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Integrative genomic phylogeography reveals signs of mitonuclear incompatibility in a natural hybrid goby population
Hybridization between divergent lineages generates new allelic combinations. One mechanism that can hinder the formation of hybrid populations is mitonuclear incompatibility, that is, dysfunctional interactions between proteins encoded in the nuclear and mitochondrial genomes (mitogenomes) of diverg...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley and Sons Inc.
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7898790/ https://www.ncbi.nlm.nih.gov/pubmed/33165944 http://dx.doi.org/10.1111/evo.14120 |
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author | Hirase, Shotaro Tezuka, Ayumi Nagano, Atsushi J. Sato, Mana Hosoya, Sho Kikuchi, Kiyoshi Iwasaki, Wataru |
author_facet | Hirase, Shotaro Tezuka, Ayumi Nagano, Atsushi J. Sato, Mana Hosoya, Sho Kikuchi, Kiyoshi Iwasaki, Wataru |
author_sort | Hirase, Shotaro |
collection | PubMed |
description | Hybridization between divergent lineages generates new allelic combinations. One mechanism that can hinder the formation of hybrid populations is mitonuclear incompatibility, that is, dysfunctional interactions between proteins encoded in the nuclear and mitochondrial genomes (mitogenomes) of diverged lineages. Theoretically, selective pressure due to mitonuclear incompatibility can affect genotypes in a hybrid population in which nuclear genomes and mitogenomes from divergent lineages admix. To directly and thoroughly observe this key process, we de novo sequenced the 747‐Mb genome of the coastal goby, Chaenogobius annularis, and investigated its integrative genomic phylogeographics using RNA‐sequencing, RAD‐sequencing, genome resequencing, whole mitogenome sequencing, amplicon sequencing, and small RNA‐sequencing. Chaenogobius annularis populations have been geographically separated into Pacific Ocean (PO) and Sea of Japan (SJ) lineages by past isolation events around the Japanese archipelago. Despite the divergence history and potential mitonuclear incompatibility between these lineages, the mitogenomes of the PO and SJ lineages have coexisted for generations in a hybrid population on the Sanriku Coast. Our analyses revealed accumulation of nonsynonymous substitutions in the PO‐lineage mitogenomes, including two convergent substitutions, as well as signals of mitochondrial lineage‐specific selection on mitochondria‐related nuclear genes. Finally, our data implied that a microRNA gene was involved in resolving mitonuclear incompatibility. Our integrative genomic phylogeographic approach revealed that mitonuclear incompatibility can affect genome evolution in a natural hybrid population. |
format | Online Article Text |
id | pubmed-7898790 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | John Wiley and Sons Inc. |
record_format | MEDLINE/PubMed |
spelling | pubmed-78987902021-03-03 Integrative genomic phylogeography reveals signs of mitonuclear incompatibility in a natural hybrid goby population Hirase, Shotaro Tezuka, Ayumi Nagano, Atsushi J. Sato, Mana Hosoya, Sho Kikuchi, Kiyoshi Iwasaki, Wataru Evolution Original Article Hybridization between divergent lineages generates new allelic combinations. One mechanism that can hinder the formation of hybrid populations is mitonuclear incompatibility, that is, dysfunctional interactions between proteins encoded in the nuclear and mitochondrial genomes (mitogenomes) of diverged lineages. Theoretically, selective pressure due to mitonuclear incompatibility can affect genotypes in a hybrid population in which nuclear genomes and mitogenomes from divergent lineages admix. To directly and thoroughly observe this key process, we de novo sequenced the 747‐Mb genome of the coastal goby, Chaenogobius annularis, and investigated its integrative genomic phylogeographics using RNA‐sequencing, RAD‐sequencing, genome resequencing, whole mitogenome sequencing, amplicon sequencing, and small RNA‐sequencing. Chaenogobius annularis populations have been geographically separated into Pacific Ocean (PO) and Sea of Japan (SJ) lineages by past isolation events around the Japanese archipelago. Despite the divergence history and potential mitonuclear incompatibility between these lineages, the mitogenomes of the PO and SJ lineages have coexisted for generations in a hybrid population on the Sanriku Coast. Our analyses revealed accumulation of nonsynonymous substitutions in the PO‐lineage mitogenomes, including two convergent substitutions, as well as signals of mitochondrial lineage‐specific selection on mitochondria‐related nuclear genes. Finally, our data implied that a microRNA gene was involved in resolving mitonuclear incompatibility. Our integrative genomic phylogeographic approach revealed that mitonuclear incompatibility can affect genome evolution in a natural hybrid population. John Wiley and Sons Inc. 2020-11-30 2021-01 /pmc/articles/PMC7898790/ /pubmed/33165944 http://dx.doi.org/10.1111/evo.14120 Text en © 2020 The Authors. Evolution published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. |
spellingShingle | Original Article Hirase, Shotaro Tezuka, Ayumi Nagano, Atsushi J. Sato, Mana Hosoya, Sho Kikuchi, Kiyoshi Iwasaki, Wataru Integrative genomic phylogeography reveals signs of mitonuclear incompatibility in a natural hybrid goby population |
title | Integrative genomic phylogeography reveals signs of mitonuclear incompatibility in a natural hybrid goby population |
title_full | Integrative genomic phylogeography reveals signs of mitonuclear incompatibility in a natural hybrid goby population |
title_fullStr | Integrative genomic phylogeography reveals signs of mitonuclear incompatibility in a natural hybrid goby population |
title_full_unstemmed | Integrative genomic phylogeography reveals signs of mitonuclear incompatibility in a natural hybrid goby population |
title_short | Integrative genomic phylogeography reveals signs of mitonuclear incompatibility in a natural hybrid goby population |
title_sort | integrative genomic phylogeography reveals signs of mitonuclear incompatibility in a natural hybrid goby population |
topic | Original Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7898790/ https://www.ncbi.nlm.nih.gov/pubmed/33165944 http://dx.doi.org/10.1111/evo.14120 |
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