Intercontinental genomic parallelism in multiple three-spined stickleback adaptive radiations

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.

Drainage-structuring of ancestral variation and a common functional pathway shape limited genomic convergence in natural high- and low-predation guppies

“…This may result in the re-use of genes with minimal constraint and minimal effects on other aspects of fitness, as suggested for MC1R in pigmentation across vertebrates [ 32 ]. Alternatively, similarity of environments within multivariate space can predict genetic convergence [ 33 – 35 ], whereby consistencies in the multidimensional fitness landscape channel adaptation along conserved paths. Conversely, inconsistencies may offer up alternative routes to fitness peaks.…”

“…Conversely, inconsistencies may offer up alternative routes to fitness peaks. This combination of pleiotropy and differences among fitness landscapes may also explain why genetic convergence can vary for the same traits in the same species in global comparisons, for example in comparisons of Pacific-derived vs Atlantic-derived freshwater stickleback [ 35 – 37 ].…”

Highly replicated evolution of parapatric ecotypes

“…Other systems providing evidence for parallel evolution include Lake Victoria cichlids (Meier et al 2017) and alpine and montane Heliosperma pusillum ecotypes (Trucchi et al 2017). Also, an obvious case showing multiple origins is when parallel evolution occurs between geographically distant populations where gene flow could not have obscured the phylogenetic signal and demographic history of populations (e.g., threespine stickleback populations that colonized freshwater environments on separate continents; Magalhaes et al 2020). However, in other systems, where gene flow is moderate between ecotypes (Rougemont et al 2015;Le Moan et al 2016;Rougeux et al 2017;Herman et al 2018;Rougeux et al 2019), it remains unclear to what extent gene flow contributed to the signal of parallel evolution.…”

Population structure limits parallel evolution

“…Parallel evolution not only requires access to the same pool of SGV (Barrett & Schluter 2008;Schluter & Conte 2009), but also parallelism of selection optima across the distribution range, which cannot be taken for granted (Bolnick et al 2018;Magalhaes et al 2020;Stuart et al 2017). Thus, lower parallelism in selection optima across freshwater habitats could also explain the lower degree of parallelism in nine-than three-spined sticklebacks.…”