, and catalog built using both the methods demonstrate that the improvement in processing speeds achieved by RADProc does not affect much the actual loci formed and the results of downstream analyses based on those loci.
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http://dx.doi.org/10.1111/1755-0998.12954DOI Listing
January 2019

Environmental extremes drive population structure at the northern range limit of Atlantic salmon in North America.

Mol Ecol 2018 10 17;27(20):4026-4040. Epub 2018 Sep 17.

Science Branch, Department of Fisheries and Oceans Canada, St. John's, NL, Canada.

Conservation of exploited species requires an understanding of both genetic diversity and the dominant structuring forces, particularly near range limits, where climatic variation can drive rapid expansions or contractions of geographic range. Here, we examine population structure and landscape associations in Atlantic salmon (Salmo salar) across a heterogeneous landscape near the northern range limit in Labrador, Canada. Analysis of two amplicon-based data sets containing 101 microsatellites and 376 single nucleotide polymorphisms (SNPs) from 35 locations revealed clear differentiation between populations spawning in rivers flowing into a large marine embayment (Lake Melville) compared to coastal populations. The mechanisms influencing the differentiation of embayment populations were investigated using both multivariate and machine-learning landscape genetic approaches. We identified temperature as the strongest correlate with genetic structure, particularly warm temperature extremes and wider annual temperature ranges. The genomic basis of this divergence was further explored using a subset of locations (n = 17) and a 220K SNP array. SNPs associated with spatial structuring and temperature mapped to a diverse set of genes and molecular pathways, including regulation of gene expression, immune response, and cell development and differentiation. The results spanning molecular marker types and both novel and established methods clearly show climate-associated, fine-scale population structure across an environmental gradient in Atlantic salmon near its range limit in North America, highlighting valuable approaches for predicting population responses to climate change and managing species sustainability.
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http://dx.doi.org/10.1111/mec.14849DOI Listing
October 2018

PMERGE: Computational filtering of paralogous sequences from RAD-seq data.

Ecol Evol 2018 Jul 11;8(14):7002-7013. Epub 2018 Jun 11.

Faculty of Computer Science Dalhousie University Halifax NS Canada.

Restriction-site associated DNA sequencing (RAD-seq) can identify and score thousands of genetic markers from a group of samples for population-genetics studies. One challenge of de novo RAD-seq analysis is to distinguish paralogous sequence variants (PSVs) from true single-nucleotide polymorphisms (SNPs) associated with orthologous loci. In the absence of a reference genome, it is difficult to differentiate true SNPs from PSVs, and their impact on downstream analysis remains unclear. Here, we introduce a network-based approach, PMERGE that connects fragments based on their DNA sequence similarity to identify probable PSVs. Applying our method to de novo RAD-seq data from 150 Atlantic salmon () samples collected from 15 locations across the Southern Newfoundland coast allowed the identification of 87% of total PSVs identified through alignment to the Atlantic salmon genome. Removal of these paralogs altered the inferred population structure, highlighting the potential impact of filtering in RAD-seq analysis. PMERGE is also applied to a green crab () data set consisting of 242 samples from 11 different locations and was successfully able to identify and remove the majority of paralogous loci (62%). The PMERGE software can be run as part of the widely used Stacks analysis package.
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http://dx.doi.org/10.1002/ece3.4219DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6065343PMC
July 2018

Genotyping-by-sequencing of genome-wide microsatellite loci reveals fine-scale harvest composition in a coastal Atlantic salmon fishery.

Evol Appl 2018 Jul 11;11(6):918-930. Epub 2018 Mar 11.

Department of Biology Dalhousie University Halifax NS Canada.

Individual assignment and genetic mixture analysis are commonly utilized in contemporary wildlife and fisheries management. Although microsatellite loci provide unparalleled numbers of alleles per locus, their use in assignment applications is increasingly limited. However, next-generation sequencing, in conjunction with novel bioinformatic tools, allows large numbers of microsatellite loci to be simultaneously genotyped, presenting new opportunities for individual assignment and genetic mixture analysis. Here, we scanned the published Atlantic salmon genome to identify 706 microsatellite loci, from which we developed a final panel of 101 microsatellites distributed across the genome (average 3.4 loci per chromosome). Using samples from 35 Atlantic salmon populations ( = 1,485 individuals) from coastal Labrador, Canada, a region characterized by low levels of differentiation in this species, this panel identified 844 alleles (average of 8.4 alleles per locus). Simulation-based evaluations of assignment and mixture identification accuracy revealed unprecedented resolution, clearly identifying 26 rivers or groups of rivers spanning 500 km of coastline. This baseline was used to examine the stock composition of 696 individuals harvested in the Labrador Atlantic salmon fishery and revealed that coastal fisheries largely targeted regional groups (<300 km). This work suggests that the development and application of large sequenced microsatellite panels presents great potential for stock resolution in Atlantic salmon and more broadly in other exploited anadromous and marine species.
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http://dx.doi.org/10.1111/eva.12606DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5999200PMC
July 2018

Population connectivity and larval dispersal of the exploited mangrove crab along the Brazilian coast.

PeerJ 2018 30;6:e4702. Epub 2018 Apr 30.

Molecular Biology Laboratory, Embrapa Caprinos e Ovinos, Sobral, Ceará, Brazil.

Background: The mangrove crab is considered a key species for the ecological balance of mangrove forests and a major source of employment and income for traditional crab collectors in Brazil. Several studies evidenced weak genetic variation among populations due to an efficient larval transport. However, gene flow patterns of the species is poorly understood, with no information about migration rates. The influence of the two main Brazilian currents in larval dispersion is also not clear. In order to provide baseline information for conservation, planning and management of this important fishery resource, the present study aimed to estimate and evaluate spatial distribution of genetic diversity, migration rates and gene flow directivity among populations of in Brazil.

Methods: Nine microsatellites were used to resolve population structure of 319 crabs collected from six sites located along the Brazilian coast. The degree of geographical differentiation included estimates of genetic diversity, population structure and gene flow models, with spatial analysis of shared alleles (SAShA), isolation by distance tests, AMOVA, discriminant analysis of principal components (DAPC) and Bayesian clustering. We estimated the amount of ongoing gene flow between clusters using the coalescent-based method implemented in Migrate-N.

Results: Loci were highly polymorphic (average of 12.4 alleles per locus) evidencing high genetic variability. There was significant differentiation among localities, despite of the low value of (= 0.019; 0.001). and Jost's indexes were also estimated in pairwise comparisons and showed significant differences between most of the surveyed site pairs ( 0.05). Structure evidenced a single genetic group among samples, however SAShA pointed to a non-panmictic condition ( 0.011). AMOVA detected four statistical significant clusters with low level of differentiation ( = 0.037; 0.023). The gene flow model that best described the population connectivity was the island model, with ∼24 crabs being exchanged among localities per generation.

Discussion: The high migration rates found among localities seem to be the main force acting to sustain the distribution of the genetic diversity of . Despite the high gene flow and the weak population structure among samples, the significant genetic differences found suggest that gene flow alone does not bypass the effects of genetic drift, natural selection and/or human exploitation. These findings are vital for the establishment of a database to be used in the development of conservation programs.
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http://dx.doi.org/10.7717/peerj.4702DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5933341PMC
April 2018

Isolation and characterization of microsatellite markers in the spiny lobster, Panulirus echinatus Smith, 1869 (Decapoda: Palinuridae) by Illumina MiSeq sequencing.

J Genet 2018 Apr 11;97(1):e25-e30. Epub 2018 Apr 11.

Universidade Federal do Piauí, Campus Universitário Ministro Petrônio Portella, Ininga, Teresina, PI, 64049-550, Brazil.

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April 2018

A climate-associated multispecies cryptic cline in the northwest Atlantic.

Sci Adv 2018 03 28;4(3):eaaq0929. Epub 2018 Mar 28.

Department of Computer Science, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada.

The spatial genetic structure of most species in the open marine environment remains largely unresolved. This information gap creates uncertainty in the sustainable management, recovery, and associated resilience of marine communities and our capacity to extrapolate beyond the few species for which such information exists. We document a previously unidentified multispecies biogeographic break aligned with a steep climatic gradient and driven by seasonal temperature minima in the northwest Atlantic. The coherence of this genetic break across our five study species with contrasting life histories suggests a pervasive macroecological phenomenon. The integration of this genetic structure with habitat suitability models and climate forecasts predicts significant variation in northward distributional shifts among populations and availability of suitable habitat in future oceans. The results of our integrated approach provide new perspective on how cryptic intraspecific diversity associated with climatic variation influences species and community response to climate change beyond simple poleward shifts.
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http://dx.doi.org/10.1126/sciadv.aaq0929DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5873842PMC
March 2018

Applications of random forest feature selection for fine-scale genetic population assignment.

Evol Appl 2018 02 14;11(2):153-165. Epub 2017 Sep 14.

Faculty of Computer Science Dalhousie University Halifax NS Canada.

Genetic population assignment used to inform wildlife management and conservation efforts requires panels of highly informative genetic markers and sensitive assignment tests. We explored the utility of machine-learning algorithms (random forest, regularized random forest and guided regularized random forest) compared with ranking for selection of single nucleotide polymorphisms (SNP) for fine-scale population assignment. We applied these methods to an unpublished SNP data set for Atlantic salmon () and a published SNP data set for Alaskan Chinook salmon (). In each species, we identified the minimum panel size required to obtain a self-assignment accuracy of at least 90% using each method to create panels of 50-700 markers Panels of SNPs identified using random forest-based methods performed up to 7.8 and 11.2 percentage points better than -selected panels of similar size for the Atlantic salmon and Chinook salmon data, respectively. Self-assignment accuracy ≥90% was obtained with panels of 670 and 384 SNPs for each data set, respectively, a level of accuracy never reached for these species using -selected panels. Our results demonstrate a role for machine-learning approaches in marker selection across large genomic data sets to improve assignment for management and conservation of exploited populations.
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http://dx.doi.org/10.1111/eva.12524DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5775496PMC
February 2018

Range-wide parallel climate-associated genomic clines in Atlantic salmon.

R Soc Open Sci 2017 Nov 15;4(11):171394. Epub 2017 Nov 15.

Fisheries and Oceans Canada, Northwest Atlantic Fisheries Centre, St John's, Newfoundland and Labrador, CanadaA1C 5X1.

Clinal variation across replicated environmental gradients can reveal evidence of local adaptation, providing insight into the demographic and evolutionary processes that shape intraspecific diversity. Using 1773 genome-wide single nucleotide polymorphisms we evaluated latitudinal variation in allele frequency for 134 populations of North American and European Atlantic salmon (). We detected 84 (4.74%) and 195 (11%) loci showing clinal patterns in North America and Europe, respectively, with 12 clinal loci in common between continents. Clinal single nucleotide polymorphisms were evenly distributed across the salmon genome and logistic regression revealed significant associations with latitude and seasonal temperatures, particularly average spring temperature in both continents. Loci displaying parallel clines were associated with several metabolic and immune functions, suggesting a potential basis for climate-associated adaptive differentiation. These climate-based clines collectively suggest evidence of large-scale environmental associated differences on either side of the North Atlantic. Our results support patterns of parallel evolution on both sides of the North Atlantic, with evidence of both similar and divergent underlying genetic architecture. The identification of climate-associated genomic clines illuminates the role of selection and demographic processes on intraspecific diversity in this species and provides a context in which to evaluate the impacts of climate change.
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http://dx.doi.org/10.1098/rsos.171394DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5717698PMC
November 2017

Ancient chromosomal rearrangement associated with local adaptation of a postglacially colonized population of Atlantic Cod in the northwest Atlantic.

Mol Ecol 2018 01 27;27(2):339-351. Epub 2017 Dec 27.

Biology Department, Dalhousie University, Halifax, NS, Canada.

Intraspecific diversity is central to the management and conservation of exploited species, yet knowledge of how this diversity is distributed and maintained in the genome of many marine species is lacking. Recent advances in genomic analyses allow for genome-wide surveys of intraspecific diversity and offer new opportunities for exploring genomic patterns of divergence. Here, we analysed genome-wide polymorphisms to measure genetic differentiation between an offshore migratory and a nonmigratory population and to define conservation units of Atlantic Cod (Gadus morhua) in coastal Labrador. A total of 141 individuals, collected from offshore sites and from a coastal site within Gilbert Bay, Labrador, were genotyped using an ~11k single nucleotide polymorphism array. Analyses of population structure revealed strong genetic differentiation between migratory offshore cod and nonmigratory Gilbert Bay cod. Genetic differentiation was elevated for loci within a chromosomal rearrangement found on linkage group 1 (LG1) that coincides with a previously found double inversion associated with migratory and nonmigratory ecotype divergence of cod in the northeast Atlantic. This inverted region includes several genes potentially associated with adaptation to differences in salinity and temperature, as well as influencing migratory behaviour. Our work provides evidence that a chromosomal rearrangement on LG1 is associated with parallel patterns of divergence between migratory and nonmigratory ecotypes on both sides of the Atlantic Ocean.
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http://dx.doi.org/10.1111/mec.14442DOI Listing
January 2018

Evolutionary genetics of immunological supertypes reveals two faces of the Red Queen.

Nat Commun 2017 11 3;8(1):1294. Epub 2017 Nov 3.

School of Environmental Sciences, University of East Anglia, Norwich, Norfolk, NR4 7TJ, UK.

Red Queen host-parasite co-evolution can drive adaptations of immune genes by positive selection that erodes genetic variation (Red Queen arms race) or results in a balanced polymorphism (Red Queen dynamics) and long-term preservation of genetic variation (trans-species polymorphism). These two Red Queen processes are opposite extremes of the co-evolutionary spectrum. Here we show that both Red Queen processes can operate simultaneously by analysing the major histocompatibility complex (MHC) in guppies (Poecilia reticulata and P. obscura) and swamp guppies (Micropoecilia picta). Sub-functionalisation of MHC alleles into 'supertypes' explains how polymorphisms persist during rapid host-parasite co-evolution. Simulations show the maintenance of supertypes as balanced polymorphisms, consistent with Red Queen dynamics, whereas alleles within supertypes are subject to positive selection in a Red Queen arms race. Building on the divergent allele advantage hypothesis, we show that functional aspects of allelic diversity help to elucidate the evolution of polymorphic genes involved in Red Queen co-evolution.
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http://dx.doi.org/10.1038/s41467-017-01183-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5670221PMC
November 2017

Barcoding Atlantic Canada's mesopelagic and upper bathypelagic marine fishes.

PLoS One 2017 20;12(9):e0185173. Epub 2017 Sep 20.

Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada.

DNA barcode sequences were developed from 557 mesopelagic and upper bathypelagic teleost specimens collected in waters off Atlantic Canada. Confident morphological identifications were available for 366 specimens, of 118 species and 93 genera, which yielded 328 haplotypes. Five of the species were novel to the Barcode of Life Database (BOLD). Most of the 118 species conformed to expectations of monophyly and the presence of a "barcode gap", though some known weaknesses in existing taxonomy were confirmed and a deficiency in published keys was revealed. Of the specimens for which no firm morphological identification was available, 156 were successfully identified to species, and a further 11 to genus, using their barcode sequences and a combination of distance- and character-based methods. The remaining 24 specimens were from species for which no reference barcode is yet available or else ones confused by apparent misidentification of publicly available sequences in BOLD. Addition of the new sequences to those previously in BOLD contributed support to recent taxonomic revisions of Chiasmodon and Poromitra, while it also revealed 18 cases of potential cryptic speciation. Most of the latter appear to result from genetic divergence among populations in different ocean basins, while the general lack of strong horizontal environmental gradients within the deep sea has allowed morphology to be conserved. Other examples of divergence appear to distinguish individuals living under the sub-tropical gyre of the North Atlantic from those under that ocean's sub-polar gyre. In contrast, the available sequences for two myctophid species, Benthosema glaciale and Notoscopelus elongatus, showed genetic structuring on finer geographic scales. The observed structure was not consistent with recent suggestions that "resident" populations of myctophids can maintain allopatry despite the mixing of ocean waters. Rather, it indicates that the very rapid speciation characteristic of the Myctophidae is both on-going and detectable using barcodes.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0185173PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5607201PMC
October 2017