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

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

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

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 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.

Keywords

Fish Proteins, 570, 330, QH301 Biology, endothermy, sharks, Sharks/genetics, Body Temperature, Evolution, Molecular, QH301, Glucosyltransferases/genetics, Tuna/genetics, 0603 Evolutionary Biology, positive selection, Animals, Fish Proteins/genetics, Selection, Genetic, Muscle, Skeletal, Glycoproteins, phylogenetics., 0604 Genetics, Muscle, Skeletal/metabolism, Tuna, Glycoproteins/genetics, phylogenetics, Glucosyltransferases, tuna, Biotechnology and Biological Sciences Research Council (BBSRC), Body Temperature/genetics, Sharks, Transcriptome, Developmental Biology, Research Article

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    influence
    This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
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    impulse
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selected citations
These citations are derived from selected sources.
This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Citations provided by BIP!
popularity
This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
BIP!Popularity provided by BIP!
influence
This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Influence provided by BIP!
impulse
This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
BIP!Impulse provided by BIP!
13
Top 10%
Average
Average
Green
gold