Selection Increases Mitonuclear DNA Discordance but Reconciles Incompatibility in African Cattle

Mitochondrial function relies on the coordinated interactions between genes in the mitochondrial DNA and nuclear genomes. Imperfect interactions following mitonuclear incompatibility may lead to reduced fitness. Mitochondrial DNA introgressions across species and populations are common and well documented. Various strategies may be expected to reconcile mitonuclear incompatibility in hybrids or admixed individuals. African admixed cattle (Bos taurus × B. indicus) show sex-biased admixture, with taurine (B. taurus) mitochondrial DNA and a nuclear genome predominantly of humped zebu (B. indicus). Here, we leveraged local ancestry inference approaches to identify the ancestry and distribution patterns of nuclear functional genes associated with the mitochondrial oxidative phosphorylation process in the genomes of African admixed cattle. We show that most of the nuclear genes involved in mitonuclear interactions are under selection and of humped zebu ancestry. Variations in mitochondrial DNA copy number may have contributed to the recovery of optimal mitochondrial function following admixture with the regulation of gene expression, alleviating or nullifying mitochondrial dysfunction. Interestingly, some nuclear mitochondrial genes with enrichment in taurine ancestry may have originated from ancient African aurochs (B. primigenius africanus) introgression. They may have contributed to the local adaptation of African cattle to pathogen burdens. Our study provides further support and new evidence showing that the successful settlement of cattle across the continent was a complex mechanism involving adaptive introgression, mitochondrial DNA copy number variation, regulation of gene expression, and selection of ancestral mitochondria-related genes.

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Publication Details

Journal
Molecular Biology and Evolution
Published
2025-02-01
DOI
https://doi.org/10.1093/molbev/msaf039
Citations
6
Primary Topic
Animal Genetics and Reproduction
Type
article
Field-Weighted Citation Impact
10.90

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article

Selection Increases Mitonuclear DNA Discordance but Reconciles Incompatibility in African Cattle

Adeniyi C. Adeola, Olivier Hanotte, Min‐Sheng Peng, Joram M. Mwacharo et al.
6 citations
Molecular Biology and Evolution
Animal Genetics and Reproduction
10.90
article

Selection Increases Mitonuclear DNA Discordance but Reconciles Incompatibility in African Cattle

Adeniyi C. Adeola, Olivier Hanotte, Min‐Sheng Peng, Joram M. Mwacharo, George Msalya, Lisheng Liu, Jun Wang, Chuzhao Lei, Wenfa Lu, Xian Shi, Ningbo Chen, Sumaya Kambal, Zheng‐Fei Cai, Yán Li, Ya‐Ping Zhang, Cheng Ma, Qiwen Yang, Mingmin Xu, Han Jianlin
article en
6 citations

Abstract

Mitochondrial function relies on the coordinated interactions between genes in the mitochondrial DNA and nuclear genomes. Imperfect interactions following mitonuclear incompatibility may lead to reduced fitness. Mitochondrial DNA introgressions across species and populations are common and well documented. Various strategies may be expected to reconcile mitonuclear incompatibility in hybrids or admixed individuals. African admixed cattle (Bos taurus × B. indicus) show sex-biased admixture, with taurine (B. taurus) mitochondrial DNA and a nuclear genome predominantly of humped zebu (B. indicus). Here, we leveraged local ancestry inference approaches to identify the ancestry and distribution patterns of nuclear functional genes associated with the mitochondrial oxidative phosphorylation process in the genomes of African admixed cattle. We show that most of the nuclear genes involved in mitonuclear interactions are under selection and of humped zebu ancestry. Variations in mitochondrial DNA copy number may have contributed to the recovery of optimal mitochondrial function following admixture with the regulation of gene expression, alleviating or nullifying mitochondrial dysfunction. Interestingly, some nuclear mitochondrial genes with enrichment in taurine ancestry may have originated from ancient African aurochs (B. primigenius africanus) introgression. They may have contributed to the local adaptation of African cattle to pathogen burdens. Our study provides further support and new evidence showing that the successful settlement of cattle across the continent was a complex mechanism involving adaptive introgression, mitochondrial DNA copy number variation, regulation of gene expression, and selection of ancestral mitochondria-related genes.

Molecular Biology and EvolutionVol. 42(2)
Uppsala University (SE), Roslin Institute (GB), University of Nottingham (GB), University of Khartoum (SD), Kunming Institute of Zoology (CN), Yunnan University (CN), International Center for Agricultural Research in the Dry Areas (LB), Chinese Academy of Sciences (CN), National University (SD), Department of Animal Health (VN), Jilin Agricultural University (CN), University of Chinese Academy of Sciences (CN), International Livestock Research Institute (KE), Sokoine University of Agriculture (TZ), Northwest A&F University (CN), Bayero University Kano (NG)
National Natural Science Foundation of China, Chinese Academy of Sciences, Chinese Academy of Agricultural Sciences, Consortium of International Agricultural Research Centers, National Key Research and Development Program of China, Sino-Africa Joint Research Center, Chinese Academy of Sciences
Life below water
Openalex Percentile: Top 2%
Animal Genetics and Reproduction
10.90
DOIOpen Access PDFOpenAlex
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