Concordant divergence of mitogenomes and a mitonuclear gene cluster in bird lineages inhabiting different climates

Abstract

Metabolic processes in eukaryotic cells depend on interactions between mitochondrial and nuclear gene products (mitonuclear interactions). These interactions could have a direct role in population divergence. Here, we study mitonuclear co-evolution in a widespread bird that experienced population divergence followed by bidirectional mitochondrial introgression into different nuclear backgrounds. Using >60,000 single nucleotide polymorphisms, we quantify patterns of nuclear genetic differentiation between populations that occupy areas with different climates and harbour deeply divergent mitochondrial lineages despite ongoing nuclear gene flow. We find that strong genetic differentiation and sequence divergence in a region of ~15.4 megabases on chromosome 1A mirror the geographic pattern of mitochondrial DNA divergence. This result is seen in two different transects representing populations with different nuclear backgrounds. The chromosome 1A region is enriched for genes performing mitochondrial functions (N-mt genes). Molecular signatures of selective sweeps in this region alongside those in the mitochondrial genome suggest a history of adaptive mitonuclear co-introgression. Moreover, evidence for large linkage disequilibrium blocks in this genomic region suggests that low recombination could facilitate functional interactions between co-evolved nuclear alleles. Our results are consistent with mitonuclear co-evolution as an important mechanism for population divergence and local adaptation.

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Fig. 1: Geographic and climatic distribution of mitochondrial and nuclear genetic variation across the EYR range.
Fig. 2: Heterogeneous genomic differentiation between mito-A- and mito-B-bearing analysis groups, and properties of the chromosome 1A cluster of differentiation.
Fig. 3: Linkage disequilibrium blocks within the chromosome 1A cluster of differentiation for individuals in the contact zone and away from the contact zone.
Fig. 4: Individual admixture at genome-wide non-outliers (GWN), autosomal outliers not in the chromosome 1A cluster of differentiation (AO) and chromosome 1A cluster outliers (1A-O), mitochondrial–nuclear matching of 1A-O, and their geographic distributions.

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Acknowledgements

H.E.M. was supported by the Holsworth Wildlife Research Endowment (2012001942) and Stuart Leslie Bird Research Award from BirdLife Australia, PhD scholarships from Monash University and the Department of Public Education of the Mexican Government, and a Monash Postgraduate Publication Award. C.G. was supported by an ARC DECRA Fellowship (DE170100310). Other funding came from Monash internal sources. Genomic analyses were undertaken at the Monash High-Performance Computing facility and on the Albiorix computer cluster at the Department of Marine Sciences, University of Gothenburg. Field samples were collected under scientific research permits issued by the Victorian Department of Environment and Primary Industries (numbers 10007165, 10005919 and 10005514), New South Wales Office of Environment and Heritage (SL100886), in accordance with Animal Ethics approvals AM13-05, BSCI_2012_20 and BSCI_2007_07, using bands issued by the Australian Bird and Bat Banding Scheme. We are grateful to L. Joseph, R. Palmer, H. Sitters and C. Connelly for providing genetic samples. A. Gonçalves da Silva, D. Marques, S. Martin and V. Soria-Carrasco provided valuable inputs regarding data analysis, L. Joseph provided input on EYR evolution, and J. Wolf provided input on functional properties of the mitonuclear candidates. We thank S. Edwards, M. Webster, L. Kvistad and S. Falk for comments on earlier versions of the manuscript.

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H.E.M., A.P. and P.S. conceived the project. H.E.M., A.P., N.A. and R.M. obtained the field samples. H.E.M. obtained the genetic data and performed the analyses. C.G. performed the protein structural analyses. H.E.M. wrote the paper with the help of A.P., C.G. and P.S. All co-authors read and approved the final version.

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Correspondence to Hernán E. Morales.

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A.K. is employed by the commercial service provider that produced genome marker data for the paper.

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Morales, H.E., Pavlova, A., Amos, N. et al. Concordant divergence of mitogenomes and a mitonuclear gene cluster in bird lineages inhabiting different climates. Nat Ecol Evol 2, 1258–1267 (2018). https://doi.org/10.1038/s41559-018-0606-3

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