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 PLOS GENETICS

Sequence variation in the mtDNA control region of Arctic charr Salvelinus alpinus and Dolly Varden Salvelinus malma from 56 Siberian and North American populations was analysed to assess their phylogeographic relationships and the origins of sympatric forms. Phylogenetic trees confirm the integrity of phylogroups reported in previous mtDNA studies except that the Siberian group does not separate as a single cluster. Haplotype network analysis indicates the proximity of Siberian and Atlantic haplotypes. These are considered as one Eurasian group represented by the Atlantic, east Siberian (interior Siberia including Transbaikalia, Taimyr) and Eurosiberian (Finland, Spitsbergen, Taimyr) sub-groups. Salvelinus alpinus with presumably introgressed Bering group (malma) haplotypes were found along eastern Siberian coasts up to the Olenek Bay and the Lena Delta region, where they overlap with the Eurasian group and in the easternmost interior region. It is proposed that Siberia was colonized by S. alpinus in two stages: from the west by the Eurasian group and later from the east by the Bering group. The high diversity of Eurasian group haplotypes in Siberia indicates its earlier colonization by S. alpinus as compared with the European Alps. This colonization was rapid, proceeded from a diverse gene pool, and was followed by differential survival of ancestral mtDNA lineages in different basins and regions, and local mutational events in isolated populations. The results presented here support a northern origin of Transbaikalian S. alpinus, the dispersion of S. alpinus to the Lake Baikal Basin from the Lena Basin, segregation of S. alpinus between Lena tributaries and their restricted migration over the divides between sub-basins. These results also support sympatric origin of intralacustrine forms of S. alpinus.

Human-mediated translocations of species beyond their native ranges can enhance evolutionary processes in populations introduced to novel environments. We studied such processes in several generations of pink salmon Oncorhynchus gorbuscha introduced to the European North of Russia using a set of morphological and life-history traits as well as molecular genetic markers with different selective values: protein-coding loci, mtDNA, microsatellites, and MHC. The introduction of reproductively isolated pink salmon broodlines of odd and even years yielded different results. The odd-year broodline established self-reproducing local populations in many rivers of new range, but sustainable changes in external morphology, reproduction, and life-history, as well as the impoverishment of the gene pool occurred. Their successful colonisation of the new range resulted in specialisation manifested in the rapid directional shifts in some highly heritable phenotypic traits accompanied by increased homozygosity at molecular markers as a consequence of genetic drift and selective processes. The returns of transplanted pink salmon of even-year broodline decreased sharply already in the second generation, but there was no marked reduction of genetic diversity. Our data, as well as the analysis of the history of all pink salmon transplantations beyond the species range, demonstrate comparatively greater success of introduced odd-year broodline and permit to assume different adaptive plasticity of the even-and odd-year broodlines in pink salmon, what is most likely determined by differences in their evolutionary histories. Population genetic data suggest that the evenyear broodline probably diverged from the odd-year broodline relatively recently and, due to the founder effect, may have lost a part of its genetic variation with which adaptive plasticity potential is associated.

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