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Investigating mitonuclear interactions in human admixed populations.

ABSTRACT: To function properly, mitochondria utilize products of 37 mitochondrial and >1,000 nuclear genes, which should be compatible with each other. Discordance between mitochondrial and nuclear genetic ancestry could contribute to phenotypic variation in admixed populations. Here, we explored potential mitonuclear incompatibility in six admixed human populations from the Americas: African Americans, African Caribbeans, Colombians, Mexicans, Peruvians and Puerto Ricans. By comparing nuclear versus mitochondrial ancestry in these populations, we first show that mitochondrial DNA (mtDNA) copy number decreases with increasing discordance between nuclear and mtDNA ancestry. The direction of this effect is consistent across mtDNA haplogroups of different geographic origins. This observation indicates suboptimal regulation of mtDNA replication when its components are encoded by nuclear and mtDNA genes with different ancestry. Second, while most populations analysed exhibit no such trend, in African Americans and Puerto Ricans, we find a significant enrichment of ancestry at nuclear-encoded mitochondrial genes towards the source populations contributing the most prevalent mtDNA haplogroups (African and Native American, respectively). This possibly reflects compensatory effects of selection in recovering mitonuclear interactions optimized in the source populations. Our results provide evidence of mitonuclear interactions in human admixed populations and we discuss their implications for human health and disease.

SUBMITTER: Zaidi AA

PROVIDER: S-EPMC6925600 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Investigating mitonuclear interactions in human admixed populations.

Zaidi Arslan A AA Makova Kateryna D KD

Nature ecology & evolution 20190114 2

To function properly, mitochondria utilize products of 37 mitochondrial and >1,000 nuclear genes, which should be compatible with each other. Discordance between mitochondrial and nuclear genetic ancestry could contribute to phenotypic variation in admixed populations. Here, we explored potential mitonuclear incompatibility in six admixed human populations from the Americas: African Americans, African Caribbeans, Colombians, Mexicans, Peruvians and Puerto Ricans. By comparing nuclear versus mito ...[more]

PMID: 30643241

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Project description:BackgroundAfrica is an important watershed in the genetic history of domestic cattle, as two lineages of modern cattle, Bos taurus and B. indicus, form distinct admixed cattle populations. Despite the predominant B. indicus nuclear ancestry of African admixed cattle, B. indicus mitochondria have not been found on the continent. This discrepancy between the mitochondrial and nuclear genomes has been previously hypothesized to be driven by male-biased introgression of Asian B. indicus into ancestral African B. taurus. Given that this hypothesis mandates extreme demographic assumptions relying on random genetic drift, we propose a novel hypothesis of selection induced by mitonuclear incompatibility and assess these hypotheses with regard to the current genomic status of African admixed cattle.ResultsBy analyzing 494 mitochondrial and 235 nuclear genome sequences, we first confirmed the genotype discrepancy between mitochondrial and nuclear genome in African admixed cattle: the absence of B. indicus mitochondria and the predominant B. indicus autosomal ancestry. We applied approximate Bayesian computation (ABC) to assess the posterior probabilities of two selection hypotheses given this observation. The results of ABC indicated that the model assuming both male-biased B. indicus introgression and selection induced by mitonuclear incompatibility explains the current genomic discrepancy most accurately. Subsequently, we identified selection signatures at autosomal loci interacting with mitochondria that are responsible for integrity of the cellular respiration system. By contrast with B. indicus-enriched genome ancestry of African admixed cattle, local ancestries at these selection signatures were enriched with B. taurus alleles, concurring with the key expectation of selection induced by mitonuclear incompatibility.ConclusionsOur findings support the current genome status of African admixed cattle as a potential outcome of male-biased B. indicus introgression, where mitonuclear incompatibility exerted selection pressure against B. indicus mitochondria. This study provides a novel perspective on African cattle demography and supports the role of mitonuclear incompatibility in the hybridization of mammalian species.

Dataset Information

Investigating mitonuclear interactions in human admixed populations.

Publications

Investigating mitonuclear interactions in human admixed populations.

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