Jacobs, A. et al. (2020) Parallelism in eco-morphology and gene expression despite variable evolutionary and genomic backgrounds in a Holarctic fish. PLoS Genetics, 16(4), e1008658. (doi: 10.1371/journal.pgen.1008658) (PMID:32302300) (PMCID:PMC7164584)
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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.
Item Type: | Articles |
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Status: | Published |
Refereed: | Yes |
Glasgow Author(s) Enlighten ID: | Carruthers, Madeleine and Jacobs, Mr Arne and Elmer, Professor Kathryn and Adams, Professor Colin and Yurchenko, Dr Andrey |
Creator Roles: | Elmer, K.Conceptualization, Data curation, Funding acquisition, Investigation, Project administration, Resources, Supervision, Writing – original draft, Writing – review and editing Adams, C.Conceptualization, Funding acquisition, Investigation, Project administration, Resources, Supervision, Writing – review and editing Jacobs, A.Conceptualization, Data curation, Formal analysis, Investigation, Project administration, Resources, Visualization, Writing – original draft, Writing – review and editing Yurchenko, A.Data curation, Formal analysis, Investigation, Supervision, Writing – review and editing Carruthers, M.Data curation, Formal analysis, Funding acquisition, Investigation, Resources, Writing – review and editing |
Authors: | Jacobs, A., Carruthers, M., Yurchenko, A., Gordeeva, N. V., Alekseyev, S. S., Hooker, O., Leong, J. S., Minkley, D. R., Rondeau, E. B., Koop, B. F., Adams, C., and Elmer, K. R. |
College/School: | College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine |
Journal Name: | PLoS Genetics |
Publisher: | Public Library of Science |
ISSN: | 1553-7390 |
ISSN (Online): | 1553-7404 |
Published Online: | 17 April 2020 |
Copyright Holders: | Copyright © 2020 Jacobs et al. |
First Published: | First published in PLoS Genetics 16(4)e1008658 |
Publisher Policy: | Reproduced under a Creative Commons Licence |
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