Convergence in form and function overcomes non-parallel evolutionary histories in a Holarctic fish

Abstract

Understanding the extent to which evolution is predictable under multifarious selection is a longstanding question in evolutionary biology. However, the interplay of stochastic and contingent factors influencing the extent of parallelism in nature is not well understood. To test the predictability of evolution, we studied a natural experiment on different organismal levels across lakes and evolutionary lineages of a freshwater salmonid fish, Arctic charr (Salvelinus alpinus). We identified significant phenotypic parallelism between Arctic charr ecotype pairs within a continuum of parallel evolution and highly parallel adaptive morphological traits. Variability in phenotypic predictability was explained by complex demographic histories, differing genomic backgrounds and genomic responses to selection, variable genetic associations with ecotype, and environmental variation. Remarkably, gene expression was highly similar across ecotype replicates, and explained the observed parallelism continuum. Our findings suggest that parallel evolution by non-parallel evolutionary routes is possible when the regulatory molecular phenotype compensates for divergent histories.