Substitutions in the Glycogenin-1 Gene Are Associated with the Evolution of Endothermy in Sharks and Tunas.
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 characterized by centralization 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 behavior. 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.
Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, UK.
Adam G
AG
Ciezarek
Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, UK Present address: Department of Animal and Plant Sciences, University of Sheffield, Sheffield, UK.
Luke T
LT
Dunning
Institute of Biological and Environmental Sciences, School of Biological Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen, Scotland, UK.
Catherine S
CS
Jones
Institute of Biological and Environmental Sciences, School of Biological Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen, Scotland, UK.
Leslie R
LR
Noble
Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, UK Present address: Department of Animal Behaviour, University of Bielefeld, Postfach 100131, Bielefeld, Germany.
Emily
E
Humble
Villa Comunale, Stazione Zoologica Anton Dohrn, Naples, Italy.
Sergio S
SS
Stefanni
Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, UK v.savolainen@imperial.ac.uk.
Vincent
V
Savolainen
D000818:Animals; D001831:Body Temperature / Q000235:genetics*; D019143:Evolution, Molecular; D029941:Fish Proteins / Q000235:genetics*; D005964:Glucosyltransferases / Q000235:genetics*; D006023:Glycoproteins / Q000235:genetics*; D018482:Muscle, Skeletal / Q000378:metabolism; D012641:Selection, Genetic; D012754:Sharks / Q000235:genetics / Q000502:physiology; D059467:Transcriptome; D014413:Tuna / Q000235:genetics / Q000502:physiology
D029941:Fish Proteins; D006023:Glycoproteins; C051887:glycogenin; D005964:Glucosyltransferases
endothermy; phylogenetics; positive selection; sharks; tuna