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Adaptive Patterns of Mitogenome Evolution Are Associated with the Loss of Shell Scutes in Turtles

The mitochondrial genome encodes several protein components of the oxidative phosphorylation (OXPHOS) pathway and is critical for aerobic respiration. These proteins have evolved adaptively in many taxa, but linking molecular-level patterns with higher-level attributes (e.g., morphology, physiology)...

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Autores principales: Escalona, Tibisay, Weadick, Cameron J, Antunes, Agostinho
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6298445/
https://www.ncbi.nlm.nih.gov/pubmed/28591857
http://dx.doi.org/10.1093/molbev/msx167
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author Escalona, Tibisay
Weadick, Cameron J
Antunes, Agostinho
author_facet Escalona, Tibisay
Weadick, Cameron J
Antunes, Agostinho
author_sort Escalona, Tibisay
collection PubMed
description The mitochondrial genome encodes several protein components of the oxidative phosphorylation (OXPHOS) pathway and is critical for aerobic respiration. These proteins have evolved adaptively in many taxa, but linking molecular-level patterns with higher-level attributes (e.g., morphology, physiology) remains a challenge. Turtles are a promising system for exploring mitochondrial genome evolution as different species face distinct respiratory challenges and employ multiple strategies for ensuring efficient respiration. One prominent adaptation to a highly aquatic lifestyle in turtles is the secondary loss of keratenized shell scutes (i.e., soft-shells), which is associated with enhanced swimming ability and, in some species, cutaneous respiration. We used codon models to examine patterns of selection on mitochondrial protein-coding genes along the three turtle lineages that independently evolved soft-shells. We found strong evidence for positive selection along the branches leading to the pig-nosed turtle (Carettochelys insculpta) and the softshells clade (Trionychidae), but only weak evidence for the leatherback (Dermochelys coriacea) branch. Positively selected sites were found to be particularly prevalent in OXPHOS Complex I proteins, especially subunit ND2, along both positively selected lineages, consistent with convergent adaptive evolution. Structural analysis showed that many of the identified sites are within key regions or near residues involved in proton transport, indicating that positive selection may have precipitated substantial changes in mitochondrial function. Overall, our study provides evidence that physiological challenges associated with adaptation to a highly aquatic lifestyle have shaped the evolution of the turtle mitochondrial genome in a lineage-specific manner.
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spelling pubmed-62984452018-12-21 Adaptive Patterns of Mitogenome Evolution Are Associated with the Loss of Shell Scutes in Turtles Escalona, Tibisay Weadick, Cameron J Antunes, Agostinho Mol Biol Evol Discoveries The mitochondrial genome encodes several protein components of the oxidative phosphorylation (OXPHOS) pathway and is critical for aerobic respiration. These proteins have evolved adaptively in many taxa, but linking molecular-level patterns with higher-level attributes (e.g., morphology, physiology) remains a challenge. Turtles are a promising system for exploring mitochondrial genome evolution as different species face distinct respiratory challenges and employ multiple strategies for ensuring efficient respiration. One prominent adaptation to a highly aquatic lifestyle in turtles is the secondary loss of keratenized shell scutes (i.e., soft-shells), which is associated with enhanced swimming ability and, in some species, cutaneous respiration. We used codon models to examine patterns of selection on mitochondrial protein-coding genes along the three turtle lineages that independently evolved soft-shells. We found strong evidence for positive selection along the branches leading to the pig-nosed turtle (Carettochelys insculpta) and the softshells clade (Trionychidae), but only weak evidence for the leatherback (Dermochelys coriacea) branch. Positively selected sites were found to be particularly prevalent in OXPHOS Complex I proteins, especially subunit ND2, along both positively selected lineages, consistent with convergent adaptive evolution. Structural analysis showed that many of the identified sites are within key regions or near residues involved in proton transport, indicating that positive selection may have precipitated substantial changes in mitochondrial function. Overall, our study provides evidence that physiological challenges associated with adaptation to a highly aquatic lifestyle have shaped the evolution of the turtle mitochondrial genome in a lineage-specific manner. Oxford University Press 2017-10 2017-06-06 /pmc/articles/PMC6298445/ /pubmed/28591857 http://dx.doi.org/10.1093/molbev/msx167 Text en © The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Escalona, Tibisay
Weadick, Cameron J
Antunes, Agostinho
Adaptive Patterns of Mitogenome Evolution Are Associated with the Loss of Shell Scutes in Turtles
title Adaptive Patterns of Mitogenome Evolution Are Associated with the Loss of Shell Scutes in Turtles
title_full Adaptive Patterns of Mitogenome Evolution Are Associated with the Loss of Shell Scutes in Turtles
title_fullStr Adaptive Patterns of Mitogenome Evolution Are Associated with the Loss of Shell Scutes in Turtles
title_full_unstemmed Adaptive Patterns of Mitogenome Evolution Are Associated with the Loss of Shell Scutes in Turtles
title_short Adaptive Patterns of Mitogenome Evolution Are Associated with the Loss of Shell Scutes in Turtles
title_sort adaptive patterns of mitogenome evolution are associated with the loss of shell scutes in turtles
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6298445/
https://www.ncbi.nlm.nih.gov/pubmed/28591857
http://dx.doi.org/10.1093/molbev/msx167
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