A well-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification

Daniel J. Macqueen* (Corresponding Author), Ian A Johnston

*Corresponding author for this work

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Abstract

Whole genome duplication (WGD) is often considered to be mechanistically associated with species diversification. Such ideas have been anecdotally attached to a WGD at the stem of the salmonid fish family, but remain untested. Here, we characterized an extensive set of gene paralogues retained from the salmonid WGD, in species covering the major lineages (subfamilies Salmoninae, Thymallinae and Coregoninae). By combining the data in calibrated relaxed molecular clock analyses, we provide the first well-constrained and direct estimate for the timing of the salmonid WGD. Our results suggest that the event occurred no later in time than 88 Ma and that 40–50 Myr passed subsequently until the subfamilies diverged. We also recovered a Thymallinae–Coregoninae sister relationship with maximal support. Comparative phylogenetic tests demonstrated that salmonid diversification patterns are closely allied in time with the continuous climatic cooling that followed the Eocene–Oligocene transition, with the highest diversification rates coinciding with recent ice ages. Further tests revealed considerably higher speciation rates in lineages that evolved anadromy—the physiological capacity to migrate between fresh and seawater—than in sister groups that retained the ancestral state of freshwater residency. Anadromy, which probably evolved in response to climatic cooling, is an established catalyst of genetic isolation, particularly during environmental perturbations (for example, glaciation cycles). We thus conclude that climate-linked ecophysiological factors, rather than WGD, were the primary drivers of salmonid diversification.
Original languageEnglish
Article number20132881
Number of pages8
JournalProceedings of the Royal Society of London. B, Biological Sciences
Volume281
Issue number1778
Early online date7 Mar 2014
DOIs
Publication statusPublished - 7 Mar 2014

Bibliographical note

Acknowledgements
We are grateful to Prof. Colin Adams and Mr Stuart Wilson (University of Glasgow) for arranging whitefish sampling, and to Mr Neil Lincoln (Environment Agency) for providing grayling samples. Dr Dani Garcia and Dr Charles Paxton (University of St Andrews) assisted with sequencing experiments and sequence statistics, respectively. We thank Prof. Mike Ritchie, Prof. Richard Abbott and Prof. Malcolm White (University of St Andrews), as well as Prof. David Hazlerigg and Prof. Chris Secombes (University of Aberdeen), for comments on the manuscript. We acknowledge Prof. Mark Wilson (University of Alberta) for helpful email discussions on the salmonid fossil record. We thank Dr Rich FitzJohn (Macquarie University) for help with the BiSSE analysis. The study was much improved by the comments of anonymous reviewers, to whom we are individually very grateful.

Funding statement
The study was supported by the Marine Alliance for Science and Technology for Scotland (Scottish Funding Council grant no. HR09011).

Keywords

  • whole genome duplication
  • species diversification
  • salmonid fish
  • climate change
  • evolution
  • anadromy

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