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.
Subscribe to Journal
Get full journal access for 1 year
only $8.67 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Seehausen, O. et al. Genomics and the origin of species. Nat. Rev. Genet. 15, 176–192 (2014).
Harrison, R. G. & Larson, E. L. Heterogeneous genome divergence, differential introgression, and the origin and structure of hybrid zones. Mol. Ecol. 25, 2454–2466 (2016).
Payseur, B. A. & Rieseberg, L. H. A genomic perspective on hybridization and speciation. Mol. Ecol. 25, 2337–2360 (2016).
Wu, C. I. The genic view of the process of speciation. J. Evol. Biol. 14, 851–865 (2001).
Wolf, J. B. & Ellegren, H. Making sense of genomic islands of differentiation in light of speciation. Nat. Rev. Genet. 18, 87–100 (2017).
Ravinet, M. et al. Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow. J. Evol. Biol. 30, 1450–1477 (2017).
Nosil, P., Funk, D. J. & Ortiz-Barrientos, D. Divergent selection and heterogeneous genomic divergence. Mol. Ecol. 18, 375–402 (2009).
Noor, M. A. & Bennett, S. M. Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species. Heredity 103, 439–444 (2009).
Cruickshank, T. E. & Hahn, M. W. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol. Ecol. 23, 3133–3157 (2014).
Jones, F. C. et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55–61 (2012).
Soria-Carrasco, V. et al. Stick insect genomes reveal natural selection’s role in parallel speciation. Science 344, 738–742 (2014).
Marques, D. A. et al. Genomics of rapid incipient speciation in sympatric threespine stickleback. PLoS Genet. 12, e1005887 (2016).
Gagnaire, P.-A., Normandeau, E. & Bernatchez, L. Comparative genomics reveals adaptive protein evolution and a possible cytonuclear incompatibility between European and American eels. Mol. Ecol. Evol. 29, 2909–2919 (2012).
Bar-Yaacov, D. et al. Mitochondrial involvement in vertebrate speciation? The case of mito-nuclear genetic divergence in chameleons. Genome Biol. Evol. 7, 3322–3336 (2015).
Sambatti, J., Ortiz-Barrientos, D., Baack, E. J. & Rieseberg, L. H. Ecological selection maintains cytonuclear incompatibilities in hybridizing sunflowers. Ecol. Lett. 11, 1082–1091 (2008).
Baris, T. Z. et al. Evolved genetic and phenotypic differences due to mitochondrial–nuclear interactions. PLoS Genet. 13, e1006517 (2017).
Boratyński, Z., Ketola, T., Koskela, E., & Mappes, T. The sex specific genetic variation of energetics in bank voles, consequences of introgression?. Evol. Biol. 43, 37–47 (2016).
Allen, J. F. The function of genomes in bioenergetic organelles. Phil. Trans. R. Soc. B 358, 19–38 (2003).
Horan, M. P., Gemmell, N. J. & Wolff, J. N. From evolutionary bystander to master manipulator: the emerging roles for the mitochondrial genome as a modulator of nuclear gene expression. Eur. J. Human Genet. 21, 1335–1337 (2013).
Bar-Yaacov, D., Blumberg, A. & Mishmar, D. Mitochondrial–nuclear co-evolution and its effects on OXPHOS activity and regulation. Biochim. Biophys. Acta 1819, 1107–1111 (2012).
Ballard, J. W. O. & Pichaud, N. Mitochondrial DNA: more than an evolutionary bystander. Funct. Ecol. 28, 218–231 (2014).
Wolff, J. N., Ladoukakis, E. D., Enríquez, J. A. & Dowling, D. K. Mitonuclear interactions: evolutionary consequences over multiple biological scales. Phil. Trans. R. Soc. B 369, 20130443 (2014).
Hoekstra, L. A., Siddiq, M. A. & Montooth, K. L. Pleiotropic effects of a mitochondrial–nuclear incompatibility depend upon the accelerating effect of temperature in Drosophila. Genetics 195, 1129–1139 (2013).
Rand, D. M., Haney, R. A. & Fry, A. J. Cytonuclear coevolution: the genomics of cooperation. Trends Ecol. Evol. 19, 645–653 (2004).
Dowling, D. K., Friberg, U. & Lindell, J. Evolutionary implications of non-neutral mitochondrial genetic variation. Trends Ecol. Evol. 23, 546–554 (2008).
Osada, N. & Akashi, H. Mitochondrial–nuclear interactions and accelerated compensatory evolution: evidence from the primate cytochrome c oxidase complex. Mol. Ecol. Evol. 29, 337–346 (2012).
Sloan, D. B., Havird, J. C. & Sharbrough, J. The on-again, off-again relationship between mitochondrial genomes and species boundaries. Mol. Ecol. 26, 2212–2236 (2017).
Burton, R. S., Pereira, R. J. & Barreto, F. S. Cytonuclear genomic interactions and hybrid breakdown. Annu. Rev. Ecol. Evol. Syst. 44, 281–302 (2013).
Hill, G. E. Mitonuclear ecology. Mol. Ecol. Evol. 32, 1917–1927 (2015).
Das, J. The role of mitochondrial respiration in physiological and evolutionary adaptation. BioEssays 28, 890–901 (2006).
Stier, A. et al. Mitochondrial uncoupling as a regulator of life-history trajectories in birds: an experimental study in the zebra finch. J. Exp. Biol. 217, 3579–3589 (2014).
Burton, R. S. & Barreto, F. S. A disproportionate role for mtDNA in Dobzhansky–Muller incompatibilities? Mol. Ecol. 21, 4942–4957 (2012).
Lindtke, D. & Buerkle, C. A. The genetic architecture of hybrid incompatibilities and their effect on barriers to introgression in secondary contact. Evolution 69, 1987–2004 (2015).
Yeaman, S. Genomic rearrangements and the evolution of clusters of locally adaptive loci. Proc. Natl Acad. Sci. USA 110, E1743–E1751 (2013).
Kirkpatrick, M. & Barton, N. Chromosome inversions, local adaptation and speciation. Genetics 173, 419–434 (2006).
Morales, H. E., Sunnucks, P., Joseph, L. & Pavlova, A. Perpendicular axes of differentiation generated by mitochondrial introgression. Mol. Ecol. 26, 3241–3255 (2017).
Pavlova, A. et al. Perched at the mito-nuclear crossroads: divergent mitochondrial lineages correlate with environment in the face of ongoing nuclear gene flow in an Australian bird. Evolution 67, 3412–3428 (2013).
Morales, H. E., Pavlova, A., Joseph, L. & Sunnucks, P. Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance. Mol. Ecol. 24, 2820–2837 (2015).
Lamb, A. et al. Climate-driven mitochondrial selection: a test in Australian songbirds. Mol. Ecol. 27, 898–918 (2018).
Beck, E. A., Thompson, A. C., Sharbrough, J., Brud, E. & Llopart, A. Gene flow between Drosophila yakuba and Drosophila santomea in subunit V of cytochrome c oxidase: a potential case of cytonuclear cointrogression. Evolution 69, 1973–1986 (2015).
Debus, S. & Ford, H. Responses of eastern yellow robins Eopsaltria australis to translocation into vegetation remnants in a fragmented landscape. Pac. Conserv. Biol. 18, 194–202 (2012).
Kilian, A. et al. Diversity arrays technology: a generic genome profiling technology on open platforms. Methods Mol. Biol. 888, 67–89 (2012).
Hoban, S. et al. Finding the genomic basis of local adaptation: pitfalls, practical solutions, and future directions. Am. Nat. 188, 379–397 (2016).
Warren, W. C. et al. The genome of a songbird. Nature 464, 757–762 (2010).
Hofer, T., Foll, M. & Excoffier, L. Evolutionary forces shaping genomic islands of population differentiation in humans. BMC Genom. 13, 107 (2012).
Riley, L. G. et al. Mutation of the mitochondrial tyrosyl-tRNA synthetase gene, YARS2, causes myopathy, lactic acidosis, and sideroblastic anemia—MLASA syndrome. Am. J. Human Genet. 87, 52–59 (2010).
Meiklejohn, C. D. et al. An incompatibility between a mitochondrial tRNA and its nuclear-encoded tRNA synthetase compromises development and fitness in Drosophila. PLoS Genet. 9, e1003238 (2013).
Yip, C. Y., Harbour, M. E., Jayawardena, K., Fearnley, I. M. & Sazanov, L. A. Evolution of respiratory complex I: “supernumerary” subunits are present in the alpha-proteobacterial enzyme. J. Biol. Chem. 286, 5023–5033 (2011).
Angerer, H. et al. The LYR protein subunit NB4M/NDUFA6 of mitochondrial complex I anchors an acyl carrier protein and is essential for catalytic activity. Proc. Natl Acad. Sci. USA 111, 5207–5212 (2014).
Fiedorczuk, K. et al. Atomic structure of the entire mammalian mitochondrial complex I. Nature 538, 406–410 (2016).
Ostergaard, E. et al. Respiratory chain complex I deficiency due to NDUFA12 mutations as a new cause of Leigh syndrome. J. Med. Genet. 48, 737–740 (2011).
Zhu, J., Vinothkumar, K. R. & Hirst, J. Structure of mammalian respiratory complex I. Nature 536, 354–358 (2016).
Kim, Y. & Nielsen, R. Linkage disequilibrium as a signature of selective sweeps. Genetics 167, 1513–1524 (2004).
Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).
Irwin, D. E., Alcaide, M., Delmore, K. E., Irwin, J. H. & Owens, G. L. Recurrent selection explains parallel evolution of genomic regions of high relative but low absolute differentiation in a ring species. Mol. Ecol. 25, 4488–4507 (2016).
Turner, T. L. & Hahn, M. W. Genomic islands of speciation or genomic islands and speciation? Mol. Ecol. 19, 848–850 (2010).
Qvarnström, A., Ålund, M., McFarlane, S. E. & Sirkiä, P. M. Climate adaptation and speciation: particular focus on reproductive barriers in Ficedula flycatchers. Evol. Appl. 9, 119–134 (2016).
Sunnucks, P., Morales, H. E., Lamb, A. M., Pavlova, A. & Greening, C. Integrative approaches for studying mitochondrial and nuclear genome co-evolution in oxidative phosphorylation. Front. Genet. 8, 25 (2017).
Singhal, S. et al. Stable recombination hotspots in birds. Science 350, 928–932 (2015).
Kawakami, T. et al. Whole-genome patterns of linkage disequilibrium across flycatcher populations clarify the causes and consequences of fine-scale recombination rate variation in birds. Mol. Ecol. 26, 4158–4172 (2017).
Ellegren, H. et al. The genomic landscape of species divergence in Ficedula flycatchers. Nature 491, 756–760 (2012).
Hooper, D. M. & Price, T. D. Chromosomal inversion differences correlate with range overlap in passerine birds. Nat. Ecol. Evol. 1, 1526–1534 (2017).
Qvarnström, A. & Bailey, R. I. Speciation through evolution of sex-linked genes. Heredity 102, 4–15 (2009).
Mank, J. E., Nam, K. & Ellegren, H. Faster-Z evolution is predominantly due to genetic drift. Mol. Ecol. Evol. 27, 661–670 (2010).
Haldane, J. B. Sex ratio and unisexual sterility in hybrid animals. J. Genet. 12, 101–109 (1922).
Beekman, M., Dowling, D. K. & Aanen, D. K. The costs of being male: are there sex-specific effects of uniparental mitochondrial inheritance? Phil. Trans. R. Soc. B 369, 20130440 (2014).
Harrisson, K. A. et al. Fine-scale effects of habitat loss and fragmentation despite large-scale gene flow for some regionally declining woodland bird species. Landsc. Ecol. 27, 813–827 (2012).
Hill, G. E.., & Johnson, J. D.. The mitonuclear compatibility hypothesis of sexual selection. Proc. R. Soc. B 280, 20131314 (2013).
Morales, H. E. et al. Neutral and selective drivers of colour evolution in a widespread Australian passerine. J. Biogeogr. 44, 522–536 (2017).
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).
Hijmans R. J. raster: Geographic Data Analysis and Modeling R package version 2.3-12 (2014); http://www.rspatial.org/
R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014); http://www.R-project.org/
Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinformatics 10, 1 (2009).
Kawakami, T. et al. A high-density linkage map enables a second-generation collared flycatcher genome assembly and reveals the patterns of avian recombination rate variation and chromosomal evolution. Mol. Ecol. 23, 4035–4058 (2014).
Jombart, T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008).
Keenan, K., McGinnity, P., Cross, T. F., Crozier, W. W. & Prodöhl, P. A. diveRsity: an R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol. Evol. 4, 782–788 (2013).
Weir, B. S. & Cockerham, C. C. Estimating F-statistics for the analysis of population-structure. Evolution 38, 1358–1370 (1984).
Villemereuil, P. & Gaggiotti, O. E. A new F ST-based method to uncover local adaptation using environmental variables. Methods Ecol. Evol. 6, 1248–1258 (2015).
Plummer, M., Best, N., Cowles, K. & Vines, K. CODA: convergence diagnosis and output analysis for MCMC. R News 6, 7–11 (2006).
Duforet-Frebourg, N., Luu, K., Laval, G., Bazin, E. & Blum, M. G. Detecting genomic signatures of natural selection with principal component analysis: application to the 1000 Genomes data. Mol. Ecol. Evol. 33, 1082–1093 (2016).
Harte, D. Package ‘HiddenMarkov’: Hidden Markov Models R package version 1.8-4 (2015); https://cran.r-project.org/web/packages/HiddenMarkov/index.html
Cunningham, F. et al. Ensembl 2015. Nucleic Acids Res. 43, D662–D669 (2015).
Kanehisa, M.., & Goto, S.. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30 (2000).
Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Human Genet. 81, 559–575 (2007).
Hill, W. & Weir, B. Variances and covariances of squared linkage disequilibria in finite populations. Theor. Popul. Biol. 33, 54–78 (1988).
Marroni, F. et al. Nucleotide diversity and linkage disequilibrium in Populus nigra cinnamyl alcohol dehydrogenase (CAD4) gene. Tree Genet. Genomes 7, 1011–1023 (2011).
Warnes, G. & Leisch, F. Genetics: Population Genetics R package version 1.1-5 (2005); https://cran.r-project.org/web/packages/genetics/index.html
Shin, J.-H., Blay, S., McNeney, B. & Graham, J. LDheatmap: an R function for graphical display of pairwise linkage disequilibria between single nucleotide polymorphisms. J. Stat. Softw. 16, 1–10 (2006).
Richards, E. J. & Martin, C. H. Adaptive introgression from distant Caribbean islands contributed to the diversification of a microendemic adaptive radiation of trophic specialist pupfishes. PLoS Genet. 13, e1006919 (2017).
Wang, J. The computer program structure for assigning individuals to populations: easy to use but easier to misuse. Mol. Ecol. Resour. 17, 981–990 (2017).
Kopelman, N. M., Mayzel, J., Jakobsson, M., Rosenberg, N. A. & Mayrose, I. Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol. Ecol. Resour. 15, 1179–1191 (2015).
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.
A.K. is employed by the commercial service provider that produced genome marker data for the paper.
Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
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
Interactions between cytoplasmic and nuclear genomes confer sex‐specific effects on lifespan in Drosophila melanogaster
Journal of Evolutionary Biology (2020)
Mitochondrial genome diversity and population mitogenomics of polar cod (Boreogadus saida) and Arctic dwelling gadoids
Polar Biology (2020)
Genome-wide data reveal discordant mitonuclear introgression in the intermediate horseshoe bat (Rhinolophus affinis)
Molecular Phylogenetics and Evolution (2020)
Systematic Biology (2020)
Biology Letters (2020)