Jean-Sébastien Moore

Conservation genomics of anadromous Atlantic salmon across its North American range: outlier loci identify the same patterns of population structure as neutral loci

Anadromous Atlantic salmon (Salmo salar) is a species of major conservation and management concern in North America, where population abundance has been declining over the past 30 years. Effective conservation actions require the delineation of conservation units to appropriately reflect the spatial scale of intraspecific variation and local adaptation. Towards this goal, we used the most comprehensive genetic and genomic database for Atlantic salmon to date, covering the entire North American range of the species. The database included microsatellite data from 9142 individuals from 149 sampling locations and data from a medium‐density SNP array providing genotypes for >3000 SNPs for 50 sampling locations. We used neutral and putatively selected loci to integrate adaptive information in the definition of conservation units. Bayesian clustering with the microsatellite data set and with neutral SNPs identified regional groupings largely consistent with previously published regional assessments. The use of outlier SNPs did not result in major differences in the regional groupings, suggesting that neutral markers can reflect the geographic scale of local adaptation despite not being under selection. We also performed assignment tests to compare power obtained from microsatellites, neutral SNPs and outlier SNPs. Using SNP data substantially improved power compared to microsatellites, and an assignment success of 97% to the population of origin and of 100% to the region of origin was achieved when all SNP loci were used. Using outlier SNPs only resulted in minor improvements to assignment success to the population of origin but improved regional assignment. We discuss the implications of these new genetic resources for the conservation and management of Atlantic salmon in North America.

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.

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.

Genetic Stock Structure of Anadromous Arctic Char in Canada’s Central Arctic: Potential Implications for the Management of Canada’s Largest Arctic Char Commercial Fishery

AbstractThe Arctic Char Salvelinus alpinus is widely considered the most important subsistence fish species in the Canadian Arctic. Throughout the species’ range, commercial fisheries for Arctic Char also exist, the management of which primarily follows river-specific harvest strategies. Such an approach, however, may not be appropriate if the management unit or stock does not accurately reflect a demographically independent population or if mixtures of populations are being harvested. We assayed microsatellite DNA variation among 744 Arctic Char from the Cambridge Bay region, Nunavut, where the largest commercial fishery for the species exists, in order to identify the most appropriate spatial scale at which these stocks should be managed. Our sampling design specifically mirrored that of the commercial fishery in order to describe patterns of genetic structure and genetic variation within and among the harvested component. We also included Arctic Char from more geographically distant sampling locations ...

Genetic and morphological support for possible sympatric origin of fish from subterranean habitats

Two blind Iran cave barbs, Garra typhlops and Garra lorestanensis, exist in sympatry in a single subterranean habitat, raising the hypothesis that they may represent a case of sympatric speciation following a colonization event. Their different mental disc forms have prompted some authors to propose the alternative hypothesis of two separate colonization events. In this study, we analysed a genome-wide panel of 11,257 SNPs genotyped by means of genotyping-by-sequencing combined with mitochondrial cytochrome c oxidase sub-unit I sequence data, field observations and morphological traits to test these two hypotheses. Field data suggest some degree of ecological divergence despite some possible niche overlap such that hybridization is possible. According to both nuclear and mtDNA data, the cave barb species are monophyletic with close phylogenetic relationships with Garra gymnothorax from the Karun-Dez and Karkheh river basins. The historical demography analysis revealed that a model of Isolation-with-Migration (IM) best fitted the data, therefore better supporting a scenario of sympatric origin than that of allopatric isolation followed by secondary contact. Overall, our results offer stronger support to the hypothesis that speciation in the subterranean habitat could have occurred in sympatry following a colonization event from the Karun-Dez-Karkheh basins in the Zagros Mountains of Iran.

Premature alarm on the impacts of climate change on Arctic Char in Lake Hazen

A recent paper by Lehnherr et al. 1 reported on a long-term study of the ecological impacts of climate change in the world’s largest high Arctic lake: Lake Hazen on Canada’s Ellesmere Island. The paper made a convincing case that climate change has had a dramatic and significant impact on the watershed of this important freshwater ecosystem. Some of these changes have clearly impacted the ecology of Lake Hazen. We disagree, however, with the conclusion that such ecological changes have resulted in a significant decline in the condition of Arctic Char (Salvelinus alpinus) from the lake based on the presented data. It is critical to examine the evidence for changes in the condition of Arctic Char given the importance of this species to communities throughout Canada’s Arctic as a valued food resource and because changes to condition could impact its management. Evidence for the impact of climate change on Arctic Char was presented in the form of a time-series (1981–2014; N= 13) of Fulton’s condition factor (Fig. 1), a widely used index of the wellbeing or robustness (i.e., mass relative to length) of individuals or populations of fish2 (for criticisms of the use of condition indices see refs. 3,4). The authors concluded that there was a significant decline in the condition factor of Arctic Char during these years as a result of climate-mediated changes in this ecosystem. We argue, however, that the statistical analysis used to assess the significance of that trend is problematic. We reanalyzed the presented data, which was graciously made available by the authors, using the same analysis as described in the paper. Here, we highlight three issues with the authors’ approach. First, the authors reported a significant quadratic regression model (F2, 1133= 8.47, p= 0.0002 in our analysis), whereas the quadratic term itself was not significant (type 3 F1, 1133= 0.1659, p= 0.684). Second, and more importantly, each individual measurement was treated by Lehnherr et al.1 as an independent data point in the analysis, artificially inflating the reported significance (a problem further accentuated by the unequal sample sizes among years). In the current data set, observations from the same year are likely to be more similar than observations from different years, violating the assumption of independent errors of multiple regression. This aspect of the data should have been treated with an alternative approach such as including a random effect of year or using the annual mean condition factor to test the hypothesis of a decline across years. For instance, the quadratic regression model working on the annual mean condition index is no longer significant (adjusted R2= 0.0075; F1, 10= 1.045; p= 0.387) and neither is a linear regression (adj. R2= 0.047; F1, 11= 1.597; p= 0.233). Our final concern regards the very weak effect size of year. Specifically, there is a weak variation of the mean of Fulton’s condition factor across years (Fig. 1). Even after removing the quadratic term, the slope of the linear regression conducted on either the annual means of condition factor or on the individual fish is −0.002. Such a modest decline across years suggests that this change is not biologically significant, potentially due to greater within-year variation in the condition factor than among years. In fact, when fitting a linear mixed model to the entire data set (N= 1136) and treating the year as a random effect, we observe higher within-year variability (σresidual= 0.116, 95% CI: [0.111, 0.121]) than the variability among years (σyear= 0.032, 95% CI: [0.018, 0.057]). Therefore, even if statistical significance had been observed (which we contend it was not), such a weak effect of year is likely an example of a statistically significant result where the effect size is not biologically significant5, 6. There are valid reasons to be concerned about the fate of Arctic Char in a rapidly changing Arctic7–9. The few longterm datasets available from the Canadian Arctic, however, do not suggest declines in abundance or body condition linked to climate change (e.g., refs. 10, 11). In fact, some studies even suggest a positive effect of an increased summer ice-free period on the condition of anadromous stocks12 (note however that the individuals studied in Lake Hazen are not anadromous). We conclude that the available evidence does not currently support the conclusion of a decline in condition DOI: 10.1038/s41467-018-06479-5 OPEN

Let's talk about sex: A rigorous statistical framework to assign the sex of individuals from reduced-representation sequencing data

Molecular markers have been used to identify the sex of sampled individuals for several decades, but the time‐consuming development phase prevented their application in many systems. Recently, a growing number of papers have applied reduced‐representation sequencing (RRS) protocols to the identification of sex‐specific markers without the use of test crosses or prior genomic information. While such an approach has great advantages in terms of versatility and ease of use, the “shotgun sequencing” nature of RRS data sets leads to a high amount of missing data, which results in statistical challenges to the confident assignment of sex to individuals. In this issue of Molecular Ecology Resources, Stovall et al. (Molecular Ecology Resources, 18, 2018) provide a statistical framework to answer two questions: (1) how many individuals of one sex only must possess a genotype for this locus to be considered significantly sex‐specific? and (2) How many sex‐specific loci must an individual of unknown sex possess (in a given data set) to be confidently assigned a sex? The statistical pipeline introduced, and applied to samples of New Zealand fur seal (Arctocephalus forsteri) to identify 90 sex‐specific loci, should be broadly applicable to a large number of species and constitutes a nice addition to the molecular ecology toolkit in the genomics era.

Demographic and genetic approaches to study dispersal in wild animal populations: A methodological review

Dispersal is a central process in ecology and evolution. At the individual level, the three stages of the dispersal process (i.e., emigration, transience and immigration) are affected by complex interactions between phenotypes and environmental factors. Condition‐ and context‐dependent dispersal have far‐reaching consequences, both for the demography and the genetic structuring of natural populations and for adaptive processes. From an applied point of view, dispersal also deeply affects the spatial dynamics of populations and their ability to respond to land‐use changes, habitat degradation and climate change. For these reasons, dispersal has received considerable attention from ecologists and evolutionary biologists. Demographic and genetic methods allow quantifying non‐effective (i.e., followed or not by a successful reproduction) and effective (i.e., with a successful reproduction) dispersal and to investigate how individual and environmental factors affect the different stages of the dispersal process. Over the past decade, demographic and genetic methods designed to quantify dispersal have rapidly evolved but interactions between researchers from the two fields are limited. We here review recent developments in both demographic and genetic methods to study dispersal in wild animal populations. We present their strengths and limits, as well as their applicability depending on study objectives and population characteristics. We propose a unified framework allowing researchers to combine methods and select the more suitable tools to address a broad range of important topics about the ecology and evolution of dispersal and its consequences on animal population dynamics and genetics.

Comparison of coded-wire tagging with parentage-based tagging and genetic stock identification in a large-scale coho salmon fisheries application in British Columbia, Canada

Wild Pacific salmon, including Coho salmon Onchorynchus kisutch, have been supplemented with hatchery propagation for over 50 years in support of increased ocean harvest and conservation of threatened populations. In Canada, the Wild Salmon Policy for Pacific salmon was established with the goal of maintaining and restoring healthy and diverse Pacific salmon populations, making conservation of wild salmon and their habitats the highest priority for resource management decision‐making. A new approach to the assessment and management of wild coho salmon, and the associated hatchery production and fishery management is needed. Implementation of parentage‐based tagging (PBT) may overcome problems associated with coded‐wire tag‐based (CWT) assessment and management of coho salmon fisheries, providing at a minimum information equivalent to that derived from the CWT program. PBT and genetic stock identification (GSI) were used to identify coho salmon sampled in fisheries (8,006 individuals) and escapements (1,692 individuals) in British Columbia to specific conservation units (CU), populations, and broodyears. Individuals were genotyped at 304 single nucleotide polymorphisms (SNPs) via direct sequencing of amplicons. Very high accuracy of assignment to population (100%) via PBT for 543 jack (age 2) assigned to correct age and collection location and 265 coded‐wire tag (CWT, age 3) coho salmon assigned to correct age and release location was observed, with a 40,774—individual, 267—population baseline available for assignment. Coho salmon from un‐CWTed enhanced populations contributed 65% of the catch in southern recreational fisheries in 2017. Application of a PBT‐GSI system of identification to individuals in 2017 fisheries and escapements provided high‐resolution estimates of stock composition, catch, and exploitation rate by CU or population, providing an alternate and more effective method in the assessment and management of Canadian‐origin coho salmon relative to CWTs, and an opportunity for a genetic‐based system to replace the current CWT system for coho salmon assessment.

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.