Les N. Harris

Microsatellite and mtDNA analysis of lake trout, Salvelinus namaycush, from Great Bear Lake, Northwest Territories: impacts of historical and contemporary evolutionary forces on Arctic ecosystems

Resolving the genetic population structure of species inhabiting pristine, high latitude ecosystems can provide novel insights into the post-glacial, evolutionary processes shaping the distribution of contemporary genetic variation. In this study, we assayed genetic variation in lake trout (Salvelinus namaycush) from Great Bear Lake (GBL), NT and one population outside of this lake (Sandy Lake, NT) at 11 microsatellite loci and the mtDNA control region (d-loop). Overall, population subdivision was low, but significant (global FST θ = 0.025), and pairwise comparisons indicated that significance was heavily influenced by comparisons between GBL localities and Sandy Lake. Our data indicate that there is no obvious genetic structure among the various basins within GBL (global FST = 0.002) despite the large geographic distances between sampling areas. We found evidence of low levels of contemporary gene flow among arms within GBL, but not between Sandy Lake and GBL. Coalescent analyses suggested that some historical gene flow occurred among arms within GBL and between GBL and Sandy Lake. It appears, therefore, that contemporary (ongoing dispersal and gene flow) and historical (historical gene flow and large founding and present-day effective population sizes) factors contribute to the lack of neutral genetic structure in GBL. Overall, our results illustrate the importance of history (e.g., post-glacial colonization) and contemporary dispersal ecology in shaping genetic population structure of Arctic faunas and provide a better understanding of the evolutionary ecology of long-lived salmonids in pristine, interconnected habitats.

Geographic influences on fine-scale, hierarchical population structure in northern Canadian populations of anadromous Arctic Char (Salvelinus alpinus)

Assessments of fine-scale population structure in natural populations are important for understanding aspects of ecology, life history variation and evolutionary history and can provide novel insights into resource management. Although Arctic char, Salvelinus alpinus, represent one of the most culturally and commercially important salmonids in the Canadian Arctic, fine-scale assessments of genetic structure in northern populations of this species are rare. In this study, we assessed population structure in anadromous Arctic char from Cumberland Sound in Canada’s Nunavut territory using 18 microsatellite loci. Specifically, we aimed at identifying potential habitat and landscape/geographic features influencing genetic variation and population structure and resolving potential barriers to gene flow. Overall population structure was moderate (global FST and Jost’s D of 0.042 and 0.236 respectively) and significant among all sampling locations. Habitat and landscape/geographic features, with the exception of fluvial (shoreline) distance, appeared to have little influence on genetic variation and population structure. Bayesian clustering revealed a hierarchical model of population structure, in which the 14 sampling locations were nested within two distinct clusters corresponding to the north and south shores of Cumberland Sound. Both isolation-by-distance analysis and calculations of mean dispersal distance suggest dispersal and gene flow is highest among proximate locations. Finally, several putative barriers to gene flow were identified and one, a putative barrier separating north and south Cumberland Sound, was consistent with the hierarchical STRUCTURE results. Our results suggest that the current river-specific management of commercially harvested Arctic char is appropriate. Overall, we provide further insights into the evolution of genetic variation and population structure in iteroparous, Arctic salmonids.

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.

Genetic analysis of sympatric migratory ecotypes of Arctic charr Salvelinus alpinus: alternative mating tactics or reproductively isolated strategies?

Three populations of Arctic charr Salvelinus alpinus from southern Baffin Island were previously identified to display variable migratory phenotypes, with an anadromous component of the population and another remaining resident in fresh water. In this study, 14 microsatellite markers were used to help distinguish between two alternative hypotheses to explain the co-existence of the two ecotypes: that the two ecotypes originate from a single population and are the result of a conditional mating tactic or that the migratory ecotypes are reproductively isolated populations utilizing alternative migratory strategies. In two of the three replicate systems, F(ST) values between the resident and anadromous individuals were non-significant, while they were significant in a third sampling location. Bayesian clustering analysis implemented in structure, however, failed to identify any within-location clustering in all three sampling locations. It is concluded from these analyses that the life-history ecotypes are most likely conditional mating tactics, rather than reproductively isolated populations. Other evidence in favour of the alternative mating tactic hypothesis is briefly reviewed, and implications for management of those populations are discussed.

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 ...

Gene flow and effective population size in two life-history types of broad whitefish Coregonus nasus from the Canadian Arctic.

In this study, the magnitude and direction of gene flow and estimates of effective population sizes (N(e) ) were quantified among two life-history types (lacustrine and anadromous) of broad whitefish Coregonus nasus in the lower Mackenzie River system. The data suggest that dispersal and subsequent gene flow occurs between these groups, with the former appearing to be asymmetrical. Gene flow may potentially be directionally biased as well, a result attributed to source-sink population dynamics and the ongoing process of post-glacial colonization and contemporary range expansion. Additionally, average N(e) estimates were consistently lower for lacustrine populations of C. nasus although confidence intervals for both contemporary and historical estimates broadly overlapped. The lower average estimates of N(e) for lacustrine populations was suggested to be the result of more recent founding events following post-glacial dispersal. This study provides one of the first assessments of gene flow and N(e) in an Arctic coregonine, results that may be relevant to other freshwater and anadromous Arctic species persisting in systems near the periphery of their range.

Migratory Variation in Mackenzie River System Broad Whitefish: Insights from Otolith Strontium Distributions

Abstract There is growing recognition of the global importance of preserving biodiversity. While many organisms show immense variation in intraspecific biodiversity, for example in life history variation and migratory strategies among conspecific populations, accurate descriptions of such variation are lacking for the majority of contemporary species. One such example is the broad whitefish Coregonus nasus of the lower Mackenzie River system in Canadas Northwest Territories, where anadromous, lacustrine, and putative riverine populations are thought to exist. In this study we resolve migratory variation exhibited by lower Mackenzie River broad whitefish by employing otolith microchemistry and find that (1) anadromous, lacustrine, and riverine populations exist in this system, (2) a high degree of variability exists within anadromous broad whitefish (e.g., varying degrees of marine and estuarine use), and (3) lacustrine populations are not composed solely of resident fish as anadromous broad whitefish occ...

From top to bottom: Do Lake Trout diversify along a depth gradient in Great Bear Lake, NT, Canada?

Depth is usually considered the main driver of Lake Trout intraspecific diversity across lakes in North America. Given that Great Bear Lake is one of the largest and deepest freshwater systems in North America, we predicted that Lake Trout intraspecific diversity to be organized along a depth axis within this system. Thus, we investigated whether a deep-water morph of Lake Trout co-existed with four shallow-water morphs previously described in Great Bear Lake. Morphology, neutral genetic variation, isotopic niches, and life-history traits of Lake Trout across depths (0–150 m) were compared among morphs. Due to the propensity of Lake Trout with high levels of morphological diversity to occupy multiple habitat niches, a novel multivariate grouping method using a suite of composite variables was applied in addition to two other commonly used grouping methods to classify individuals. Depth alone did not explain Lake Trout diversity in Great Bear Lake; a distinct fifth deep-water morph was not found. Rather, Lake Trout diversity followed an ecological continuum, with some evidence for adaptation to local conditions in deep-water habitat. Overall, trout caught from deep-water showed low levels of genetic and phenotypic differentiation from shallow-water trout, and displayed higher lipid content (C:N ratio) and occupied a higher trophic level that suggested an potential increase of piscivory (including cannibalism) than the previously described four morphs. Why phenotypic divergence between shallow- and deep-water Lake Trout was low is unknown, especially when the potential for phenotypic variation should be high in deep and large Great Bear Lake. Given that variation in complexity of freshwater environments has dramatic consequences for divergence, variation in the complexity in Great Bear Lake (i.e., shallow being more complex than deep), may explain the observed dichotomy in the expression of intraspecific phenotypic diversity between shallow- vs. deep-water habitats. The ambiguity surrounding mechanisms driving divergence of Lake Trout in Great Bear Lake should be seen as reflective of the highly variable nature of ecological opportunity and divergent natural selection itself.

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