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

Understanding the extent to which ecological divergence is repeatable is essential for predicting responses of biodiversity to environmental change. Here we test the predictability of evolution, from genotype to phenotype, by studying parallel evolution in a salmonid fish, Arctic charr (Salvelinus alpinus), across eleven replicate sympatric ecotype pairs (benthivorous-planktivorous and planktivorous-piscivorous) and two evolutionary lineages. We found considerable variability in eco-morphological divergence, with several traits related to foraging (eye diameter, pectoral fin length) being highly parallel even across lineages. This suggests repeated and predictable adaptation to environment. Consistent with ancestral genetic variation, hundreds of loci were associated with ecotype divergence within lineages of which eight were shared across lineages. This shared genetic variation was maintained despite variation in evolutionary histories, ranging from postglacial divergence in sympatry (ca. 10-15kya) to pre-glacial divergence (ca. 20-40kya) with postglacial secondary contact. Transcriptome-wide gene expression (44,102 genes) was highly parallel across replicates, involved biological processes characteristic of ecotype morphology and physiology, and revealed parallelism at the level of regulatory networks. This expression divergence was not only plastic but in part genetically controlled by parallel cis-eQTL. Lastly, we found that the magnitude of phenotypic divergence was largely correlated with the genetic differentiation and gene expression divergence. In contrast, the direction of phenotypic change was mostly determined by the interplay of adaptive genetic variation, gene expression, and ecosystem size. Ecosystem size further explained variation in putatively adaptive, ecotype-associated genomic patterns within and across lineages, highlighting the role of environmental variation and stochasticity in parallel evolution. Together, our findings demonstrate the parallel evolution of eco-morphology and gene expression within and across evolutionary lineages, which is controlled by the interplay of environmental stochasticity and evolutionary contingencies, largely overcoming variable evolutionary histories and genomic backgrounds. Author summary: A renowned natural model system for adaptive evolution is the repeated and rapid divergence of fishes into different sympatric trophic and morphological specialists, known as ecotypes. The drivers and constraints of these repeated divergences are complex and not well understood but it is often observed that postglacial fishes diverge in predictable patterns. Here we use a framework of parallel (or convergent) evolution to test the predictability of divergence in the most variable northern freshwater fish, the Arctic charr. Using a hierarchy of replication—from individuals to divergent phylogeographic lineages—we detect parallel evolution of foraging-related traits despite variation in genomic backgrounds and evolutionary histories. The level of phenotypic parallelism can be explained by the complex interplay of environment, shared genetic variation, and variability in gene expression. While phenotypic divergence may be determined and/or constraint by genetic and molecular divergence, the direction of change is largely determined by molecular parallelism and shared adaptive genetic variation. These are in turn associated with environmental similarity, reflected as ecosystem size. We suggest that gene expression facilitates parallel ecotype evolution, but that the extent of parallelism is further influenced by the level of shared genetic variation and ecological opportunity. [ABSTRACT FROM AUTHOR]