Substitutions in the Glycogenin-1 Gene Are Associated with the Evolution of Endothermy in Sharks and Tunas

Adam G. Ciezarek, Luke T. Dunning, Catherine S. Jones, Leslie R. Noble, Emily Humble, Sergio S. Stefanni, Vincent Savolainen

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Abstract

Despite 400-450 million years of independent evolution, a strong phenotypic convergence has occurred between two groups of fish: tunas and lamnid sharks. This convergence is characterised by centralisation of red muscle, a distinctive swimming style (stiffened body powered through tail movements) and elevated body temperature (endothermy). Furthermore, both groups demonstrate elevated white muscle metabolic capacities. All these traits are unusual in fish and more likely evolved to support their fast-swimming, pelagic, predatory behaviour. Here we tested the hypothesis that their convergent evolution was driven by selection on a set of metabolic genes. We sequenced white muscle transcriptomes of six tuna, one mackerel and three shark species, and supplemented this data set with previously published RNA-seq data. Using 26 species in total, (including 7,032 tuna genes plus 1,719 shark genes), we constructed phylogenetic trees and carried out maximum-likelihood analyses of gene selection. We inferred several genes relating to metabolism to be under selection. We also found that the same one gene, glycogenin-1, evolved under positive selection independently in tunas and lamnid sharks, providing evidence of convergent selective pressures at gene level possibly underlying shared physiology.

Original languageEnglish
Pages (from-to)3011-3021
Number of pages11
JournalGenome biology and evolution
Volume8
Issue number9
Early online date10 Sep 2016
DOIs
Publication statusPublished - Sep 2016

Keywords

  • tuna
  • sharks
  • endothermy
  • positive selection
  • phylogenetics

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    Ciezarek, A. G., Dunning, L. T., Jones, C. S., Noble, L. R., Humble, E., Stefanni, S. S., & Savolainen, V. (2016). Substitutions in the Glycogenin-1 Gene Are Associated with the Evolution of Endothermy in Sharks and Tunas. Genome biology and evolution, 8(9), 3011-3021. https://doi.org/10.1093/gbe/evw211