Ben Sutherland

Salmonid chromosome evolution as revealed by a novel method for comparing RADseq linkage maps

Whole genome duplication (WGD) can provide material for evolutionary innovation. Family Salmonidae is ideal for studying the effects of WGD as the ancestral salmonid underwent WGD relatively recently, ∼65 Ma, then rediploidized and diversified. Extensive synteny between homologous chromosome arms occurs in extant salmonids, but each species has both conserved and unique chromosome arm fusions and fissions. Assembly of large, outbred eukaryotic genomes can be difficult, but structural rearrangements within such taxa can be investigated using linkage maps. RAD sequencing provides unprecedented ability to generate high-density linkage maps for nonmodel species, but can result in low numbers of homologous markers between species due to phylogenetic distance or differences in library preparation. Here, we generate a high-density linkage map (3,826 markers) for the Salvelinus genera (Brook Charr S. fontinalis), and then identify corresponding chromosome arms among the other available salmonid high-density linkage maps, including six species of Oncorhynchus, and one species for each of Salmo, Coregonus, and the nonduplicated sister group for the salmonids, Northern Pike Esox lucius for identifying post-duplicated homeologs. To facilitate this process, we developed MapComp to identify identical and proximate (i.e. nearby) markers between linkage maps using a reference genome of a related species as an intermediate, increasing the number of comparable markers between linkage maps by 5-fold. This enabled a characterization of the most likely history of retained chromosomal rearrangements post-WGD, and several conserved chromosomal inversions. Analyses of RADseq-based linkage maps from other taxa will also benefit from MapComp, available at: https://github.com/enormandeau/mapcomp/

Sex matters in Massive Parallel Sequencing: evidence for biases in genetic parameter estimation and investigation of sex determination systems

Using massively parallel sequencing data from two species with different life history traits, American lobster (Homarus americanus) and Arctic Char (Salvelinus alpinus), we highlight how an unbalanced sex ratio in the samples and a few sex-linked markers may lead to false interpretations of population structure and thus to potentially erroneous management recommendations. Here, multivariate analyses revealed two genetic clusters separating samples by sex instead of by expected spatial variation: inshore and offshore locations in lobster, or east and west locations in Arctic Char. To further investigate this, we created several subsamples artificially varying the sex ratio in the inshore/offshore and east/west groups and then demonstrated that significant genetic differentiation could be observed despite panmixia in lobster, and that FST values were overestimated in Arctic Char. This pattern was due to 12 and 94 sex-linked markers driving differentiation for lobster and Arctic Char, respectively. Removing sex-linked markers led to nonsignificant genetic structure in lobster and a more accurate estimation of FST in Arctic Char. The locations of these markers and putative identities of genes containing or nearby the markers were determined using available transcriptomic and genomic data, and this provided new information related to sex determination in both species. Given that only 9.6% of all marine/diadromous population genomic studies to date have reported sex information, we urge researchers to collect and consider individual sex information. Sex information is therefore relevant for avoiding unexpected biases due to sex-linked markers as well as for improving our knowledge of sex determination systems in nonmodel species.

Genomic patterns of diversity and divergence of two introduced salmonid species in Patagonia, South America

Invasive species have become widespread in aquatic environments throughout the world, yet there are few studies that have examined genomic variation of multiple introduced species in newly colonized environments. In this study, we contrast genomic variation in two salmonid species (anadromous Chinook Salmon, Oncorhynchus tshawytscha, 11,579 SNPs and resident Brook Charr Salvelinus fontinalis, 13,522 SNPs) with differing invasion success after introduction to new environments in South America relative to populations from their native range in North America. Estimates of genetic diversity were not significantly different between introduced and source populations for either species, indicative of propagule pressure that has been shown to maintain diversity in founding populations relative to their native range. Introduced populations also demonstrated higher connectivity and gene flow than those in their native range. Evidence for candidate loci under divergent selection was observed, but was limited to specific introduced populations and was not widely evident. Patterns of genomic variation were consistent with general dispersal potential of each species and therefore also the notion that life history variation may contribute to both invasion success and subsequent genetic structure of these two salmonids in Patagonia.

Sex Chromosome Evolution, Heterochiasmy and Physiological QTL in the Salmonid Brook Charr Salvelinus fontinalis

Whole-genome duplication (WGD) can have large impacts on genome evolution, and much remains unknown about these impacts. This includes the mechanisms of coping with a duplicated sex determination system and whether this has an impact on increasing the diversity of sex determination mechanisms. Other impacts include sexual conflict, where alleles having different optimums in each sex can result in sequestration of genes into nonrecombining sex chromosomes. Sex chromosome development itself may involve sex-specific recombination rate (i.e., heterochiasmy), which is also poorly understood. The family Salmonidae is a model system for these phenomena, having undergone autotetraploidization and subsequent rediploidization in most of the genome at the base of the lineage. The salmonid master sex determining gene is known, and many species have nonhomologous sex chromosomes, putatively due to transposition of this gene. In this study, we identify the sex chromosome of Brook Charr Salvelinus fontinalis and compare sex chromosome identities across the lineage (eight species and four genera). Although nonhomology is frequent, homologous sex chromosomes and other consistencies are present in distantly related species, indicating probable convergence on specific sex and neo-sex chromosomes. We also characterize strong heterochiasmy with 2.7-fold more crossovers in maternal than paternal haplotypes with paternal crossovers biased to chromosome ends. When considering only rediploidized chromosomes, the overall heterochiasmy trend remains, although with only 1.9-fold more recombination in the female than the male. Y chromosome crossovers are restricted to a single end of the chromosome, and this chromosome contains a large interspecific inversion, although its status between males and females remains unknown. Finally, we identify quantitative trait loci (QTL) for 21 unique growth, reproductive, and stress-related phenotypes to improve knowledge of the genetic architecture of these traits important to aquaculture and evolution.

Genomics and telemetry suggest a role for migration harshness in determining overwintering habitat choice, but not gene flow, in anadromous Arctic Char

Migration is a ubiquitous life history trait with profound evolutionary and ecological consequences. Recent developments in telemetry and genomics, when combined, can bring significant insights on the migratory ecology of nonmodel organisms in the wild. Here, we used this integrative approach to document dispersal, gene flow and potential for local adaptation in anadromous Arctic Char from six rivers in the Canadian Arctic. Acoustic telemetry data from 124 tracked individuals indicated asymmetric dispersal, with a large proportion of fish (72%) tagged in three different rivers migrating up the same short river in the fall. Population genomics data from 6,136 SNP markers revealed weak, albeit significant, population differentiation (average pairwise FST = 0.011) and asymmetric dispersal was also revealed by population assignments. Approximate Bayesian computation simulations suggested the presence of asymmetric gene flow, although in the opposite direction to that observed from the telemetry data, suggesting that dispersal does not necessarily lead to gene flow. These observations suggested that Arctic Char home to their natal river to spawn, but may overwinter in rivers with the shortest migratory route to minimize the costs of migration in nonbreeding years. Genome scans and genetic–environment associations identified 90 outlier markers putatively under selection, 23 of which were in or near a gene. Of these, at least four were involved in muscle and cardiac function, consistent with the hypothesis that migratory harshness could drive local adaptation. Our study illustrates the power of integrating genomics and telemetry to study migrations in nonmodel organisms in logistically challenging environments such as the Arctic.

Novel Method for Comparing RADseq Linkage Maps Reveals Chromosome Evolution in Salmonids

Genome duplication can provide material for evolutionary innovation, and much remains unknown about its functional effects. Assembly of large, outbred eukaryotic genomes is difficult, but structural rearrangements within such taxa can be investigated using linkage maps. RAD sequencing provides unprecedented ability to generate high-density linkage maps for non-model species. However, these methods often result in a low number of homologous markers between species due to phylogenetic distance or technical differences in library preparation. Family Salmonidae is ideal for studying the effects of whole genome duplication. The ancestral salmonid underwent whole genome duplication around 65 million years ago and the tetraploid genome has undergone rediploidization during the salmonid diversification. In the salmonids, synteny occurs between orthologous chromosomes, but each species exhibits conserved and unique chromosome arm fusions and fissions. In this study, we identify orthologous chromosome arms within the salmonids using available RADseq salmonid linkage maps along with a new high-density linkage map (3826 markers) constructed for the Salvelinus genera (Brook Charr S. fontinalis ). We developed MapComp, a program that identifies identical and proximal markers between linkage maps using a reference genome of a related species as an intermediate (e.g. Rainbow Trout Oncorhynchus mykiss ). We greatly increased the number of comparable markers between linkage maps relative to that obtained using only identical markers. This enabled a characterization of the most likely history of retained chromosomal rearrangements post-whole genome duplication in five species of Oncorhynchus , and one species of each of Salvelinus , Salmo , and Coregonus , representing all of the main salmonid genera. Additionally, integration with the genetic map of the pre-duplicated sister species Northern Pike Esox lucius permitted the identification of homeologous chromosomes in all species. Putative conserved inversions within chromosome arms were also identified among species. Analyses of RADseq-based linkage maps from other taxa are likely to benefit from MapComp, available at: https://github.com/enormandeau/mapcomp/.Whole genome duplication (WGD) can provide material for evolutionary innovation. Assembly of large, outbred eukaryotic genomes can be difficult, but structural rearrangements within such taxa can be investigated using linkage maps. RAD sequencing provides unprecedented ability to generate high-density linkage maps for non-model species, but can result in low numbers of homologous markers between species due to phylogenetic distance or differences in library preparation. Family Salmonidae is ideal for studying the effects of WGD as the ancestral salmonid underwent WGD relatively recently, around 65 million years ago, then rediploidized and diversified. Extensive synteny between orthologous chromosomes occurs in extant salmonids, but each species has both conserved and unique chromosome arm fusions and fissions. Here we generate a high-density linkage map (3826 markers) for the Salvelinus genera (Brook Charr S. fontinalis), and then identify orthologous chromosome arms among the other available salmonid high-density linkage maps, including six species of Oncorhynchus, and one species for each of Salmo and Coregonus, as well as the sister group for the salmonids, Esox lucius for homeolog designation. To this end, we developed MapComp, a program that identifies identical and proximal markers between linkage maps using a reference genome of a related species as an intermediate. This approach increases the number of comparable markers between linkage maps by 5-fold, enabling a characterization of the most likely history of retained chromosomal rearrangements post-WGD, and identifying several conserved chromosomal inversions. Analyses of RADseq-based linkage maps from other taxa will also benefit from MapComp, available at: https://github.com/enormandeau/mapcomp/

Migration Harshness Drives Habitat Choice And Local Adaptation In Anadromous Arctic Char: Evidence From Integrating Population Genomics And Acoustic Telemetry

Migration is a ubiquitous life history trait with profound evolutionary and ecological consequences. Recent developments in telemetry and genomics, when combined, can bring significant insights on the migratory ecology of non-model organisms in the wild. Here, we used this integrative approach to document dispersal, gene flow and potential for local adaptation in anadromous Arctic Char from six rivers in the Canadian Arctic. Acoustic telemetry data from 124 tracked individuals indicated asymmetric dispersal, with a large proportion of fish (72%) tagged in three different rivers migrating up the same short river in the fall. Population genomics data from 6,136 SNP markers revealed weak, albeit significant, population differentiation (average pairwise FST = 0.011) and asymmetric dispersal was also revealed by population assignments. Approximate Bayesian Computation simulations suggested the presence of asymmetric gene flow, although in the opposite direction to that observed from the telemetry data, suggesting that dispersal does not necessarily lead to gene flow. These observations suggested that Arctic Char home to their natal river to spawn, but may overwinter in rivers with the shortest migratory route to minimize the costs of migration in non-breeding years. Genome scans and genetic-environment associations identified 90 outlier markers putatively under selection, 23 of which were in or near a gene. Of these, at least four were involved in muscle and cardiac function, consistent with the hypothesis that migratory harshness could drive local adaptation. Our study illustrates the power of integrating genomics and telemetry to study migrations in non-model organisms in logistically challenging environments such as the Arctic.Migration is a ubiquitous life history trait with profound evolutionary and ecological consequences. Recent developments in telemetry and genomics, when combined, can bring significant insights on the migratory ecology of non-model organisms in the wild. Here, we used this integrative approach to document dispersal, gene flow and local adaptation in anadromous Arctic Char from six rivers in the Canadian Arctic. Telemetry data from 124 tracked individuals indicated asymmetric dispersal, with a large proportion (72%) of fish tagged in three rivers migrating up the shortest river in the fall. Population genomics data from 6,136 SNP markers revealed weak, albeit significant, population differentiation (FST = 0.011) and population assignments confirmed the asymmetric dispersal revealed by telemetry data. Approximate Bayesian Computation simulations suggested the presence of asymmetric gene flow but in the opposite direction than that observed from the telemetry data, suggesting that dispersal does not necessarily lead to gene flow. These observations suggested that Arctic Char home to their natal river to spawn, but may overwinter in rivers with the least harsh migratory route to minimize the costs of migration in non-breeding years. Genome scans and genetic-environment-associations identified 90 markers putatively associated with local adaptation, 23 of which were in or near a gene. Of those, at least four were involved in muscle and cardiac function, further highlighting the potential importance of migratory harshness as a selective pressure. Our study illustrates the power of integrating genomic and telemetry to study migrations in non-model organisms in logistically challenging environments such as the Arctic.