Abstract
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.
Highlights
The degree to which the pathways of evolution are predictable, under complex natural conditions, remains one of the greatest questions in evolutionary biology [1,2]
It is known that plasticity plays an important role in the divergence of Arctic charr [46], we found that ecotype-associated expression in white muscle of wild-caught individuals was in part genetically determined
In contrast to the genomic patterns, we found gene expression divergence to be highly parallel between replicated ecotype pairs both within and across evolutionary lineages (Fig 6A and 6B) We speculate that differential gene expression might facilitate parallel phenotypic evolution despite variation in genetic parallelism in these replicate divergences of Arctic charr, as has been suggested in Littorina snails [63] and Australian groundsel [64]
Summary
The degree to which the pathways of evolution are predictable, under complex natural conditions, remains one of the greatest questions in evolutionary biology [1,2]. Extensive variation in the magnitude and direction of evolutionary trajectories has been observed in some classic examples of ‘parallel evolution’ [7,10,11,12]. Stochastic factors such as differences in the local environment, gene flow, and selection regimes, or contingencies such as genomic background, demographic history, and the genetic architecture of adaptive traits, can lead to departures from phenotypic parallelism and non-parallelism at the genomic level [6,7,13]. It is critical to understand the evolutionary routes leading to replicated ecological divergence in a range of independent systems [15] and to disentangle the impact of various contingent and stochastic factors on parallel evolution
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