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

Autoři: Arne Jacobs aff001;  Madeleine Carruthers aff001;  Andrey Yurchenko aff001;  Natalia V. Gordeeva aff002;  Sergey S. Alekseyev aff003;  Oliver Hooker aff001;  Jong S. Leong aff006;  David R. Minkley aff006;  Eric B. Rondeau aff006;  Ben F. Koop aff006;  Colin E. Adams aff001;  Kathryn R. Elmer aff001
Působiště autorů: Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, United Kingdom aff001;  Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, Russia aff002;  Koltzov Institute of Developmental Biology, Russian Academy of Sciences, Moscow, Russia aff003;  Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia aff004;  Scottish Centre for Ecology and the Natural Environment, University of Glasgow, Rowardennan, Loch Lomond, Glasgow, United Kingdom aff005;  Biology/Centre for Biomedical Research, University of Victoria, British Columbia, Canada aff006
Vyšlo v časopise: Parallelism in eco-morphology and gene expression despite variable evolutionary and genomic backgrounds in a Holarctic fish. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008658
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008658


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.

Klíčová slova:

Evolutionary genetics – Gene expression – Genetic loci – Genetic polymorphism – Genome evolution – Lakes – Phenotypes – Parallel evolution


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