Paul Bentzen | Dalhousie University (original) (raw)

Papers by Paul Bentzen

Research paper thumbnail of Kinship Analysis of Pacific Salmon: Insights Into Mating, Homing, and Timing of Reproduction

Journal of Heredity, 2001

Multilocus microsatellite genotypes were used to infer kinship and relatedness in two species of ... more Multilocus microsatellite genotypes were used to infer kinship and relatedness in two species of Pacific salmon from three populations in Washington State. Even in the absence of direct genetic data from parents, clustering of individuals according to allele sharing and reconstruction of parental genotypes allowed resolution of full-and half-sib relationships among 135 chinook salmon (Oncorhynchus tshawytscha) sampled as preemergent juveniles from 14 redds in the Dungeness River. Inferred reproductive behaviors included single-pair matings, polyandry in which females mated with two to three males at a single redd, polygyny in which males mated with two females at different redds, use of two redds by a single female, and use of one redd site by two females. Greater average relatedness (r xy) in the upper reach of the Dungeness River implied within-reach homing of returning adults. In steelhead trout (O. mykiss), the frequency of related pairs (dyads) of mature individuals that migrated up Snow Creek less than a week apart was greater than expected for randomly chosen dyads, as was the frequency of steelhead dyads that were spawned on the same day in the Forks Creek hatchery. These results imply a heritable basis for upstream migration date and maturation date in steelhead trout.

Research paper thumbnail of Multiple decades of stocking has resulted in limited hatchery introgression in wild brook trout (<i>Salvelinus fontinalis</i>) populations of Nova Scotia

Evolutionary Applications, Feb 20, 2020

This is an open access article under the terms of the Creative Commons Attribution License, which... more This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Research paper thumbnail of Polymorphic tetranucleotide microsatellite markers in the Caribbean spiny lobster, Panulirus argus

Molecular Ecology Notes, Sep 1, 2004

Ten tetranucleotide microsatellite loci are described for the Caribbean spiny lobster Panulirus a... more Ten tetranucleotide microsatellite loci are described for the Caribbean spiny lobster Panulirus argus. Loci were polymorphic (4–15 alleles per locus) and exhibited high levels of expected (0.553–0.921) and observed heterozygosity (0.469–0.906) from samples caught off Belize and Puerto Rico coasts. No significant departure from Hardy–Weinberg equilibrium conditions were observed for any locus. All microsatellite loci should be useful for assessing population discrimination for this valuable marine animal currently subjected to excessive fishing efforts.

Research paper thumbnail of Loss of genetic diversity and reduction of genetic distance among lake trout Salvelinus namaycush ecomorphs, Lake Superior 1959 to 2013

Journal of Great Lakes Research, Apr 1, 2016

North America's northern lakes are undergoing major changes. Lake Superior is the coldest and nor... more North America's northern lakes are undergoing major changes. Lake Superior is the coldest and northernmost of the Laurentian Great Lakes. Here, we present an extension of a long-term data set that monitors genetic and phenotypic diversity of lake trout Salvelinus namaycush in Lake Superior. Hypotheses were investigated pertaining to loss of genetic diversity and genetic homogenization among three lake trout ecomorphs in Lake Superior during their recovery several decades after a major fishery collapse in the early 1960s. Comparison of a contemporary (2004-2013) microsatellite DNA data set to a previously published, post-collapse recovery period data set (1995-1999) indicated substantive losses in genetic diversity. Allelic richness decreased by 5.7%, 12.3%, and 6.8% at Isle Royale, Stannard Rock, and Klondike Reef, respectively. A 60.7% reduction in genetic distance among ecomorphs since the 1990s was detected. Comparisons with a third data set of samples collected during the fishery collapse (1959) indicated an overall 18.2% loss in allelic richness at Isle Royale. The amount of introgression among ecomorphs has likely increased over time. Apparent losses in genetic diversity could be a consequence of historical fishery harvests (early 1900s) exacerbated by intensive stocking (1950s-1980s) and invasions of non-native species (1960s-1990s). Overlap in foraging and breeding areas may have contributed to increasing levels of hybridization among ecomorphs. Knowledge of these processes will help to identify impediments and strategies for the maintenance of lake trout biodiversity in northern Great Lakes, and their re-establishment in the Laurentian Great Lakes.

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

Evolutionary Applications, Mar 11, 2018

This is an open access article under the terms of the Creative Commons Attribution License, which... more This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Research paper thumbnail of Ultra-deep Illumina sequencing accurately identifies MHC class IIb alleles and provides evidence for copy number variation in the guppy (<i>Poecilia reticulata</i>)

Molecular Ecology Resources, Feb 5, 2014

We address the bioinformatic issue of accurately separating amplified genes of the major histocom... more We address the bioinformatic issue of accurately separating amplified genes of the major histocompatibility complex (MHC) from artefacts generated during high‐throughput sequencing workflows. We fit observed ultra‐deep sequencing depths (hundreds to thousands of sequences per amplicon) of allelic variants to expectations from genetic models of copy number variation (CNV). We provide a simple, accurate and repeatable method for genotyping multigene families, evaluating our method via analyses of 209 b of MHC class IIb exon 2 in guppies (Poecilia reticulata). Genotype repeatability for resequenced individuals (N = 49) was high (100%) within the same sequencing run. However, repeatability dropped to 83.7% between independent runs, either because of lower mean amplicon sequencing depth in the initial run or random PCR effects. This highlights the importance of fully independent replicates. Significant improvements in genotyping accuracy were made by greatly reducing type I genotyping error (i.e. accepting an artefact as a true allele), which may occur when using low‐depth allele validation thresholds used by previous methods. Only a small amount (4.9%) of type II error (i.e. rejecting a genuine allele as an artefact) was detected through fully independent sequencing runs. We observed 1–6 alleles per individual, and evidence of sharing of alleles across loci. Variation in the total number of MHC class II loci among individuals, both among and within populations was also observed, and some genotypes appeared to be partially hemizygous; total allelic dosage added up to an odd number of allelic copies. Collectively, observations provide evidence of MHC CNV and its complex basis in natural populations.

Research paper thumbnail of Author Correction: Genomic evidence of past and future climate-linked loss in a migratory Arctic fish

Nature Climate Change, 2021

In the version of this Article originally published, ref. 84 was an article that has since been r... more In the version of this Article originally published, ref. 84 was an article that has since been retracted; it has now been replaced with "Salvelinus. NCBI https://www.ncbi.nlm.nih.gov/genome/86400 (2021). " This change does not alter the results or findings of the study. The online versions of the Article have been corrected.

Research paper thumbnail of Loma morhua infections in Atlantic cod (Gadus morhua) reveal relative parasite resistance and differential effects on host growth among family lines

Aquaculture, 2020

infections in Atlantic cod (Gadus morhua) reveal relative parasite resistance and differential ef... more infections in Atlantic cod (Gadus morhua) reveal relative parasite resistance and differential effects on host growth among family lines, aquaculture (2020),

Research paper thumbnail of Parasite diversity and ecology in a model species, the guppy ( Poecilia reticulata ) in Trinidad

Royal Society Open Science, 2020

The guppy ( Poecilia reticulata ) is a model species in ecology and evolution. Many studies have ... more The guppy ( Poecilia reticulata ) 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 an...

Research paper thumbnail of Microsatellite markers developed in the stingless bee Melipona fasciculata by next-generation sequencing and an exploratory analysis of geographic genetic variation

Background. Native meliponines are currently threatened by increased human impacts. The assessmen... more Background. Native meliponines are currently threatened by increased human impacts. The assessment of their genetic variation by microsatellite DNA markers can assist in the conservation of populations and help in the planning and establishment of efficient management strategies. Next generation sequencing has proven to be useful for identifying microsatellite loci from the large amounts of sequence data generated. Methods. The purpose of this study was to develop the first set of microsatellite markers for Melipona fasciculata, selected from partial genome assembly of Illumina paired-end reads. Contigs were created from the resulting paired-end sequence data and these were analyzed with specialized software to extract those reads that contained microsatellite loci. Primer pairs were designed for each detected locus at their flanking regions. Bee samples were genotyped from two different locations for markers characterization and validation. Results. A total of 17 microsatellite loc...

Research paper thumbnail of Range-wide regional assignment of Atlantic salmon (Salmo salar) using genome wide single-nucleotide polymorphisms

Fisheries Research, 2018

The estimation of stock specific exploitation is imperative to fisheries management and the conse... more The estimation of stock specific exploitation is imperative to fisheries management and the conservation of biodiversity, particularly in instances where fisheries simultaneously exploit mixtures of stocks. Mixed stock harvests are particularly common in species that have extensive marine migrations, such as Atlantic and Pacific salmon. Here we develop a range-wide genetic baseline for Atlantic salmon (Salmo salar) from North American and European rivers to allow regional assignment of individuals targeted in international mixed stock fisheries. A combination of published data and additional genotyping was used to assemble a dataset of 96 SNPs for 285 range-wide Atlantic salmon populations for regional assignment. Clustering of baseline samples identified 20 North American and eight European reporting groups with mean individual assignment accuracy of 90% (range 70-100%). This baseline was applied to disentangle the stock composition of individuals in a subset of individuals from the West Greenland Atlantic salmon fishery. Genetic mixture analysis revealed that both European and North American individuals originated from multiple regions, with 92% of European individuals originating from the United Kingdom and Ireland, and North American individuals originating from three regions; Gulf of St. Lawrence (28%), Gaspé Peninsula (23%), and coastal Labrador (21%). The baseline represents a significant resource for the management of Atlantic salmon fisheries and the quantification of salmon migration patterns at sea.

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

Molecular Ecology, 2018

Conservation of exploited species requires an understanding of both genetic diversity and the dom... more 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 Accepted Article This article is protected by copyright. All rights reserved. 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.

Research paper thumbnail of Discovery of novel NGS-mined microsatellite markers and an exploratory analysis of genetic differentiation between two Western Atlantic populations ofCardisoma guanhumiLatreille, 1825 (Decapoda: Brachyura: Gecarcinidae)

Journal of Crustacean Biology, 2019

Research paper thumbnail of Challenge to the model of lake charr evolution: shallow- and deep-water morphs exist within a small postglacial lake

Biological Journal of the Linnean Society, 2016

All examples of lake charr (Salvelinus namaycush) diversity occur within the largest, deepest lak... more All examples of lake charr (Salvelinus namaycush) diversity occur within the largest, deepest lakes of North America (i.e. > 2000 km 2). We report here Rush Lake (1.3 km 2) as the first example of a small lake with two lake charr morphs (lean and huronicus). Morphology, diet, life history, and genetics were examined to demonstrate the existence of morphs and determine the potential influence of evolutionary processes that led to their formation or maintenance. Results showed that the huronicus morph, caught in deep-water, had a deeper body, smaller head and jaws, higher eye position, greater buoyancy, and deeper peduncle than the shallow-water lean morph. Huronicus grew slower to a smaller adult size, and had an older mean age than the lean morph. Genetic comparisons showed low genetic divergence between morphs, indicating incomplete reproductive isolation. Phenotypic plasticity and differences in habitat use between deep and shallow waters associated with variation in foraging opportunities seems to have been sufficient to maintain the two morphs, demonstrating their important roles in resource polymorphism. Rush Lake expands previous explanations for lake charr intraspecific diversity, from large to small lakes and from reproductive isolation to the presence of gene flow associated with strong ecological drivers. Published 2016. This article has been contributed to by US Government employees and their work is in the public domain in the USA,

Research paper thumbnail of Genomic basis of deep‐water adaptation in Arctic Charr ( <i>Salvelinus alpinus</i> ) morphs

Molecular Ecology, Aug 12, 2021

Research paper thumbnail of A putative structural variant and environmental variation associated with genomic divergence across the Northwest Atlantic in Atlantic Halibut

Ices Journal of Marine Science, Aug 1, 2021

39 40 Characterizing the nature of genetic differentiation among individuals and populations and ... more 39 40 Characterizing the nature of genetic differentiation among individuals and populations and its 41 distribution across the genome is increasingly important to inform both conservation and management 42 of exploited species. Atlantic Halibut (Hippoglossus hippoglossus) is an ecologically and 43 commercially important fish species, yet knowledge of population structure and genomic diversity in 44 this species remains lacking. Here, we use restriction-site associated DNA sequencing and a 45 chromosome-level genome assembly to identify over 86,000 single nucleotide polymorphisms mapped 46 to 24 chromosome-sized scaffolds, genotyped in 734 individuals across the Northwest Atlantic. We 47 describe subtle but significant genome-wide regional structuring between the Gulf of St. Lawrence and 48 adjacent Atlantic continental shelf. However, the majority of genetic divergence is associated with a 49 large putative chromosomal rearrangement (5.74 megabases) displaying high differentiation and 50 linkage disequilibrium, but no evidence of geographic variation. Demographic reconstructions suggest 51 periods of expansion coinciding with glacial retreat, and more recent declines in N e. This work 52 highlights the utility of genomic data to identify multiple sources of genetic structure and genomic 53 diversity in commercially exploited marine species. 54

Research paper thumbnail of Genetic and phenotypic variation along an ecological gradient in lake trout Salvelinus namaycush

BMC Evolutionary Biology, Oct 19, 2016

Background: Adaptive radiation involving a colonizing phenotype that rapidly evolves into at leas... more Background: Adaptive radiation involving a colonizing phenotype that rapidly evolves into at least one other ecological variant, or ecotype, has been observed in a variety of freshwater fishes in post-glacial environments. However, few studies consider how phenotypic traits vary with regard to neutral genetic partitioning along ecological gradients. Here, we present the first detailed investigation of lake trout Salvelinus namaycush that considers variation as a cline rather than discriminatory among ecotypes. Genetic and phenotypic traits organized along common ecological gradients of water depth and geographic distance provide important insights into diversification processes in a lake with high levels of human disturbance from over-fishing. Results: Four putative lake trout ecotypes could not be distinguished using population genetic methods, despite morphological differences. Neutral genetic partitioning in lake trout was stronger along a gradient of water depth, than by locality or ecotype. Contemporary genetic migration patterns were consistent with isolation-by-depth. Historical gene flow patterns indicated colonization from shallow to deep water. Comparison of phenotypic (Pst) and neutral genetic variation (Fst) revealed that morphological traits related to swimming performance (e.g., buoyancy, pelvic fin length) departed more strongly from neutral expectations along a depth gradient than craniofacial feeding traits. Elevated phenotypic variance with increasing water depth in pelvic fin length indicated possible ongoing character release and diversification. Finally, differences in early growth rate and asymptotic fish length across depth strata may be associated with limiting factors attributable to cold deep-water environments. Conclusion: We provide evidence of reductions in gene flow and divergent natural selection associated with water depth in Lake Superior. Such information is relevant for documenting intraspecific biodiversity in the largest freshwater lake in the world for a species that recently lost considerable genetic diversity and is now in recovery. Unknown is whether observed patterns are a result of an early stage of incipient speciation, gene flow-selection equilibrium, or reverse speciation causing formerly divergent ecotypes to collapse into a single gene pool.

Research paper thumbnail of Characterization of tetranucleotide microsatellite markers in guppy (Poecilia reticulata)

Molecular Ecology Notes, Feb 17, 2005

Ten tetranucleotide microsatellite loci are characterized for guppy, Poecilia reticulata , an imp... more Ten tetranucleotide microsatellite loci are characterized for guppy, Poecilia reticulata , an important model species in the study of adaptation and mating systems. Loci were isolated following a microsatellite enrichment procedure using probe-labelled magnetic beads. These microsatellites were designed for use in examining gene flow, reproductive isolation, and parentage within natural guppy populations.

Research paper thumbnail of Critical review of NGS analyses for de novo genotyping multigene families

Molecular Ecology, Jul 21, 2014

The genotyping of highly polymorphic multigene families across many individuals used to be a part... more The genotyping of highly polymorphic multigene families across many individuals used to be a particularly challenging task because of methodological limitations associated with traditional approaches. Next generation sequencing (NGS) can overcome most of these limitations, and it is increasingly being applied in population genetic studies of multigene families. Here, we critically review NGS bioinformatic approaches that have been used to genotype the Major Accepted Article This article is protected by copyright. All rights reserved. Histocompatability Complex (MHC) immune genes, and we discuss how the significant advances made in this field are applicable to population genetic studies of gene families. Increasingly, approaches are introduced that apply thresholds of sequencing depth and sequence similarity to separate alleles from methodological artefacts. We explain why these methods are particularly sensitive to methodological biases by violating fundamental genotyping assumptions. An alternative approach that utilizes ultra-deep sequencing (hundreds to thousands of sequences per amplicon) to reconstruct genotypes and applies statistical methods on the sequencing depth to separate alleles from artefacts appears to be more robust. Importantly, the "degree of change" (DOC) method avoids using arbitrary cutoff thresholds by looking for statistical boundaries between the sequencing depth for alleles and artefacts, and hence, it is entirely repeatable across studies. Although the advances made in generating NGS data are still far ahead of our ability to reliably process, interpret and analyse the data, the community is developing statistically rigorous protocols that will allow us to address novel questions in evolution, ecology, and genetics. Future developments in third generation singlemolecule sequencing may potentially help overcome problems that still persist in de novo multigene amplicon genotyping when using current second generation sequencing approaches. Accepted Article This article is protected by copyright. All rights reserved. and rapidly generated. However, with ever-decreasing costs, genetic datasets become bigger and so do the challenges in analyzing them. Ironically, some of the genes that have taught us the most about adaptive processes in the last three decades prove to offer some of the biggest challenges. Consider for example the adaptive immunity genes of the major histocompatability complex (MHC), which are among the best-studied systems in evolutionary genetics. The MHC is a notoriously difficult region to assemble and characterize, even when using non-targeted 'shotgun' sequencing approaches aimed at resolving large unknown genomic regions (Warren et al. 2012). Approaches that target individual MHC genes in multiple individuals (i.e. in population genetic studies) have been popular, yet bear a unique set of problems that still hinder accurate MHC characterization (see Babik 2010, and below). Moreover, newly emerging targeted NGS analyses raise novel complications that need to be considered when genotyping highly polymorphic multigene families. In this review we will discuss the current advances made in this field, and although we focus on the MHC, the lessons learned from analyzing these genes can be extended and applied to other multigene families, including resistance genes (R-genes) and self-incompatibility genes (SI-genes) in plants; the P450 superfamily and ATP-binding cassette transporter superfamily present in all domains of life; homeobox genes in animals, plants and fungi; the immunoglobin superfamily in vertebrates; effector and virulence genes in pathogens; reptile toxin genes; cadherin cell adhesion genes, and many more (e.g., see www.genenames.org/genefamilies; www.genomics.msu.edu/cgibin/plant_specific/family_search.cgi). The vertebrate immune genes of the MHC are perhaps the most studied gene family and remain one of the best systems to investigate the effects of evolutionary forces operating

Research paper thumbnail of Genetic Diversity

Research paper thumbnail of Kinship Analysis of Pacific Salmon: Insights Into Mating, Homing, and Timing of Reproduction

Journal of Heredity, 2001

Multilocus microsatellite genotypes were used to infer kinship and relatedness in two species of ... more Multilocus microsatellite genotypes were used to infer kinship and relatedness in two species of Pacific salmon from three populations in Washington State. Even in the absence of direct genetic data from parents, clustering of individuals according to allele sharing and reconstruction of parental genotypes allowed resolution of full-and half-sib relationships among 135 chinook salmon (Oncorhynchus tshawytscha) sampled as preemergent juveniles from 14 redds in the Dungeness River. Inferred reproductive behaviors included single-pair matings, polyandry in which females mated with two to three males at a single redd, polygyny in which males mated with two females at different redds, use of two redds by a single female, and use of one redd site by two females. Greater average relatedness (r xy) in the upper reach of the Dungeness River implied within-reach homing of returning adults. In steelhead trout (O. mykiss), the frequency of related pairs (dyads) of mature individuals that migrated up Snow Creek less than a week apart was greater than expected for randomly chosen dyads, as was the frequency of steelhead dyads that were spawned on the same day in the Forks Creek hatchery. These results imply a heritable basis for upstream migration date and maturation date in steelhead trout.

Research paper thumbnail of Multiple decades of stocking has resulted in limited hatchery introgression in wild brook trout (<i>Salvelinus fontinalis</i>) populations of Nova Scotia

Evolutionary Applications, Feb 20, 2020

This is an open access article under the terms of the Creative Commons Attribution License, which... more This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Research paper thumbnail of Polymorphic tetranucleotide microsatellite markers in the Caribbean spiny lobster, Panulirus argus

Molecular Ecology Notes, Sep 1, 2004

Ten tetranucleotide microsatellite loci are described for the Caribbean spiny lobster Panulirus a... more Ten tetranucleotide microsatellite loci are described for the Caribbean spiny lobster Panulirus argus. Loci were polymorphic (4–15 alleles per locus) and exhibited high levels of expected (0.553–0.921) and observed heterozygosity (0.469–0.906) from samples caught off Belize and Puerto Rico coasts. No significant departure from Hardy–Weinberg equilibrium conditions were observed for any locus. All microsatellite loci should be useful for assessing population discrimination for this valuable marine animal currently subjected to excessive fishing efforts.

Research paper thumbnail of Loss of genetic diversity and reduction of genetic distance among lake trout Salvelinus namaycush ecomorphs, Lake Superior 1959 to 2013

Journal of Great Lakes Research, Apr 1, 2016

North America's northern lakes are undergoing major changes. Lake Superior is the coldest and nor... more North America's northern lakes are undergoing major changes. Lake Superior is the coldest and northernmost of the Laurentian Great Lakes. Here, we present an extension of a long-term data set that monitors genetic and phenotypic diversity of lake trout Salvelinus namaycush in Lake Superior. Hypotheses were investigated pertaining to loss of genetic diversity and genetic homogenization among three lake trout ecomorphs in Lake Superior during their recovery several decades after a major fishery collapse in the early 1960s. Comparison of a contemporary (2004-2013) microsatellite DNA data set to a previously published, post-collapse recovery period data set (1995-1999) indicated substantive losses in genetic diversity. Allelic richness decreased by 5.7%, 12.3%, and 6.8% at Isle Royale, Stannard Rock, and Klondike Reef, respectively. A 60.7% reduction in genetic distance among ecomorphs since the 1990s was detected. Comparisons with a third data set of samples collected during the fishery collapse (1959) indicated an overall 18.2% loss in allelic richness at Isle Royale. The amount of introgression among ecomorphs has likely increased over time. Apparent losses in genetic diversity could be a consequence of historical fishery harvests (early 1900s) exacerbated by intensive stocking (1950s-1980s) and invasions of non-native species (1960s-1990s). Overlap in foraging and breeding areas may have contributed to increasing levels of hybridization among ecomorphs. Knowledge of these processes will help to identify impediments and strategies for the maintenance of lake trout biodiversity in northern Great Lakes, and their re-establishment in the Laurentian Great Lakes.

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

Evolutionary Applications, Mar 11, 2018

This is an open access article under the terms of the Creative Commons Attribution License, which... more This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Research paper thumbnail of Ultra-deep Illumina sequencing accurately identifies MHC class IIb alleles and provides evidence for copy number variation in the guppy (<i>Poecilia reticulata</i>)

Molecular Ecology Resources, Feb 5, 2014

We address the bioinformatic issue of accurately separating amplified genes of the major histocom... more We address the bioinformatic issue of accurately separating amplified genes of the major histocompatibility complex (MHC) from artefacts generated during high‐throughput sequencing workflows. We fit observed ultra‐deep sequencing depths (hundreds to thousands of sequences per amplicon) of allelic variants to expectations from genetic models of copy number variation (CNV). We provide a simple, accurate and repeatable method for genotyping multigene families, evaluating our method via analyses of 209 b of MHC class IIb exon 2 in guppies (Poecilia reticulata). Genotype repeatability for resequenced individuals (N = 49) was high (100%) within the same sequencing run. However, repeatability dropped to 83.7% between independent runs, either because of lower mean amplicon sequencing depth in the initial run or random PCR effects. This highlights the importance of fully independent replicates. Significant improvements in genotyping accuracy were made by greatly reducing type I genotyping error (i.e. accepting an artefact as a true allele), which may occur when using low‐depth allele validation thresholds used by previous methods. Only a small amount (4.9%) of type II error (i.e. rejecting a genuine allele as an artefact) was detected through fully independent sequencing runs. We observed 1–6 alleles per individual, and evidence of sharing of alleles across loci. Variation in the total number of MHC class II loci among individuals, both among and within populations was also observed, and some genotypes appeared to be partially hemizygous; total allelic dosage added up to an odd number of allelic copies. Collectively, observations provide evidence of MHC CNV and its complex basis in natural populations.

Research paper thumbnail of Author Correction: Genomic evidence of past and future climate-linked loss in a migratory Arctic fish

Nature Climate Change, 2021

In the version of this Article originally published, ref. 84 was an article that has since been r... more In the version of this Article originally published, ref. 84 was an article that has since been retracted; it has now been replaced with "Salvelinus. NCBI https://www.ncbi.nlm.nih.gov/genome/86400 (2021). " This change does not alter the results or findings of the study. The online versions of the Article have been corrected.

Research paper thumbnail of Loma morhua infections in Atlantic cod (Gadus morhua) reveal relative parasite resistance and differential effects on host growth among family lines

Aquaculture, 2020

infections in Atlantic cod (Gadus morhua) reveal relative parasite resistance and differential ef... more infections in Atlantic cod (Gadus morhua) reveal relative parasite resistance and differential effects on host growth among family lines, aquaculture (2020),

Research paper thumbnail of Parasite diversity and ecology in a model species, the guppy ( Poecilia reticulata ) in Trinidad

Royal Society Open Science, 2020

The guppy ( Poecilia reticulata ) is a model species in ecology and evolution. Many studies have ... more The guppy ( Poecilia reticulata ) 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 an...

Research paper thumbnail of Microsatellite markers developed in the stingless bee Melipona fasciculata by next-generation sequencing and an exploratory analysis of geographic genetic variation

Background. Native meliponines are currently threatened by increased human impacts. The assessmen... more Background. Native meliponines are currently threatened by increased human impacts. The assessment of their genetic variation by microsatellite DNA markers can assist in the conservation of populations and help in the planning and establishment of efficient management strategies. Next generation sequencing has proven to be useful for identifying microsatellite loci from the large amounts of sequence data generated. Methods. The purpose of this study was to develop the first set of microsatellite markers for Melipona fasciculata, selected from partial genome assembly of Illumina paired-end reads. Contigs were created from the resulting paired-end sequence data and these were analyzed with specialized software to extract those reads that contained microsatellite loci. Primer pairs were designed for each detected locus at their flanking regions. Bee samples were genotyped from two different locations for markers characterization and validation. Results. A total of 17 microsatellite loc...

Research paper thumbnail of Range-wide regional assignment of Atlantic salmon (Salmo salar) using genome wide single-nucleotide polymorphisms

Fisheries Research, 2018

The estimation of stock specific exploitation is imperative to fisheries management and the conse... more The estimation of stock specific exploitation is imperative to fisheries management and the conservation of biodiversity, particularly in instances where fisheries simultaneously exploit mixtures of stocks. Mixed stock harvests are particularly common in species that have extensive marine migrations, such as Atlantic and Pacific salmon. Here we develop a range-wide genetic baseline for Atlantic salmon (Salmo salar) from North American and European rivers to allow regional assignment of individuals targeted in international mixed stock fisheries. A combination of published data and additional genotyping was used to assemble a dataset of 96 SNPs for 285 range-wide Atlantic salmon populations for regional assignment. Clustering of baseline samples identified 20 North American and eight European reporting groups with mean individual assignment accuracy of 90% (range 70-100%). This baseline was applied to disentangle the stock composition of individuals in a subset of individuals from the West Greenland Atlantic salmon fishery. Genetic mixture analysis revealed that both European and North American individuals originated from multiple regions, with 92% of European individuals originating from the United Kingdom and Ireland, and North American individuals originating from three regions; Gulf of St. Lawrence (28%), Gaspé Peninsula (23%), and coastal Labrador (21%). The baseline represents a significant resource for the management of Atlantic salmon fisheries and the quantification of salmon migration patterns at sea.

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

Molecular Ecology, 2018

Conservation of exploited species requires an understanding of both genetic diversity and the dom... more 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 Accepted Article This article is protected by copyright. All rights reserved. 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.

Research paper thumbnail of Discovery of novel NGS-mined microsatellite markers and an exploratory analysis of genetic differentiation between two Western Atlantic populations ofCardisoma guanhumiLatreille, 1825 (Decapoda: Brachyura: Gecarcinidae)

Journal of Crustacean Biology, 2019

Research paper thumbnail of Challenge to the model of lake charr evolution: shallow- and deep-water morphs exist within a small postglacial lake

Biological Journal of the Linnean Society, 2016

All examples of lake charr (Salvelinus namaycush) diversity occur within the largest, deepest lak... more All examples of lake charr (Salvelinus namaycush) diversity occur within the largest, deepest lakes of North America (i.e. > 2000 km 2). We report here Rush Lake (1.3 km 2) as the first example of a small lake with two lake charr morphs (lean and huronicus). Morphology, diet, life history, and genetics were examined to demonstrate the existence of morphs and determine the potential influence of evolutionary processes that led to their formation or maintenance. Results showed that the huronicus morph, caught in deep-water, had a deeper body, smaller head and jaws, higher eye position, greater buoyancy, and deeper peduncle than the shallow-water lean morph. Huronicus grew slower to a smaller adult size, and had an older mean age than the lean morph. Genetic comparisons showed low genetic divergence between morphs, indicating incomplete reproductive isolation. Phenotypic plasticity and differences in habitat use between deep and shallow waters associated with variation in foraging opportunities seems to have been sufficient to maintain the two morphs, demonstrating their important roles in resource polymorphism. Rush Lake expands previous explanations for lake charr intraspecific diversity, from large to small lakes and from reproductive isolation to the presence of gene flow associated with strong ecological drivers. Published 2016. This article has been contributed to by US Government employees and their work is in the public domain in the USA,

Research paper thumbnail of Genomic basis of deep‐water adaptation in Arctic Charr ( <i>Salvelinus alpinus</i> ) morphs

Molecular Ecology, Aug 12, 2021

Research paper thumbnail of A putative structural variant and environmental variation associated with genomic divergence across the Northwest Atlantic in Atlantic Halibut

Ices Journal of Marine Science, Aug 1, 2021

39 40 Characterizing the nature of genetic differentiation among individuals and populations and ... more 39 40 Characterizing the nature of genetic differentiation among individuals and populations and its 41 distribution across the genome is increasingly important to inform both conservation and management 42 of exploited species. Atlantic Halibut (Hippoglossus hippoglossus) is an ecologically and 43 commercially important fish species, yet knowledge of population structure and genomic diversity in 44 this species remains lacking. Here, we use restriction-site associated DNA sequencing and a 45 chromosome-level genome assembly to identify over 86,000 single nucleotide polymorphisms mapped 46 to 24 chromosome-sized scaffolds, genotyped in 734 individuals across the Northwest Atlantic. We 47 describe subtle but significant genome-wide regional structuring between the Gulf of St. Lawrence and 48 adjacent Atlantic continental shelf. However, the majority of genetic divergence is associated with a 49 large putative chromosomal rearrangement (5.74 megabases) displaying high differentiation and 50 linkage disequilibrium, but no evidence of geographic variation. Demographic reconstructions suggest 51 periods of expansion coinciding with glacial retreat, and more recent declines in N e. This work 52 highlights the utility of genomic data to identify multiple sources of genetic structure and genomic 53 diversity in commercially exploited marine species. 54

Research paper thumbnail of Genetic and phenotypic variation along an ecological gradient in lake trout Salvelinus namaycush

BMC Evolutionary Biology, Oct 19, 2016

Background: Adaptive radiation involving a colonizing phenotype that rapidly evolves into at leas... more Background: Adaptive radiation involving a colonizing phenotype that rapidly evolves into at least one other ecological variant, or ecotype, has been observed in a variety of freshwater fishes in post-glacial environments. However, few studies consider how phenotypic traits vary with regard to neutral genetic partitioning along ecological gradients. Here, we present the first detailed investigation of lake trout Salvelinus namaycush that considers variation as a cline rather than discriminatory among ecotypes. Genetic and phenotypic traits organized along common ecological gradients of water depth and geographic distance provide important insights into diversification processes in a lake with high levels of human disturbance from over-fishing. Results: Four putative lake trout ecotypes could not be distinguished using population genetic methods, despite morphological differences. Neutral genetic partitioning in lake trout was stronger along a gradient of water depth, than by locality or ecotype. Contemporary genetic migration patterns were consistent with isolation-by-depth. Historical gene flow patterns indicated colonization from shallow to deep water. Comparison of phenotypic (Pst) and neutral genetic variation (Fst) revealed that morphological traits related to swimming performance (e.g., buoyancy, pelvic fin length) departed more strongly from neutral expectations along a depth gradient than craniofacial feeding traits. Elevated phenotypic variance with increasing water depth in pelvic fin length indicated possible ongoing character release and diversification. Finally, differences in early growth rate and asymptotic fish length across depth strata may be associated with limiting factors attributable to cold deep-water environments. Conclusion: We provide evidence of reductions in gene flow and divergent natural selection associated with water depth in Lake Superior. Such information is relevant for documenting intraspecific biodiversity in the largest freshwater lake in the world for a species that recently lost considerable genetic diversity and is now in recovery. Unknown is whether observed patterns are a result of an early stage of incipient speciation, gene flow-selection equilibrium, or reverse speciation causing formerly divergent ecotypes to collapse into a single gene pool.

Research paper thumbnail of Characterization of tetranucleotide microsatellite markers in guppy (Poecilia reticulata)

Molecular Ecology Notes, Feb 17, 2005

Ten tetranucleotide microsatellite loci are characterized for guppy, Poecilia reticulata , an imp... more Ten tetranucleotide microsatellite loci are characterized for guppy, Poecilia reticulata , an important model species in the study of adaptation and mating systems. Loci were isolated following a microsatellite enrichment procedure using probe-labelled magnetic beads. These microsatellites were designed for use in examining gene flow, reproductive isolation, and parentage within natural guppy populations.

Research paper thumbnail of Critical review of NGS analyses for de novo genotyping multigene families

Molecular Ecology, Jul 21, 2014

The genotyping of highly polymorphic multigene families across many individuals used to be a part... more The genotyping of highly polymorphic multigene families across many individuals used to be a particularly challenging task because of methodological limitations associated with traditional approaches. Next generation sequencing (NGS) can overcome most of these limitations, and it is increasingly being applied in population genetic studies of multigene families. Here, we critically review NGS bioinformatic approaches that have been used to genotype the Major Accepted Article This article is protected by copyright. All rights reserved. Histocompatability Complex (MHC) immune genes, and we discuss how the significant advances made in this field are applicable to population genetic studies of gene families. Increasingly, approaches are introduced that apply thresholds of sequencing depth and sequence similarity to separate alleles from methodological artefacts. We explain why these methods are particularly sensitive to methodological biases by violating fundamental genotyping assumptions. An alternative approach that utilizes ultra-deep sequencing (hundreds to thousands of sequences per amplicon) to reconstruct genotypes and applies statistical methods on the sequencing depth to separate alleles from artefacts appears to be more robust. Importantly, the "degree of change" (DOC) method avoids using arbitrary cutoff thresholds by looking for statistical boundaries between the sequencing depth for alleles and artefacts, and hence, it is entirely repeatable across studies. Although the advances made in generating NGS data are still far ahead of our ability to reliably process, interpret and analyse the data, the community is developing statistically rigorous protocols that will allow us to address novel questions in evolution, ecology, and genetics. Future developments in third generation singlemolecule sequencing may potentially help overcome problems that still persist in de novo multigene amplicon genotyping when using current second generation sequencing approaches. Accepted Article This article is protected by copyright. All rights reserved. and rapidly generated. However, with ever-decreasing costs, genetic datasets become bigger and so do the challenges in analyzing them. Ironically, some of the genes that have taught us the most about adaptive processes in the last three decades prove to offer some of the biggest challenges. Consider for example the adaptive immunity genes of the major histocompatability complex (MHC), which are among the best-studied systems in evolutionary genetics. The MHC is a notoriously difficult region to assemble and characterize, even when using non-targeted 'shotgun' sequencing approaches aimed at resolving large unknown genomic regions (Warren et al. 2012). Approaches that target individual MHC genes in multiple individuals (i.e. in population genetic studies) have been popular, yet bear a unique set of problems that still hinder accurate MHC characterization (see Babik 2010, and below). Moreover, newly emerging targeted NGS analyses raise novel complications that need to be considered when genotyping highly polymorphic multigene families. In this review we will discuss the current advances made in this field, and although we focus on the MHC, the lessons learned from analyzing these genes can be extended and applied to other multigene families, including resistance genes (R-genes) and self-incompatibility genes (SI-genes) in plants; the P450 superfamily and ATP-binding cassette transporter superfamily present in all domains of life; homeobox genes in animals, plants and fungi; the immunoglobin superfamily in vertebrates; effector and virulence genes in pathogens; reptile toxin genes; cadherin cell adhesion genes, and many more (e.g., see www.genenames.org/genefamilies; www.genomics.msu.edu/cgibin/plant_specific/family_search.cgi). The vertebrate immune genes of the MHC are perhaps the most studied gene family and remain one of the best systems to investigate the effects of evolutionary forces operating

Research paper thumbnail of Genetic Diversity