Abstract
Parallelism, the evolution of similar traits in populations diversifying in similar conditions, provides strong evidence of adaptation by natural selection. Many studies of parallelism focus on comparisons of different ecotypes or contrasting environments, defined a priori, which could upwardly bias the apparent prevalence of parallelism. Here, we estimated genomic parallelism associated with components of environmental and phenotypic variation at an intercontinental scale across four freshwater adaptive radiations (Alaska, British Columbia, Iceland, Scotland) of the three-spined stickleback (Gasterosteus aculeatus). We combined large-scale biological sampling and phenotyping with RAD-sequencing data from 73 freshwater lake populations and four marine ones (1,380 fish) to associate genome-wide allele frequencies with continuous distributions of environmental and phenotypic variation. Our three main findings demonstrate: 1) quantitative variation in phenotypes and environments can predict genomic parallelism; 2) genomic parallelism at the early stages of adaptive radiations, even at large geographic scales, is founded on standing variation; and 3) similar environments are a better predictor of genome-wide parallelism than similar phenotypes. Overall, this study validates the importance and predictive power of major phenotypic and environmental factors likely to influence the emergence of common patterns of genomic divergence, providing a clearer picture than analyses of dichotomous phenotypes and environments.
Highlights
Adaptive radiations are rapid branchings on the tree of life, associated with adaptation to distinct ecological niches [1]
We first quantified environmental and phenotypic parallelism across four adaptive radiations to provide an indication of how much genomic parallelism associated with environments and phenotypes to expect
A Principal Component Analysis (PCA) on all seven variables across all lakes revealed that the first axis of environmental variance (EnvPC1) separated lakes along a predominant gradient of phenotype interactions in all (pH), with additional minor loadings reflecting Ca and Gyro (Fig. 2a; Supplementary Table 3)
Summary
Adaptive radiations are rapid branchings on the tree of life, associated with adaptation to distinct ecological niches [1]. Similar environments are typically assumed on the basis of comparable, typically morphological or life history, phenotypes, concealing the role of individual components of environmental variation in driving parallelism This compromises our ability to understand adaptation, much of which is likely to be broadly physiological. A major barrier to combining genotype, environment and phenotype has been achieving the necessary biological replication across all three to make broad inferences and shift from description to hypothesis testing This has rarely been applied (but see 20–22), and it remains to be shown whether signals of parallelism obtained from continuous measures are comparable to those from ecotypes and previous studies. We quantify parallelism between phenotypes, environments, and genomic loci under
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