Intercontinental genomic parallelism in multiple adaptive radiations

Abstract

Parallelism, the evolution of similar traits in populations diversifying in similar conditions, provides good evidence of adaptation by natural selection. Many studies of parallelism have focused on comparisons of strongly different ecotypes or sharply contrasting environments, defined a priori, which could upwardly bias the apparent prevalence of parallelism. Here, we estimated genomic parallelism associated with individual components of environmental and phenotypic variation at an intercontinental scale across four adaptive radiations of the three-spined stickleback (Gasterosteus aculeatus), by associating genome-wide allele frequencies with continuous distributions of environmental and phenotypic variation. We found that genomic parallelism was well predicted by parallelism of phenotype-environment associations, suggesting that a quantitative characterization of phenotypes and environments can provide a good prediction of expected genomic parallelism. Further, we examined the explanatory power of genetic, phenotypic, and environmental similarity in predicting parallelism. We found that parallelism tended to be greater for geographically proximate, genetically similar radiations, highlighting the significant contingency of standing variation in the early stages of adaptive radiations, before new mutations accumulate. However, we also demonstrate that distance within multivariate environmental space predicts parallelism, after correction for genetic distance. This study thus demonstrates the relative influences of environment, phenotype and genetic contingency on repeatable signatures of adaptation in the genome.

Parallelism in eco-morphology and gene expression despite variable evolutionary and genomic backgrounds in a Holarctic fish

“…Evidence from theory and empirical studies suggests that the extent of genomic parallelism is impacted by factors such as genetic co-ancestry and shared genetic variation [60], demographic history [13], and similarity in selection pressures [52]. Indeed, the higher parallelism of ecotype-associated SNPs within lineages compared to across lineages in these Arctic charr replicates likely reflects the role of genetic co-ancestry and shared adaptive genetic variation in genetic parallelism, in line with observations in other systems [60,61].…”

“…For example, we found benthivorous-planktivorous ecotype pairs from Dughaill in Scotland and Kamkanda in Transbaikalia were highly parallel (θ P = 24.4˚; ΔL P = 0.0152). In fact, phenotypic trajectories for replicated Arctic charr ecotype pairs ( Fig 2B) were overall more parallel than those reported for global lake-stream sticklebacks [12,52]. Together, these results suggest that repeated natural selection can lead to phenotypic parallelism in both single phenotypic traits and overall eco-morphology, even across evolutionary and geographically distinct lineages that have been separated for more than 60,000 years.…”

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][34][35], whereby consistencies in the multidimensional fitness landscape channel adaptation along conserved paths. Conversely, inconsistencies may offer up alternative routes to fitness peaks.…”

Highly replicated evolution of parapatric ecotypes

“…Other systems providing clear evidence for parallel evolution include Lake Victoria cichlids 28 and alpine and montane Heliosperma pusillum ecotypes 22 . Also, an obvious case of 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 29 ). However, in other systems where gene flow is moderate between We must keep in mind that identifying the genetic basis of parallel trait evolution often provides unambiguous evidence for parallel evolution of ecotypes.…”