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

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)

[img]
Preview
Text
209794.pdf - Published Version
Available under License Creative Commons Attribution.

3MB

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
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Elmer, Dr Kathryn and Yurchenko, Dr Andrey and Carruthers, Ms Madeleine and Jacobs, Mr Arne and Adams, Professor Colin
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 > Institute of Biodiversity Animal Health and Comparative Medicine
Journal Name:PLoS Genetics
Publisher:Public Library of Science
ISSN:1553-7390
ISSN (Online):1553-7404
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

University Staff: Request a correction | Enlighten Editors: Update this record

Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
190536Integrated Health - Polyomics and Systems Biomedicine (ISSF Bid)Anna DominiczakWellcome Trust (WELLCOTR)097821/Z/11/ZInstitute of Cardiovascular & Medical Sciences
167342GEN ECOL ADAPT: Adaptation genomics of trophic polymorphismKathryn ElmerEuropean Commission (EC)Elmer, Dr KathrynInstitute of Biodiversity, Animal Health and Comparative Medicine
171939Environmental and genomic drivers of diversity in Scottish fishes of high natural heritage valueKathryn ElmerThe Carnegie Trust for the Universities of Scotland (CARNEGTR)70287Institute of Biodiversity, Animal Health and Comparative Medicine
190659BBSRC Doctoral Training Partnership 2012Jeremy MottramBiotechnology and Biological Sciences Research Council (BBSRC)BB/J013854/1MVLS - Graduate School
166084IBIS (SCENE 2)Colin AdamsEuropean Commission (EC)Adams, Prof ColinInstitute of Biodiversity, Animal Health and Comparative Medicine