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Investigating mitonuclear interactions in human admixed populations

Nature Ecology & Evolution volume 3, pages 213–222 (2019)Cite this article

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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.

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Fig. 1: Expected signatures of mitonuclear incompatibility at the level of individuals or populations.
Fig. 2: Ternary plots showing the distribution of African, European and Native American ancestry in the samples analysed (samples sizes are shown in parentheses).
Fig. 3: mtDNA copy number in admixed and non-admixed populations.
Fig. 4: Expected versus observed frequency of mtDNA haplogroups from each of the three source populations.
Fig. 5: Systematic deviations in local ancestry for different functional categories of genes.

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Data availability

All analyses were conducted using publicly available data. The 1000 Genomes Project data are available on its FTP site. Intermediate files and code have been made publicly available on github: (https://github.com/makovalab-psu/Mito_nuclear_incompatibility).

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Acknowledgements

We thank R. Nielsen, M. Shriver, W. Chase and S. Craig for their comments on the manuscript. We would also like to thank E. Torres Gonzalez for reviewing the code. This project was supported by a seed grant awarded to A.A.Z. and K.D.M. from the Center of Human Evolution and Diversity (CHED) at The Pennsylvania State University and by a grant from NIH (R01GM116044). Additional funding was provided by the Eberly College of Sciences, The Huck Institute of Life Sciences and the Institute for CyberScience at Penn State, as well as, in part, under grants from the Pennsylvania Department of Health using Tobacco Settlement and CURE Funds. The department specifically disclaims any responsibility for any analyses, responsibility or conclusions.

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  1. Department of Biology, The Pennsylvania State University, University Park, PA, USA

    Arslan A. Zaidi & Kateryna D. Makova

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  1. Arslan A. Zaidi
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A.A.Z. and K.D.M. conceived the study. A.A.Z. carried out analyses. A.A.Z. and K.D.M. wrote and edited the paper.

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Correspondence to Kateryna D. Makova.

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Supplementary Tables

Supplementary Table 1, mtDNA copy number data; Supplementary Table 2, Autosomal ancestry fractions for all samples used in the study; Supplementary Table 3, X-chromosomal ancestry fractions for all samples used in the study; Supplementary Table 4, mtDNA haplogroup information for each sample; Supplementary Table 5, List of genes from Mitocarta 2.0 with functional annotation

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Zaidi, A.A., Makova, K.D. Investigating mitonuclear interactions in human admixed populations. Nat Ecol Evol 3, 213–222 (2019). https://doi.org/10.1038/s41559-018-0766-1

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