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Including environmental covariates clarifies the relationship between endangered Atlantic salmon (Salmo salar) abundance and environmental DNA
Morrison, Melissa K.; Lacoursière-Roussel, Anaïs; Wood, Zachary T.; Trudel, Marc; Gagné, Nellie; LeBlanc, Francis; Samways, Kurt; Kinnison, Michael T.; Pavey, Scott A. — 2023-06-07 <p><span id="161">Collecting environmental DNA (eDNA) as a nonlethal sampling approach has been valuable in detecting the presence/absence of many imperiled taxa; however, its application to indicate species abundance poses many challenges. A deeper understanding of eDNA dynamics in aquatic systems is required to better interpret the substantial variability often associated with eDNA samples. Our sampling design took advantage of natural variation in juvenile Atlantic salmon (</span><span id="162"><em>Salmo</em> <em>salar</em></span><span id="163">) distribution and abundance along 9 km of a single river in the Province of New Brunswick (Canada), covering different spatial and temporal scales to address the unknown seasonal impacts of environmental variables on the quantitative relationship between eDNA concentration and species abundance. First, we asked whether accounting for environmental variables strengthened the relationship between eDNA and salmon abundance by sampling eDNA during their spring seaward migration. Second, we asked how environmental variables affected eDNA dynamics during the summer as the parr abundance remained relatively constant. Spring eDNA samples were collected over a 6‐week period (12 times) near a rotary screw trap that captured approximately 18.6% of migrating smolts, whereas summer sampling occurred (i) at three distinct salmon habitats (9 times) and (ii) along the full 9 km (3 times). We modeled eDNA concentration as a product of fish abundance and environmental variables, demonstrating that (1) with inclusion of abundance and environmental covariates, eDNA was highly correlated with spring smolt abundance and (2) the relationships among environmental covariates and eDNA were affected by seasonal variation with relatively constant parr abundance in summer. Our findings underscore that with appropriate study design that accounts for seasonal environmental variation and life history phenology, eDNA salmon population assessments may have the potential to evaluate abundance fluctuations in spring and summer.</span></p>
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Data from: RAD-sequencing highlights polygenic discrimination of habitat ecotypes in the panmictic American eel (Anguilla rostrata)
Pavey, Scott A.; Gaudin, Jérémy; Normandeau, Eric; Dionne, Mélanie; Castonguay, Martin; Audet, Céline; Bernatchez, Louis — 2016-04-20 The two primary ways that species respond to heterogeneous environments is through local adaptation and phenotypic plasticity. The American eel (Anguilla rostrata) presents a paradox; despite inhabiting drastically different environments, the species is panmictic. Spawning takes place only in the southern Sargasso Sea in the Atlantic Ocean. Then, the planktonic larvae (leptocephali) disperse to rearing locations from Cuba to Greenland, and juveniles colonize either freshwater or brackish/saltwater habitats, where they spend 3–25 years before returning to the Sargasso Sea to spawn as a panmictic species. Depending on rearing habitat, individuals exhibit drastically different ecotypes. In particular, individuals rearing in freshwater tend to grow slowly and mature older and are more likely to be female in comparison to individuals that rear in brackish/saltwater. The hypothesis that phenotypic plasticity alone can account for all of the differences was not supported by three independent controlled experiments. Here, we present a genome-wide association study that demonstrates a polygenic basis that discriminates these habitat-specific ecotypes belonging to the same panmictic population. We found that 331 co-varying loci out of 42,424 initially considered were associated with the divergent ecotypes, allowing a reclassification of 89.6%. These 331 SNPs are associated with 101 genes that represent vascular and morphological development, calcium ion regulation, growth and transcription factors, and olfactory receptors. Our results are consistent with divergent natural selection of phenotypes and/or genotype-dependent habitat choice by individuals that results in these genetic differences between habitats, occurring every generation anew in this panmictic species.
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Data from: RAD-sequencing reveals within-generation polygenic selection in response to anthropogenic organic and metal contamination in North Atlantic Eels
Laporte, Martin; Pavey, Scott A.; Rougeux, Clément; Pierron, Fabien; Budzinski, Hélène; Lauzent, M.; Labadie, P.; Geneste, E.; Couture, P.; Baudrimont, M.; Bernatchez, L. — 2015-11-11 Measuring the effects of selection on the genome imposed by human-altered environment is currently a major goal in ecological genomics. Given the polygenic basis of most phenotypic traits, quantitative genetic theory predicts that selection is expected to cause subtle allelic changes among covarying loci rather than pronounced changes at few loci of large effects. The goal of this study was to test for the occurrence of polygenic selection in both North Atlantic eels (European Eel, Anguilla anguilla and American Eel, A. rostrata), using a method that searches for covariation among loci that would discriminate eels from “control” vs. “polluted” environments and be associated with specific contaminants acting as putative selective agents. RAD-seq libraries resulted in 23,659 and 14,755 filtered loci for the European and American Eels respectively. A total of 142 and 141 covarying markers discriminating European and American Eels from “control” vs. “polluted” sampling localities were obtained using the Random Forest algorithm. Distance-based redundancy analyses (db-RDAs) were used to assess the relationships between these covarying markers and concentration of 34 contaminants measured for each individual eel. PCB153, 4'4'DDE and selenium were associated with covarying markers for both species, thus pointing to these contaminants as major selective agents in contaminated sites . Gene enrichment analyses suggested that sterol regulation plays an important role in the differential survival of eels in “polluted” environment. This study illustrates the power of combining methods for detecting signals of polygenic selection and for associating variation of markers with putative selective agents in studies aiming at documenting the dynamics of selection at the genomic level, and particularly so in human altered environments.
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Data from: Microbiome investigation in the ecological speciation context of lake whitefish (Coregonus clupeaformis) using next-generation sequencing
Sevellec, Maelle; Pavey, Scott A.; Boutin, Sébastien; Filteau, Marie; Derome, Nicolas; Bernatchez, Louis — 2014-04-11 Few studies have applied NGS methods to investigate the microbiome of vertebrates in their natural environment and in freshwater fishes in particularly. Here, we used pyrosequencing of the 16S gene rRNA to (i) test for differences in kidney bacterial communities (i.e. microbiota) of dwarf and normal whitefish found as sympatric pairs, (ii) test the hypothesis of higher bacterial diversity in normal compared with dwarf whitefish and (iii) test for the occurrence of parallelism with the presence and composition of bacterial communities across species pairs inhabiting different lakes. The kidney microbiota of 253 dwarf and normal whitefish from five lakes was analysed combining a double-nested PCR approach with 454 pyrosequencing. Bacteria were detected in 52.6% of the analysed whitefish. There was no overall significant difference among lakes and forms, although the lake × form interaction was found significant. We identified 579 bacterial genera, which is substantially more than previous descriptions using less sensitive techniques of fish bacterial diversity in kidney, pathogenic or not. Ten of these genera contained eighteen pathogenic species. Differences in bacteria composition between whitefish forms were not parallel among lakes. In accordance with the higher diversity of prey types, normal whitefish kidney tissue consistently had a more diverse bacterial community and this pattern was parallel among lakes. These results add to building evidence from previous studies on this system that the adaptive divergence of dwarf, and normal whitefish has been driven by both parallel and nonparallel ecological conditions across lakes.
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Data from: Draft genome of the American eel (Anguilla rostrata)
Pavey, Scott A.; Laporte, Martin; Normandeau, Eric; Gaudin, Jérémy; Létourneau, Louis; Boisvert, Sébastien; Corbeil, Jacques; Audet, Céline; Bernatchez, Louis — 2016-10-26 Freshwater eels (Anguilla sp.) have large economic, cultural, ecological and aesthetic importance worldwide, but they suffered more than 90% decline in global stocks over the past few decades. Proper genetic resources, such as sequenced, assembled and annotated genomes, are essential to help plan sustainable recoveries by identifying physiological, biochemical and genetic mechanisms that caused the declines or that may lead to recoveries. Here, we present the first sequenced genome of the American Eel. This genome contained 305,043 contigs (N50 = 7,397) and 79,209 scaffolds (N50 = 86,641) for a total size of 1.41 Gb, which is in the middle of the range of previous estimations for this species. In addition, protein coding regions, including introns and flanking regions, are very well represented in the genome, as 95.2% of the 458 core eukaryotic genes and 98.8% of the 248 ultra-conserved subset were represented in the assembly. and a total of 24,564 genes were annotated for future functional genomics studies. We performed a candidate gene analysis to compare three genes among all three freshwater eel species and, congruent with the phylogenetic relationships, Japanese eel (A. japanica) exibited the most divergence. Overall, the sequenced genome presented in this study is a crucial addition to the presently available genetic tools to help guide future conservation efforts of Freshwater eels.
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Data from: Gene coexpression networks reveal key drivers of phenotypic divergence in lake whitefish
Filteau, Marie; Pavey, Scott A.; St-Cyr, Jérôme; Bernatchez, Louis — 2013-05-20 BACKGROUND: A functional understanding of processes involved in adaptive divergence is one of the awaiting opportunities afforded by high throughput transcriptomic technologies. Functional analysis of co-expressed genes has succeeded in the biomedical field in identifying key drivers of disease pathways. However, in ecology and evolutionary biology, functional interpretation of transcriptomic data is still limited. RESULTS: Here we used Weighted Gene Co-Expression Network Analysis (WGCNA) to identify modules of co-expressed genes in muscle and brain tissue of a lake whitefish backcross progeny. Modules were connected to gradients of known adaptive traits involved in the ecological speciation process between benthic and limnetic ecotypes. Key drivers, i.e. hub genes of functional modules related to reproduction, growth, and behavior were identified, and module preservation was assessed in natural populations. Using this approach, we identified modules of co-expressed genes involved in phenotypic divergence and their key drivers, and further identified a module part specifically rewired in the backcross progeny. CONCLUSIONS: Functional analysis of transcriptomic data can significantly contribute to the understanding of the mechanisms underlying ecological speciation. Our findings point to BMP and Calcium signaling as common pathways involved in coordinated evolution of trophic behavior, trophic morphology (gill rakers), and reproduction. Results also point to pathways implicating hemoglobins and constitutive stress response (HSP70) governing growth in lake whitefish.
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Atlantic Puffin (Fratercula arctica) single-nucleotide polymorphism (SNP) datasets
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Carvey, Quinn; Pavey, Scott A.; Diamond, Tony; Davoren, Gail K.; Lavoie, Raphael A.; Legard, Matthew; Robertson, Gregory J.; Runnells, Emily; Petalas, Christina; Major, Heather — 2024-02-20 Blood samples were collected from Atlantic Puffins breeding at five colonies in Atlantic Canada. DNA was extracted using a DNeasy Blood and Tissue DNA Kit from Qiagen. Triple digest genotype-by-sequencing (3D-GbS) library preparation was performed using three restriction enzymes (PstI/NsiI/MspI). Samples were sequenced on one lane using 150 bp, paired-end sequencing with an Illumina NovaSeq 6000. Data were assembled with Stacks v.2.6.1, see publication for full methodological details. Filtered SNP datasets used in genetic analyses are included here.
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Data from: Neutral and selective processes shape MHC gene diversity and expression in stocked brook charr populations (Salvelinus fontinalis)
Lamaze, Fabien C.; Pavey, Scott A.; Normandeau, Eric; Roy, Gabriel; Garant, Dany; Bernatchez, Louis — 2014-02-25 The capacity of an individual to battle infection is an important fitness determinant in wild vertebrate populations. The major histocompatibility complex (MHC) genes are crucial for a host’s adaptive immune system to detect pathogens. However, anthropogenic activities may disrupt natural cycles of co-evolution between hosts and pathogens. In this study we investigated the dynamic sequence and expression variation of host parasite interactions in brook charr (Salvelinus fontinalis) in a context of past human disturbance via population supplementation from domestic individuals. To do so, we developed a new method to examine selection shaping MHC diversity within and between populations and found a complex interplay between neutral and selective processes that varied among lakes that were investigated. We provided evidence for a lower introgression rate of domestic alleles and found that parasite infection increased with domestic genomic background of individuals. We also documented an association between individual MHC alleles and parasite taxa. Finally, longer cis regulatory minisatellites were positively correlated with MHC II down-regulation and domestic admixture, suggesting that inadvertent selection during domestication resulted in a lower immune response capacity, through a trade-off between growth and immunity, which explained the negative selection of domestic alleles at least under certain circumstances.
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Data from: Mapping phenotypic, expression and transmission ratio distortion QTL using RAD markers in the Lake Whitefish (Coregonus clupeaformis)
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Gagnaire, Pierre-Alexandre; Normandeau, Éric; Pavey, Scott; Bernatchez, Louis; Pavey, Scott A. — 2012-10-22 The evolution of reproductive isolation in an ecological context may involve multiple facets of species divergence on which divergent selection may operate. These include variation in quantitative phenotypic traits, regulation of gene expression, and differential transmission of particular allelic combinations. Thus, an integrative approach to the speciation process involves identifying the genetic basis of these traits, in order to understand how they are affected by divergent selection in nature and how they ultimately contribute to reproductive isolation. In the Lake Whitefish (Coregonus clupeaformis), dwarf and normal species pairs sympatrically occur in several North American postglacial lakes. The limnetic dwarf whitefish distinguishes from its normal benthic relative by numerous life history, behavioural, morphological and gene expression traits, in relation with the exploitation of distinct ecological niches. Here, we have applied the RAD-Sequencing method to a hybrid backcross family to reconstruct a high-density genetic linkage map and perform QTL mapping in the Lake Whitefish. The 3061 cM map encompassed 3438 segregating RAD markers distributed over 40 linkage groups, for an average resolution of 0.89 cM. We mapped phenotypic and expression QTL underlying ecologically important traits as well as transmission ratio distortion QTL, and identified genomic regions harbouring clusters of such QTL. A narrow genomic region strongly associated with sex determination was also evidenced. Positional and functional information revealed in this study will be useful in ongoing population genomic studies to illuminate our understanding of the genomic architecture of reproductive isolation between whitefish species pairs.

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(Author: Pavey, Scott A.)

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