A three-pronged approach that leans on Indigenous knowledge for northern fish monitoring and conservation.

Investigating whether changes within fish populations may result from harvesting requires a comprehensive approach, especially in more data-sparse northern regions. Our study took a three-pronged approach to investigate walleye population change by combining Indigenous knowledge (IK), phenotypic traits, and genomics. We thank Larson et al. (2020) for their critiques of our study; certainly, there are aspects of their critique that are warranted and merit further investigation. However, we argue that their critique is over-stated and misleading, primarily given that (a) one of three prongs of our research, IK, was dismissed in their assessment of our study's conclusions; (b) our Bayesian size-at-age modeling should help to mitigate sample size issues; (c) their re-analysis of our size-at-age data does not actually refute our results; (d) genomic changes that we observed are nascent; (e) the data file that Larson et al. (2020) used for their genomic re-analysis was not correct; and (f) criteria that Larson et al. (2020) use for their genomic re-analysis were not properly justified.

Size reductions and genomic changes within two generations in wild walleye populations: associated with harvest?

The extent and rate of harvest-induced genetic changes in natural populations may impact population productivity, recovery, and persistence. While there is substantial evidence for phenotypic changes in harvested fishes, knowledge of genetic change in the wild remains limited, as phenotypic and genetic data are seldom considered in tandem, and the number of generations needed for genetic changes to occur is not well understood. We quantified changes in size-at-age, sex-specific changes in body size, and genomic metrics in three harvested walleye (Sander vitreus) populations and a fourth reference population with low harvest levels over a 15-year period in Mistassini Lake, Quebec. We also collected Indigenous knowledge (IK) surrounding concerns about these populations over time. Using ~9,000 SNPs, genomic metrics included changes in population structure, neutral genomic diversity, effective population size, and signatures of selection. Indigenous knowledge revealed overall reductions in body size and number of fish caught. Smaller body size, a small reduction in size-at-age, nascent changes to population structure (population differentiation within one river and homogenization between two others), and signatures of selection between historical and contemporary samples reflected coupled phenotypic and genomic change in the three harvested populations in both sexes, while no change occurred in the reference population. Sex-specific analyses revealed differences in both body size and genomic metrics but were inconclusive about whether one sex was disproportionately affected. Although alternative explanations cannot be ruled out, our collective results are consistent with the hypothesis that genetic changes associated with harvesting may arise within 1-2.5 generations in long-lived wild fishes. This study thus demonstrates the need to investigate concerns about harvest-induced evolution quickly once they have been raised.

Population correlates of rapid captive-induced maladaptation in a wild fish.

Understanding the extent to which captivity generates maladaptation in wild species can inform species recovery programs and elucidate wild population responses to novel environmental change. Although rarely quantified, effective population size (N e ) and genetic diversity should influence the magnitude of plastic and genetic changes manifested in captivity that reduce wild fitness. Sexually dimorphic traits might also mediate consequences of captivity. To evaluate these relationships, we generated >600 full- and half-sibling families from nine wild brook trout populations, reared them for one generation under common, captive environmental conditions and contrasted several fitness-related traits in wild versus captive lines. We found substantial variation in lifetime success (lifetime survival and reproductive success) and life history traits among wild populations after just one captive generation (fourteen- and threefold ranges across populations, respectively). Populations with lower heterozygosity showed lower captive lifetime success, suggesting that captivity generates maladaptation within one generation. Greater male-biased mortality in captivity occurred in populations having disproportionately higher growth rates in males than females. Wild population N e and allelic diversity had little or no influence on captive trait expression and lifetime success. Our results have four conservation implications: (i) Trait values and lifetime success were highly variable across populations following one generation of captivity. (ii) Maladaptation induced by captive breeding might be particularly intense for the very populations practitioners are most interested in conserving, such as those with low heterozygosity. (iii) Maladaptive sex differences in captivity might be associated with population-dependent growth costs of reproduction. (iv) Heterozygosity can be a good indicator of short-term, intraspecific responses to novel environmental change.

Geo-referenced population-specific microsatellite data across American continents, the MacroPopGen Database.

Population genetic data from nuclear DNA has yet to be synthesized to allow broad scale comparisons of intraspecific diversity versus species diversity. The MacroPopGen database collates and geo-references vertebrate population genetic data across the Americas from 1,308 nuclear microsatellite DNA studies, 897 species, and 9,090 genetically distinct populations where genetic differentiation (FST) was measured. Caribbean populations were particularly distinguished from North, Central, and South American populations, in having higher differentiation (FST = 0.12 vs. 0.07-0.09) and lower mean numbers of alleles (MNA = 4.11 vs. 4.84-5.54). While mammalian populations had lower MNA (4.86) than anadromous fish, reptiles, amphibians, freshwater fish, and birds (5.34-7.81), mean heterozygosity was largely similar across groups (0.57-0.63). Mean FST was consistently lowest in anadromous fishes (0.06) and birds (0.05) relative to all other groups (0.09-0.11). Significant differences in Family/Genera variance among continental regions or taxonomic groups were also observed. MacroPopGen can be used in many future applications including latitudinal analyses, spatial analyses (e.g. central-margin), taxonomic comparisons, regional assessments of anthropogenic impacts on biodiversity, and conservation of wild populations.

Striking Phenotypic Variation yet Low Genetic Differentiation in Sympatric Lake Trout (Salvelinus namaycush).

The study of population differentiation in the context of ecological speciation is commonly assessed using populations with obvious discreteness. Fewer studies have examined diversifying populations with occasional adaptive variation and minor reproductive isolation, so factors impeding or facilitating the progress of early stage differentiation are less understood. We detected non-random genetic structuring in lake trout (Salvelinus namaycush) inhabiting a large, pristine, postglacial lake (Mistassini Lake, Canada), with up to five discernible genetic clusters having distinctions in body shape, size, colouration and head shape. However, genetic differentiation was low (FST = 0.017) and genetic clustering was largely incongruent between several population- and individual-based clustering approaches. Genotype- and phenotype-environment associations with spatial habitat, depth and fish community structure (competitors and prey) were either inconsistent or weak. Striking morphological variation was often more continuous within than among defined genetic clusters. Low genetic differentiation was a consequence of relatively high contemporary gene flow despite large effective population sizes, not migration-drift disequilibrium. Our results suggest a highly plastic propensity for occupying multiple habitat niches in lake trout and a low cost of morphological plasticity, which may constrain the speed and extent of adaptive divergence. We discuss how factors relating to niche conservatism in this species may also influence how plasticity affects adaptive divergence, even where ample ecological opportunity apparently exists.