David C. Hardie

Parallel adaptive evolution of Atlantic cod on both sides of the Atlantic Ocean in response to temperature

Despite the enormous economic and ecological importance of marine organisms, the spatial scales of adaptation and biocomplexity remain largely unknown. Yet, the preservation of local stocks that possess adaptive diversity is critical to the long-term maintenance of productive stable fisheries and ecosystems. Here, we document genomic evidence of range-wide adaptive differentiation in a broadcast spawning marine fish, Atlantic cod (Gadus morhua), using a genome survey of single nucleotide polymorphisms. Of 1641 gene-associated polymorphisms examined, 70 (4.2%) tested positive for signatures of selection using a Bayesian approach. We identify a subset of these loci (n = 40) for which allele frequencies show parallel temperature-associated clines (p < 0.001, r2 = 0.89) in the eastern and western north Atlantic. Temperature associations were robust to the statistical removal of geographic distance or latitude effects, and contrasted ‘neutral’ loci, which displayed no temperature association. Allele frequencies at temperature-associated loci were significantly correlated, spanned three linkage groups and several were successfully annotated supporting the involvement of multiple independent genes. Our results are consistent with the evolution and/or selective sweep of multiple genes in response to ocean temperature, and support the possibility of a new conservation paradigm for non-model marine organisms based on genomic approaches to resolving functional and adaptive diversity.

Evolutionary ecology at the extremes of species’ ranges

The nature of species at the extremes of their ranges impinges fundamentally on diverse biological issues, including species’ range dynamics, population variability, speciation and conservation biology. We review the literature concerning genetic and ecological variation at species’ range edges, and discuss historical and contemporary forces that may generate observed trends, as well as their current and future implications. We discuss literature which shows how environmental, ecological and evolutionary factors act to limit species’ ranges, and how these factors impose selection for adaptation or dispersal in peripheral populations exposed to extreme and stochastic biotic and abiotic stressors. When conditions are sufficiently harsh such that local extinction is certain, peripheral populations may represent temporary offshoots from stable core populations. However, in cases where peripheral populations persist at the range edge under divergent or extreme conditions, biologically significant differences c...

Genomic islands of divergence and their consequences for the resolution of spatial structure in an exploited marine fish

As populations diverge, genomic regions associated with adaptation display elevated differentiation. These genomic islands of adaptive divergence can inform conservation efforts in exploited species, by refining the delineation of management units, and providing genomic tools for more precise and effective population monitoring and the successful assignment of individuals and products. We explored heterogeneity in genomic divergence and its impact on the resolution of spatial population structure in exploited populations of Atlantic cod, Gadus morhua, using genome wide expressed sequence derived single nucleotide polymorphisms in 466 individuals sampled across the range. Outlier tests identified elevated divergence at 5.2% of SNPs, consistent with directional selection in one‐third of linkage groups. Genomic regions of elevated divergence ranged in size from a single position to several cM. Structuring at neutral loci was associated with geographic features, whereas outlier SNPs revealed genetic discontinuities in both the eastern and western Atlantic. This fine‐scale geographic differentiation enhanced assignment to region of origin, and through the identification of adaptive diversity, fundamentally changes how these populations should be conserved. This work demonstrates the utility of genome scans for adaptive divergence in the delineation of stock structure, the traceability of individuals and products, and ultimately a role for population genomics in fisheries conservation.

Evaluating SNP ascertainment bias and its impact on population assignment in Atlantic cod, Gadus morhua.

The increasing use of single nucleotide polymorphisms (SNPs) in studies of nonmodel organisms accentuates the need to evaluate the influence of ascertainment bias on accurate ecological or evolutionary inference. Using a panel of 1641 expressed sequence tag–derived SNPs developed for northwest Atlantic cod (Gadus morhua), we examined the influence of ascertainment bias and its potential impact on assignment of individuals to populations ranging widely in origin. We hypothesized that reductions in assignment success would be associated with lower diversity in geographical regions outside the location of ascertainment. Individuals were genotyped from 13 locations spanning much of the contemporary range of Atlantic cod. Diversity, measured as average sample heterozygosity and number of polymorphic loci, declined (c. 30%) from the western (He = 0.36) to eastern (He = 0.25) Atlantic, consistent with a signal of ascertainment bias. Assignment success was examined separately for pools of loci representing differing degrees of reductions in diversity. SNPs displaying the largest declines in diversity produced the most accurate assignment in the ascertainment region (c. 83%) and the lowest levels of correct assignment outside the ascertainment region (c. 31%). Interestingly, several isolated locations showed no effect of assignment bias and consistently displayed 100% correct assignment. Contrary to expectations, estimates of accurate assignment range‐wide using all loci displayed remarkable similarity despite reductions in diversity. Our results support the use of large SNP panels in assignment studies of high geneflow marine species. However, our evidence of significant reductions in assignment success using some pools of loci suggests that ascertainment bias may influence assignment results and should be evaluated in large‐scale assignment studies.

Evolutionary and ecological feedbacks of the survival cost of reproduction

Arguably the most fundamental of trade‐offs in life‐history evolution is the increase in natural mortality resulting from sexual maturity and reproduction. Despite its central importance, this increase in mortality, a survival cost, garners surprisingly little attention in fish and fisheries modeling studies. We undertook an exploratory analysis to evaluate the consequences of this omission for life‐history projections. To this end, we developed a simulation approach that integrates quantitative genetics into the ecological dynamics of a fish population and parameterized the model for Atlantic cod (Gadus morhua, L.). When compared to simulations in which the mortality of immature and mature individuals is equal, the inclusion of a survival cost results in larger asymptotic body size, older age at maturity, and larger size at maturity. We also find that measures of population productivity (spawning stock biomass, recruits‐per‐spawner) are overestimated if the survival cost is excluded. This sensitivity of key metrics of population growth rate and reproductive capacity to the magnitude of the survival cost of reproduction underscores the need to explicitly account for this trade‐off in projections of fish population responses to natural and anthropogenic environmental change, including fisheries.

Morphometric and genetic analyses of two sympatric morphs of Arctic char (Salvelinus alpinus) in the Canadian High Arctic

Multivariate morphometric analyses were used to examine variation in head, body, and fin shape between two sympatric morphotypes of Arctic char (Salvelinus alpinus (L., 1758)) from Lake Hazen, Ellesmere Island, Nunavut, Canada. Population structure of the Lake Hazen Arctic char was examined using five microsatellite loci. The “small” morph was found to have a larger (primarily deeper) head, larger and more elongate fins, and a deeper lateral profile than the “large” morph. The morphs also differed in allometric growth patterns. The large and small morphs do not appear to represent genetically distinct populations. The head morphology of the Lake Hazen small and large morphs exhibited similarities to benthic and pelagic morphs (respectively) from other lakes. We hypothesize that the large morph may be adapted to high-efficiency swimming and that the small morph may be adapted to low-efficiency, high-acceleration swimming. Such functional trade-offs are not uncommon among fish specializing in dispersed or m...

The isolation of Atlantic cod, Gadus morhua (Gadiformes), populations in Northern Meromictic lakes—A recurrent arctic phenomenon

Although it has previously been considered to be a rare phenomenon, this paper provides evidence of eight occurrences of Atlantic cod in northern coastal saline lakes in Arctic Canada, Greenland, Norway, and Russia. Historic and current habitat features that are necessary for Atlantic cod to colonize and persist in Arctic meromictic lakes are discussed. Data analyses confirm that the persistence of Atlantic cod in Arctic lakes is a recurrent phenomenon, and these populations represent an important component of intraspecific biodiversity.