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Rondeau, E. B.

Publications and source records attributed to Rondeau, E. B..

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Whole genome analyses of the endangered Northern abalone (Haliotis kamtschatkana) reveal population differentiation and a genomic signature of a dramatic population decline

Despite widespread declines of many wildlife species, the effects of population decline on the genetic health and the recovery potential of affected species is still poorly understood, especially beyond a few charismatic species. The Northern abalone (or Pinto abalone; Haliotis kamtschatkana) is a marine gastropod mollusc of social, cultural and historical economic importance in the Pacific Northwest of North America that experienced a decline in population density due to commercial harvest and is currently listed as endangered in Canada under the Species at Risk Act. Previous genetic investigations based on microsatellites and reduced-representation approaches concluded that Northern abalone is panmictic throughout its range, from Alaska to California, and identified high levels of genetic variation with no indication of population decline. Using whole genome resequencing data from Northern abalone sampled across the northern part of the species range, we instead identified both: 1) significant differentiation between two genetic groups, albeit very concentrated in the genome; and 2) a strong signature of a dramatic population decline, without evidence of genetic inbreeding. Even though demographic reconstructions showed a timid signal of recent population expansion, the pervasive excess of rare alleles identified (including a high occurrence of singletons) may pose a genetic load risk, potentially hindering the species recovery. We also found evidence of historical, rather than current, connectivity throughout the area investigated. These results are important for management decisions and highlight the utility of whole genome data in conservation, especially in species with historically large effective population sizes like the Northern abalone.

evolutionary biology↗

Revealing the evolutionary history and contemporary population structure of Pacific salmon in the Fraser River through genome resequencing

The Fraser River once supported massive salmon returns, but now years with half of the recorded historical maximum are considered good. There is substantial interest from surrounding communities, governments, and other groups to increase salmon returns for both human use and for functional ecosystems. To help generate resources for this endeavour, we resequenced hundreds of genomes at moderate coverage ([~]16x) of Chinook (Oncorhynchus tshawytscha), coho (O. kisutch), and sockeye salmon (O. nerka) from the Fraser River. The resequenced genomes are an important resource that can give us new insights. In this study, we found evidence that Chinook salmon have 1.5-2x more polymorphic loci than coho or sockeye salmon. Using principal component analysis (PCA) and admixture analysis, we also identified genetic groups similar to those previously identified with only a few microsatellite markers. As the higher density data supports these previous genetic groups, it suggests that the identity of these groups is not overly sensitive to the number of genetic markers or when the groups were sampled. With the increased resolution from resequenced genomes, we were able to further identify factors influencing these genetic groups, including isolation-by-distance, migration barriers, recolonization from different glacial refugia, and environmental factors like precipitation. We were also able to identify 20 potentially adaptive loci among the genetic groups by analyzing runs of homozygosity. All of the resequenced genomes have been submitted to a public database where they can be used as a reference for the contemporary genomics of Fraser River salmon. Article SummaryConcerns over Fraser River salmon declines led us to generate resources to better understand the genetics of these salmon. Our findings were similar to previous studies that examined a very small fraction of the genetic markers examined here. We expanded upon previous studies by identifying possible influences on the genetics of Fraser River salmon. These included environmental factors, historical differences, and a lack of connectivity in the river caused by the Fraser Canyon.

evolutionary biology↗

Isolation-by-distance and population-size history inferences from the coho salmon (Oncorhynchus kisutch) genome

Coho salmon (Oncorhynchus kisutch) are a culturally and economically important species that return from multiyear ocean migrations to spawn in rivers that flow to the Northern Pacific Ocean. Southern stocks of coho salmon have significantly declined over the past quarter century, and unfortunately, conservation efforts have not reversed this trend. To assist in stock management and conservation efforts, we generated two chromosome-level genome assemblies and sequenced 24 RNA-seq libraries to better annotate the coho salmon genome assemblies. We also resequenced the genomes of 83 coho salmon across their North American range to identify nucleotide variants, characterize the broad effects of isolation-by-distance using a genome-wide association analysis approach, and understand the demographic histories of these salmon by modeling population size from genome-wide data. We observed that more than 13% of all SNPs were associated with latitude (before multiple test correction), likely an affect of isolation-by-distance. From demographic history modeling, we estimated that the SNP latitudinal gradient likely developed as recently as 8,000 years ago. In addition, we identified four genes each harboring multiple SNPs associated with latitude; all of these SNPs were also predicted to modify the function of the gene. Three of these genes have roles in cell junction maintenance and may be involved in osmoregulation. This signifies that ocean salinity may have been a factor influencing coho salmon recolonization after the last glaciation period - generating the current pattern of variation in these three genes.

genomics↗

Genome assembly, transcriptome and SNP database for chum salmon (Oncorhynchus keta)

Chum salmon (Oncorhynchus keta) is the species with the widest geographic range of the anadromous Pacific salmonids. Chum salmon is the second largest of the Pacific salmon, behind Chinook salmon, and considered the most plentiful Pacific salmon by overall biomass. This species is of significant commercial and economic importance: on average the commercial chum salmon fishery has the second highest processed value of the Pacific salmon within British Columbia. The aim of this work was to establish genomic baseline resources for this species. Our first step to accomplish this goal was to generate a chum salmon reference genome assembly from a doubled-haploid chum salmon. Gene annotation of this genome was facilitated by an extensive RNA-seq database we were able to create from multiple tissues. Range-wide resequencing of chum salmon genomes allowed us to categorize genome-wide geographic variation, which in turn reinforced the idea that genetic differentiation was best described on a regional, rather than at a stock-specific, level. Within British Columbia, chum salmon regional groupings were described at the conservation unit (CU) level, and there may be substructure within particular CUs. Genome wide associations of phenotypic sex to SNP genetic markers identified two clear peaks, a very strong peak on Linkage Group 15, and another on Linkage Group 3. With these new resources, we were better able to characterize the sex-determining region and gain further insights into sex determination in chum salmon and the general biology of this species.

genomics↗

Long distance migration is a major factor driving local adaptation at continental scale in Coho Salmon

Inferring the genomic basis of local adaptation is a long-standing goal of evolutionary biology. Beyond its fundamental evolutionary implications, such knowledge can guide conservation decisions for populations of conservation and management concern. Here, we investigated the genomic basis of local adaptation in the Coho salmon (Oncorhynchus kisutch) across its entire North American range. We hypothesized that extensive spatial variation in environmental conditions and the species homing behavior may promote the establishment of local adaptation. We genotyped 7,829 individuals representing 217 sampling locations at more than 100,000 high-quality RADseq loci to investigate how recombination might affect the detection of loci putatively under selection and took advantage of the precise description of the demographic history of the species from our previous work to draw accurate population genomic inferences about local adaptation. Results indicated that genetic differentiation scans and genetic-environment association analyses were both significantly affected by variation in recombination rate as low recombination regions displayed an increased number of outliers. By taking these confounding factors into consideration, we revealed that migration distance was the primary selective factor driving local adaptation and partial parallel divergence among distant populations. Moreover, we identified several candidates SNP associated with long distance migration and altitude including a gene known to be involved in adaptation to altitude in other species. The evolutionary implications of our findings are discussed along with conservation applications.

evolutionary biology↗

The pink salmon genome: uncovering the genomic consequences of a strict two-year life-cycle

Pink salmon (Oncorhynchus gorbuscha) adults are the smallest of the five Pacific salmon native to the western Pacific Ocean. Pink salmon are also the most abundant of these species and account for a large proportion of the commercial value of the salmon fishery worldwide. A strict two-year life-history of most pink salmon generates temporally isolated populations that spawn either in even-years or odd-years. To uncover the influence of this genetic isolation, reference genome assemblies were generated for each year-class and whole genome re-sequencing data was collected from salmon of both year-classes. The salmon were sampled from six Canadian rivers and one Japanese river. At multiple centromeres we identified peaks of Fst between year-classes that were millions of base-pairs long. The largest Fst peak was also associated with a million base-pair chromosomal polymorphism found in the odd-year genome near a centromere. These Fst peaks may be the result of centromere drive or a combination or reduced recombination and genetic drift, and they could influence speciation. Other regions of the genome influenced by odd-year and even-year temporal isolation and tentatively under selection were mostly associated with genes related to immune function, organ development/maintenance, and behaviour.

genomics↗

In-field genetic stock identification of overwintering coho salmon in the Gulf of Alaska: Evaluation of Nanopore sequencing for remote real-time deployment

Genetic stock identification (GSI) by single nucleotide polymorphism (SNP) sequencing has become the gold standard for stock identification in Pacific salmon, which are found in mixed-stocks during the oceanic phase of their lifecycle. Sequencing platforms currently applied require large batch sizes and multi-day processing in specialized facilities to perform genotyping by the thousands. However, recent advances in third-generation single-molecule sequencing platforms, like the Oxford Nanopore minION, provide base calling on portable, pocket-sized sequencers and hold promise for the application of real-time, in-field stock identification on variable batch sizes. Here we report and evaluate utility and comparability of at-sea stock identification of coho salmon Oncorhynchus kisutch based on targeted SNP amplicon sequencing on the minION platform during the International Year of the Salmon Signature Expedition to the Gulf of Alaska in the winter of 2019. Long read sequencers are not optimized for short amplicons, therefore we concatenate amplicons to increase coverage and throughput. Nanopore sequencing at-sea yielded stock assignment for 50 of the 80 assessed individuals. Nanopore-based SNP calls agreed with Ion Torrent based genotypes in 83.25%, but assignment of individuals to stock of origin only agreed in 61.5% of individuals highlighting inherent challenges of Nanopore sequencing, such as resolution of homopolymer tracts and indels. However, poor representation of assayed coho salmon in the queried baseline dataset contributed to poor assignment confidence on both platforms. Future improvements will focus on lowering turnaround time, accuracy, throughput, and cost, as well as augmentation of the existing baselines, specifically in stocks from coastal northern BC and Alaska. If successfully implemented, Nanopore sequencing will provide an alternative method to the large-scale laboratory approach. Genotyping by amplicon sequencing in the hands of diverse stakeholders could inform management decisions over a broad expanse of the coast by allowing the analysis of small batches in remote areas in near real-time.

genetics↗

Comparative regulomics reveals pervasive selection on gene dosage following whole genome duplication

Whole genome duplication (WGD) events have played a major role in eukaryotic genome evolution, but the consequence of these extreme events in adaptive genome evolution is still not well understood. To address this knowledge gap we used a comparative phylogenetic model and transcriptomic data from seven species to infer selection on gene expression in duplicated genes (ohnologs) following the salmonid WGD 80-100 million years ago. We find rare cases of tissue-specific expression evolution but pervasive expression evolution affecting many tissues, reflecting strong selection on maintenance of genome stability following genome doubling. Although ohnolog expression levels have evolved mostly asymmetrically, by diverting one ohnolog copy down a path towards pseudogenization, strong evolutionary constraints have frequently also favoured symmetric shifts in gene dosage of both copies, likely to achieve gene dose reduction while avoiding accumulation of toxic mutations. Mechanistically, ohnolog regulatory divergence is dictated by the number of bound transcription factors in promoters, with transposable elements being one source of novel binding sites driving tissue-specific gains in expression. Our results imply pervasive adaptive expression evolution following WGD to overcome the immediate challenges posed by genome doubling and to exploit the long-term genetic opportunities for novel phenotype evolution.

evolutionary biology↗

Population genomics of North American northern pike: variation and sex-specific signals from a chromosome-level, long read genome assembly

The northern pike Esox lucius is a freshwater fish renowned for having low genetic diversity but ecological success throughout the Northern Hemisphere. Here we generate an annotated chromosome-level genome assembly of 941 Mbp in length with 25 chromosome-length scaffolds using long-reads and chromatin capture technology. We then align whole-genome resequencing data against this reference to genotype northern pike from Alaska through New Jersey (n = 47). A striking decrease in genetic diversity occurs along the sampling range, whereby samples to the west of the North American Continental Divide have substantially higher diversity than populations to the east. As an example, individuals from Interior Alaska in the west and St. Lawrence River in the east have on average 181K and 64K heterozygous SNPs per individual, respectively (i.e., a SNP variant every 3.2 kbp and 11.2 kbp, respectively). Even with such low diversity, individuals clustered with strong support within each population, and this may be related to numerous private alleles in each population. Evidence for recent population expansion was observed for a Manitoba hatchery and the St. Lawrence population (Tajimas D = -1.07 and -1.30, respectively). Non-uniform patterns of diversity were observed across the genome, with large regions showing elevated diversity in several chromosomes, including LG24. In populations with the master sex determining gene amhby still present in the genome, amhby is in LG24. As expected, amhby was largely male-specific in Alaska and the Yukon and absent southeast to these populations, but we also document some amhby(-) males in Alaska and amhby(+) males in the Columbia River. This indicates that rather than a discrete boundary after which amhby was lost in North America, there is a patchwork of presence of this system in the western region. These results support the theory that northern pike recolonized North America from refugia in Alaska and expanded following deglaciation from west to east, with probable founder effects resulting in loss of both neutral and functional diversity including the loss of the sex determination system.

genomics↗

Sex-dependent dominance maintains migration supergene in rainbow trout

Traits with different fitness optima in males and females cause sexual conflict when they have a shared genetic basis. Heteromorphic sex chromosomes can resolve this conflict and protect sexually antagonistic polymorphisms but accumulate deleterious mutations. However, many taxa lack differentiated sex chromosomes, and how sexual conflict is resolved in these species is largely unknown. Here we present a chromosome-anchored genome assembly for rainbow trout (Oncorhynchus mykiss) and characterize a 56 Mb double-inversion supergene that mediates sex-specific migration through sex-dependent dominance, a mechanism that reduces sexual conflict. The double-inversion contains key photosensory, circadian rhythm, adiposity, and sexual differentiation genes and displays frequency clines associated with latitude and temperature, revealing environmental dependence. Our results constitute the first example of sex-dependent dominance across a large autosomal supergene, a novel mechanism for sexual conflict resolution capable of protecting polygenic sexually antagonistic variation while avoiding the homozygous lethality and deleterious mutation load of heteromorphic sex chromosomes.

evolutionary biology↗

Parallel epigenetic modifications induced by hatchery rearing in a Pacific Salmon

Highlights- First study to highlight parallel epigenetic modifications induced by hatchery rearing as a potential explanatory mechanism for rapid change in fitness\n\nSummaryA puzzling question in conservation biology is how to maintain overall fitness of individuals bred in captive environment upon release into the wild, especially for rehabilitating declining or threatened species [1,2]. For salmonid species, a heritable change in fitness related traits and gene expression has been reported to occur in a single generation of captivity in hatchery environment [3-5]. Such rapid changes are congruent with models of inadvertent domestication selection which may lead to maladaptation in the natural environment [4]. Arguably, the underlying mechanism by which captivity may induce fitness difference between wild and captive congeners is still poorly understood. Short-term selection on complex phenotypic traits is expected to induce subtle changes in allele frequency over multiple loci [7-9]. Yet, most studies investigating the molecular basis for rapid change in fitness related traits occurring in hatchery have concentrated their effort on finding evidence for selection at the genome level by identifying loci with large effect.\n\nNumerous wild stocks of Pacific anadromous salmon and trout (genus Oncorhynchus and Salmo) have experienced fluctuating abundance over the past century, with a series of sharp declines [6-8]. With the objectives of preserving ecosystem integrity, enhancing declining populations and sustaining fisheries, conservation hatcheries have been flourishing. This is particularly true along the North American Pacific coast where billions of salmonids, all species included, are released each year. Despite substantial improvement of production management, the beneficial ecological role of hatcheries in enhancing and restoring wild stocks is still debated, mainly because of the reduced fitness and maladaptation of hatchery-fish when released in the wild [3,5,9]. Although previous studies showed that domestication selection was involved in such fitness impairment, they also observed that different environmental conditions (e.g. reduced fish density) significantly modulated the physiological acclimation to hatchery environment [4].\n\nEnvironmental stimuli are especially relevant during early embryonic development, which also correspond to a sensitive methylation reprogramming window in vertebrates [10,11]. It is therefore plausible that differences in rearing environment during early development may result in epigenetic modifications that could in turn impact on fitness. However, the only epigenetic study to date pertaining to captive rearing in salmonids and performed using methylation-sensitive amplified fragments (MSAP) failed to identify significant changes in methylation profile associated with hatchery rearing [12]\n\nHere, we used a higher resolution approach to compare the genome-wide pattern of methylation in hatchery-reared juvenile (smolt) Coho Salmon with that of their wild counterparts in two geographically distant rivers in British Columbia, Canada. Using a reduced representation bisulfite sequencing (RRBS) approach covering an average per individual of about 70 million cytosines in CpG context, we identified 100 methylated regions (DMRs) that differed in parallel between hatchery and natural origin salmon in both rivers. The total variance of epigenetic variation among individuals explained by river or origin and rearing environment in a RDA model was 16% (adj.R2=0.16), and both variables equally explained about 8% of the variance after controlling for each other. The gene ontology analysis revealed that regions with different methylation levels between hatchery and natural origin salmon showed enrichment for ion homeostasis, synaptic and neuromuscular regulation, immune and stress response, and control of locomotion functions. We further identified 15,044 SNPs that allowed detection of significant differences between either rivers or sexes. However, no effect of rearing environment was observed, confirming that hatchery and natural origin fish of a given river belong to the same panmictic population, as expected based on the hatchery programs applied in these rivers (see Supplementary experimental procedures). Moreover, neither a standard genome-scan approach nor a polygenic statistical framework allowed detection of selective effects within a single generation between hatchery and natural origin salmon. Therefore, this is the first study to demonstrate that parallel epigenetic modifications induced by hatchery rearing during early development may represent a potential explanatory mechanism for rapid change in fitness-related traits previously reported in salmonids.

genomics↗