Genetic diversity is related to climatic variation and vulnerability in threatened bull trout

Abstract

Understanding how climatic variation influences ecological and evolutionary processes is crucial for informed conservation decision-making. Nevertheless, few studies have measured how climatic variation influences genetic diversity within populations or how genetic diversity is distributed across space relative to future climatic stress. Here, we tested whether patterns of genetic diversity (allelic richness) were related to climatic variation and habitat features in 130 bull trout (Salvelinus confluentus) populations from 24 watersheds (i.e., ~4-7th order river subbasins) across the Columbia River Basin, USA. We then determined whether bull trout genetic diversity was related to climate vulnerability at the watershed scale, which we quantified on the basis of exposure to future climatic conditions (projected scenarios for the 2040s) and existing habitat complexity. We found a strong gradient in genetic diversity in bull trout populations across the Columbia River Basin, where populations located in the most upstream headwater areas had the greatest genetic diversity. After accounting for spatial patterns with linear mixed models, allelic richness in bull trout populations was positively related to habitat patch size and complexity, and negatively related to maximum summer temperature and the frequency of winter flooding. These relationships strongly suggest that climatic variation influences evolutionary processes in this threatened species and that genetic diversity will likely decrease due to future climate change. Vulnerability at a watershed scale was negatively correlated with average genetic diversity (r = -0.77; P < 0.001); watersheds containing populations with lower average genetic diversity generally had the lowest habitat complexity, warmest stream temperatures, and greatest frequency of winter flooding. Together, these findings have important conservation implications for bull trout and other imperiled species. Genetic diversity is already depressed where climatic vulnerability is highest; it will likely erode further in the very places where diversity may be most needed for future persistence.

Identifying environmental correlates of intraspecific genetic variation

“…For a standard panel of 10-15 loci, in open populations (for example, populations with migration and/or admixture, as for Murray cod), HL should also be more correlated with genome-wide homozygosity and inbreeding coefficients than are other common individual-based measures: internal relatedness and the uncorrected proportion of homozygous loci (Aparicio et al, 2006). Our panel of loci is comparable to other studies that have found associations between intraspecific genetic variation and environment (for example, Faulks et al, 2011;Kovach et al, 2015).…”

“…By integrating information about evolutionary and demographic processes, the distribution of genetic variation across a species' range can reveal critical insights about the viability of populations that is not necessarily represented in species occurrence or abundance patterns (Thomassen et al, 2010;Kovach et al, 2015). Understanding the distribution of intraspecific genetic variation and how it relates to environmental factors can assist better allocation of conservation resources and more robust predictions about species responses to environmental change (Frankel, 1974;Moritz, 2002;Vandergast et al, 2008;Scoble and Lowe, 2010;Thomassen et al, 2010;Sgrò et al, 2011;Gotelli and StantonGeddes, 2015).…”

“…Understanding the distribution of intraspecific genetic variation and how it relates to environmental factors can assist better allocation of conservation resources and more robust predictions about species responses to environmental change (Frankel, 1974;Moritz, 2002;Vandergast et al, 2008;Scoble and Lowe, 2010;Thomassen et al, 2010;Sgrò et al, 2011;Gotelli and StantonGeddes, 2015). Although many studies have explored links between environmental factors and species' occurrence or abundance patterns (Elith and Leathwick, 2009), few studies have explicitly and rigorously quantified associations between the environment and levels of intraspecific genetic variation across species' ranges (that is, with individual-or site-based measures of the amount of genetic variation as the response variable) (but see Thomassen et al, 2010;Kovach et al, 2015). Methods based on individual-or site-based measures of genetic variation (that is, amount of genetic diversity) are distinguished here from related methods based on population structure and/ or patterns of genetic differentiation (for example, Foll and Gaggiotti, 2006;Jay et al, 2012;Manel and Holderegger, 2013;Wang and Bradburd, 2014;Fitzpatrick and Keller, 2015).…”

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“…Estimates of variance in allele frequency among locales (e.g., quantified using F ST or G′ ST ) provide a measure of β-genetic diversity among populations or collection locations. These estimates of genetic diversity can be used as response variables to assess how landscape features and disturbance influence persistence of aquatic species (e.g., Kovach et al 2015). Genetic data can also be used to estimate traditional ecological metrics (population size, movement, dispersal, etc.…”

“…Climate change can effectively isolate populations by changing thermal or hydrologic regimes in different regions of rivers used by fish during different seasons and by different ontogenetic stages. Given overwhelming evidence for climate change and the likelihood that the scope of climate effects to fish populations will continue to expand, genetic data and analyses would help fisheries managers anticipate and mitigate these impacts (Landguth et al 2014;Kovach et al 2015). Genetic data will inform fisheries managers of population response to cryptic thermal barriers that decrease connectivity (i.e., reducing gene flow and thereby increasing genetic β-diversity, while also reducing effective population size and genetic α-diversity) and potentially identify the locations of these barriers to allow for management action.…”