Phylotranscriptomic Insights into the Diversification of Endothermic Thunnus Tunas
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Author(s)
Type
Journal Article
Abstract
Birds, mammals, and certain fishes, including tunas, opahs and lamnid sharks, are endothermic, conserving internally
generated, metabolic heat to maintain body or tissue temperatures above that of the environment. Bluefin tunas are
commercially important fishes worldwide, and some populations are threatened. They are renowned for their endothermy, maintaining elevated temperatures of the oxidative locomotor muscle, viscera, brain and eyes, and occupying cold, productive high-latitude waters. Less cold-tolerant tunas, such as yellowfin tuna, by contrast, remain in
warm-temperate to tropical waters year-round, reproducing more rapidly than most temperate bluefin tuna populations, providing resiliency in the face of large-scale industrial fisheries. Despite the importance of these traits to
not only fisheries but also habitat utilization and responses to climate change, little is known of the genetic processes
underlying the diversification of tunas. In collecting and analyzing sequence data across 29,556 genes, we found that
parallel selection on standing genetic variation is associated with the evolution of endothermy in bluefin tunas. This
includes two shared substitutions in genes encoding glycerol-3 phosphate dehydrogenase, an enzyme that contributes
to thermogenesis in bumblebees and mammals, as well as four genes involved in the Krebs cycle, oxidative phosphorylation, b-oxidation, and superoxide removal. Using phylogenetic techniques, we further illustrate that the eight
Thunnus species are genetically distinct, but found evidence of mitochondrial genome introgression across two
species. Phylogeny-based metrics highlight conservation needs for some of these species.
generated, metabolic heat to maintain body or tissue temperatures above that of the environment. Bluefin tunas are
commercially important fishes worldwide, and some populations are threatened. They are renowned for their endothermy, maintaining elevated temperatures of the oxidative locomotor muscle, viscera, brain and eyes, and occupying cold, productive high-latitude waters. Less cold-tolerant tunas, such as yellowfin tuna, by contrast, remain in
warm-temperate to tropical waters year-round, reproducing more rapidly than most temperate bluefin tuna populations, providing resiliency in the face of large-scale industrial fisheries. Despite the importance of these traits to
not only fisheries but also habitat utilization and responses to climate change, little is known of the genetic processes
underlying the diversification of tunas. In collecting and analyzing sequence data across 29,556 genes, we found that
parallel selection on standing genetic variation is associated with the evolution of endothermy in bluefin tunas. This
includes two shared substitutions in genes encoding glycerol-3 phosphate dehydrogenase, an enzyme that contributes
to thermogenesis in bumblebees and mammals, as well as four genes involved in the Krebs cycle, oxidative phosphorylation, b-oxidation, and superoxide removal. Using phylogenetic techniques, we further illustrate that the eight
Thunnus species are genetically distinct, but found evidence of mitochondrial genome introgression across two
species. Phylogeny-based metrics highlight conservation needs for some of these species.
Date Issued
2019-01-01
Date Acceptance
2018-10-01
Citation
Molecular Biology and Evolution, 2019, 36 (1), pp.84-96
ISSN
0737-4038
Publisher
Oxford University Press (OUP)
Start Page
84
End Page
96
Journal / Book Title
Molecular Biology and Evolution
Volume
36
Issue
1
Copyright Statement
The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/
licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is
properly cited.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/
licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is
properly cited.
License URL
Sponsor
Natural Environment Research Council (NERC)
The Leverhulme Trust
Identifier
http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000459327400008&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=1ba7043ffcc86c417c072aa74d649202
Grant Number
NE/M015742/1
RF-2016-373/2
Subjects
Science & Technology
Life Sciences & Biomedicine
Biochemistry & Molecular Biology
Evolutionary Biology
Genetics & Heredity
endothermy
thermogenesis
phylogenomics
RNA-sequencing
transcriptomics
introgression
positive selection
mitochondrial-nuclear discordance
BROWN ADIPOSE-TISSUE
PACIFIC BLUEFIN TUNA
PHYLOGENETIC ANALYSIS
GENE TREES
NUCLEAR INTROGRESSION
MUSCLE TEMPERATURES
CONCATENATED DATA
METABOLIC-RATE
BIGEYE TUNA
MITOCHONDRIAL
Publication Status
Published
Date Publish Online
2018-10-26