Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

High heterogeneity in genomic differentiation between phenotypically divergent songbirds: a test of mitonuclear co-introgression

Abstract

Comparisons of genomic variation among closely related species often show more differentiation in mitochondrial DNA (mtDNA) and sex chromosomes than in autosomes, a pattern expected due to the differing effective population sizes and evolutionary dynamics of these genomic components. Yet, introgression can cause species pairs to deviate dramatically from general differentiation trends. The yellowhammer (Emberiza citrinella) and pine bunting (E. leucocephalos) are hybridizing avian sister species that differ greatly in appearance and moderately in nuclear DNA, but that show no mtDNA differentiation. This discordance is best explained by adaptive mtDNA introgression—a process that can select for co-introgression at nuclear genes with mitochondrial functions (mitonuclear genes). To better understand these discordant differentiation patterns and characterize nuclear differentiation in this system, we investigated genome-wide differentiation between allopatric yellowhammers and pine buntings and compared it to what was seen previously in mtDNA. We found significant nuclear differentiation that was highly heterogeneous across the genome, with a particularly wide differentiation peak on the sex chromosome Z. We further investigated mitonuclear gene co-introgression between yellowhammers and pine buntings and found support for this process in the direction of pine buntings into yellowhammers. Genomic signals indicative of co-introgression were common in mitonuclear genes coding for subunits of the mitoribosome and electron transport chain complexes. Such introgression of mitochondrial DNA and mitonuclear genes provides a possible explanation for the patterns of high genomic heterogeneity in genomic differentiation seen among some species groups.

This is a preview of subscription content, access via your institution

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Fig. 1: Geographic distribution and phenotypic variation of sampled yellowhammers and pine buntings.
Fig. 2: Unrooted neighbor-joining tree of Emberizidae species constructed based on average absolute between-population nucleotide diversity (πB).
Fig. 3: PCA of genetic variation between allopatric yellowhammers (yellow; n = 53) and allopatric pine buntings (brown; n = 42), based on 374,780 genome-wide SNPs.
Fig. 4: Relative differentiation (FST) of 349,807 genome-wide SNPs identified among allopatric yellowhammers (n = 53) and allopatric pine buntings (n = 42), with chromosomes represented with alternating black and gray.
Fig. 5: Patterns of genetic variation comparing allopatric yellowhammers (n = 53) and allopatric pine buntings (n = 42) across chromosomes 2, 5 and Z shown as examples of general genomic patterns in this system (similar plots for all chromosomes can be found in Supplementary Fig. S4).
Fig. 6: A summary of genetic statistics calculated for allopatric populations of yellowhammers and pine buntings.

Data availability

Raw DNA sequencing reads are available on the NBCI Sequence Read Archive (BioProject PRJNA768601). Read processing codes, barcodes, genotype data and R codes associated with statistical analyses will be made available on Dryad.

References

  • Alcaide M, Scordato ESC, Price TD, Irwin DE (2014) Genomic divergence in a ring species complex. Nature 511:83–85

    Article  CAS  Google Scholar 

  • Alström P, Olsson U, Lei F, Wang H, Gao W, Sundberg P (2008) Phylogeny and classification of the old world Emberizini (Aves, Passeriformes). Mol Phylogenet Evol 47:960–973

    Article  Google Scholar 

  • Alves PC, Melo-Ferreira J, Freitas H, Boursot P (2008) The ubiquitous mountain hare mitochondria: Multiple introgressive hybridization in hares, genus Lepus. Philos Trans R Soc B 363:2831–2839

    Article  Google Scholar 

  • Avise JC (2000) Phylogeography: The history and formation of species. Harvard University Press, Cambridge, Mass

  • Ballard JWO, Melvin RG, Katewa SD, Maas K (2007) Mitochondrial DNA variation is associated with measurable differences in life-history traits and mitochondrial metabolism in Drosophila simulans. Evolution 61:1735–1747

    Article  CAS  Google Scholar 

  • Barreto FS, Watson ET, Lima TG, Willett CS, Edmands S, Li W et al. (2018) Genomic signatures of mitonuclear coevolution across populations of Tigriopus californicus. Nat Ecol Evol 2:1250–1257

    Article  Google Scholar 

  • Barrientos A, Müller S, Dey R, Wienberg J, Moraes CT (2000) Cytochrome c oxidase assembly in primates is sensitive to small evolutionary variations in amino acid sequence. Mol Biol Evol 17:1508–1519

    Article  CAS  Google Scholar 

  • Baute GJ, Owens GL, Bock DG, Rieseberg LH (2016) Genome‐wide genotyping‐by‐sequencing data provide a high‐resolution view of wild Helianthus diversity, genetic structure, and interspecies gene flow. Am J Bot 103:2170–2177

    Article  Google Scholar 

  • Beck EA, Thompson AC, Sharbrough J, Brud E, Llopart A (2015) 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

    Article  CAS  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  Google Scholar 

  • Borge T, Webster MT, Andersson G, Saetre G (2005) Contrasting patterns of polymorphism and divergence on the Z chromosome and autosomes in two Ficedula flycatcher species. Genetics 171:1861–1873

    Article  CAS  Google Scholar 

  • Burton RS, Barreto FS (2012) A disproportionate role for mtDNA in Dobzhansky–Muller incompatibilities? Mol Ecol 21:4942–4957

    Article  CAS  Google Scholar 

  • Bryson J, Robert W, De Oca AN, Jaeger JR, Riddle BR (2010) Elucidation of cryptic diversity in a widespread Nearctic treefrog reveals episodes of mitochondrial gene capture as frogs diversified across a dynamic landscape. Evolution 64:2315–2330

    CAS  Google Scholar 

  • Calvo SE, Mootha VK (2010) The mitochondrial proteome and human disease. Annu Rev Genom. Hum Genet 11:25–44

    CAS  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland, Mass

  • Cruickshank TE, Hahn MW (2014) Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol Ecol 23:3133–3157

    Article  Google Scholar 

  • Cutter AD, Payseur BA (2013) Genomic signatures of selection at linked sites: unifying the disparity among species. Nat Rev Genet 14:262–274

    Article  CAS  Google Scholar 

  • Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA et al. (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158

    Article  CAS  Google Scholar 

  • Dean R, Zimmer F, Mank JE (2014) The potential role of sexual conflict and sexual selection in shaping the genomic distribution of mito-nuclear genes. Genome Biol Evol 6:1096–1104

    Article  CAS  Google Scholar 

  • Diodato D, Ghezzi D, Tiranti V (2014) The mitochondrial aminoacyl tRNA synthetases: Genes and syndromes. Int J Cell Biol 2014:1–11

    Article  Google Scholar 

  • Drown DM, Preuss KM, Wade MJ (2012) Evidence of a paucity of genes that interact with the mitochondrion on the X in mammals. Genome Biol Evol 4:763–880

    Article  Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES et al. (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PloS ONE 6:e19379

    Article  CAS  Google Scholar 

  • Ernster L, Schatz G (1981) Mitochondria: A historical review. J Cell Biol 91:227s–255s

    Article  CAS  Google Scholar 

  • Gascuel O (1997) BIONJ: An improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14:685–695

    Article  CAS  Google Scholar 

  • Geraldes A, Askelson KK, Nikelski E, Doyle FI, Harrower WL, Winker K et al. (2019) Population genomic analyses reveal a highly differentiated and endangered genetic cluster of northern goshawks (Accipiter gentilis laingi) in Haida Gwaii. Evol Appl 12:757–772

    Article  CAS  Google Scholar 

  • Gershoni M, Levin L, Ovadia O, Toiw Y, Shani N, Dadon S et al. (2014) Disrupting mitochondrial-nuclear coevolution affects OXPHOS complex I integrity and impacts human health. Genome Biol Evol 6:2665–2680

    Article  CAS  Google Scholar 

  • Gershoni M, Templeton AR, Mishmar D (2009) Mitochondrial bioenergetics as a major motive force of speciation. BioEssays 31:642–650

    Article  CAS  Google Scholar 

  • Greber BJ, Ban N (2016) Structure and function of the mitochondrial ribosome. Annu Rev Biochem 85:103–132

    Article  CAS  Google Scholar 

  • Harr B (2006) Genomic islands of differentiation between house mouse subspecies. Genome Res 16:730–737

    Article  CAS  Google Scholar 

  • Hebert PD, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101:14812–14817

    Article  CAS  Google Scholar 

  • Hejase HA, Salman-Minkov A, Campagna L, Hubisz MJ, Lovette IJ, Gronau I et al. (2020) Genomic islands of differentiation in a rapid avian radiation have been driven by recent selective sweeps. Proc Natl Acad Sci USA 117:30554–30565

    Article  CAS  Google Scholar 

  • Hill GE, (2019a) Reconciling the mitonuclear compatibility species concept with rampant mitochondrial introgression Integr Comp Biol 59:912–924

  • Hill GE (2019b) Mitonuclear Ecology (First ed.). Oxford University Press, Oxford

  • Hill GE (2020) Genetic hitchhiking, mitonuclear coadaptation, and the origins of mt DNA barcode gaps. Ecol Evol 10:9048–9059

    Article  Google Scholar 

  • Hulsey CD, Bell KL, García‐de‐León FJ, Nice CC, Meyer A (2016) Do relaxed selection and habitat temperature facilitate biased mitogenomic introgression in a narrowly endemic fish? Ecol Evol 6:3684–3698

    Article  Google Scholar 

  • Irwin DE (2018) Sex chromosomes and speciation in birds and other ZW systems. Mol Ecol 27:3831–3851

    Article  CAS  Google Scholar 

  • Irwin DE, Alcaide M, Delmore KE, Irwin JH, Owens GL (2016) Recurrent selection explains parallel evolution of genomic regions of high relative but low absolute differentiation in a ring species. Mol Ecol 25:4488–4507

    Article  Google Scholar 

  • Irwin DE, Milá B, Toews DPL, Brelsford A, Kenyon HL, Porter AN et al. (2018) A comparison of genomic islands of differentiation across three young avian species pairs. Mol Ecol 27:4839–4855

    Article  CAS  Google Scholar 

  • Irwin DE, Rubtsov AS, Panov EN (2009) Mitochondrial introgression and replacement between yellowhammers (Emberiza citrinella) and pine buntings (Emberiza leucocephalos) (Aves: Passeriformes). Biol J Linn Soc 98:422–438

    Article  Google Scholar 

  • Kerr KCR, Stoeckle MY, Dove CJ, Weigt LA, Francis CM, Hebert PDN (2007) Comprehensive DNA barcode coverage of North American birds. Mol Ecol Notes 7:535–543

    Article  CAS  Google Scholar 

  • Kirkpatrick M (2010) How and why chromosome inversions evolve. PLoS Biol 8:e1000501

    Article  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows- Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N et al. (2009) The sequence alignment map format and SAMtools. Bioinformatics 25:2078–2079

    Article  Google Scholar 

  • Llopart A, Herrig D, Brud E, Stecklein Z (2014) Sequential adaptive introgression of the mitochondrial genome in Drosophila yakuba and Drosophila santomea. Mol Ecol 23:1124–1136

    Article  CAS  Google Scholar 

  • Lotz C, Lin AJ, Black CM, Zhang J, Lau E, Deng N et al. (2014) Characterization, design, and function of the mitochondrial proteome: From organs to organisms. J Proteome Res 13:433–446

    Article  CAS  Google Scholar 

  • Lu J, Wu C (2005) Weak selection revealed by the whole-genome comparison of the X chromosome and autosomes of human and chimpanzee. Proc Natl Acad Sci 102:4063–4067

    Article  CAS  Google Scholar 

  • Lynch M, Koskella B, Schaack S (2006) Mutation pressure and the evolution of organelle genomic architecture. Science 311:1727–1730

    Article  CAS  Google Scholar 

  • Mank JE, Nam K, Ellegren H (2010) Faster-Z evolution is predominantly due to genetic drift. Mol Biol Evol 27:661–670

    Article  CAS  Google Scholar 

  • Manthey JD, Geiger M, Moyle RG (2017) Relationships of morphological groups in the northern flicker superspecies complex (Colaptes auratus & C. chrysoides). Syst Biodivers 15:183–191

    Article  Google Scholar 

  • McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A et al. (2010) The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    Article  CAS  Google Scholar 

  • Meisel RP, Connallon T (2013) The faster-X effect: Integrating theory and data. Trends Genet 29:537–544

    Article  CAS  Google Scholar 

  • Moore WS (1995) Inferring phylogenies from mtDNA variation: Mitochondrial-gene trees versus nuclear-gene trees. Evolution 49:718–726

    Google Scholar 

  • Morales HE, Pavlova A, Amos N, Major R, Kilian A, Greening C et al. (2018) Concordant divergence of mitogenomes and a mitonuclear gene cluster in bird lineages inhabiting different climates. Nat Ecol Evol 2:1258–1267

    Article  Google Scholar 

  • Nadeau NJ, Whibley A, Jones RT, Davey JW, Dasmahapatra KK, Baxter SW et al. (2012) Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing. Philos Trans R Soc B 367:343–353

    Article  CAS  Google Scholar 

  • Osada N, Akashi H (2012) Mitochondrial-nuclear interactions and accelerated compensatory evolution: Evidence from the primate cytochrome c oxidase complex. Mol Biol Evol 29:337–346

    Article  CAS  Google Scholar 

  • Panov EN, Rubtsov AS, Monzikov DG (2003) Hybridization between yellowhammer and pine bunting in Russia. Dutch Bird 25:17–31

    Google Scholar 

  • Panov EN, Rubtsov AS, Mordkovich MV (2007) New data on the relationships between two species of buntings (Emberiza citrinella and E. leucocephalos) hybridizing in the areas of overlap of their ranges. Zool Zh 86:1362–1378

    Google Scholar 

  • Paradis E, Schliep K (2019) Ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528

    Article  CAS  Google Scholar 

  • Price T (2008) Speciation in birds. Roberts and Co, Greenwood Village, Colo

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.r-project.org/

    Google Scholar 

  • Rubtsov AS (2007) Variability of songs of the yellowhammer (Emberiza citrinella) and pine bunting (Emberiza leucocephala) as an evidence of population structure and evolutionary history of the species. Zool Zh 86:863–876

    Google Scholar 

  • Rubtsov AS, Opaev AS (2012) Phylogeny reconstruction of the yellowhammer (Emberiza citrinella) and pine bunting (Emberiza leucocephala) based on song and morphological characters. Biol Bull Russ Acad Sci 39:715–728

    Article  Google Scholar 

  • Rubtsov AS, Tarasov VV (2017) Relations between the yellowhammer (Emberiza citrinella) and the pine bunting (Emberiza leucocephalos) in the forested steppe of the Trans-Urals. Biol Bull 44:1059–1072

    Article  Google Scholar 

  • Ruegg K, Anderson EC, Boone J, Pouls J, Smith TB (2014) A role for migration-linked genes and genomic islands in divergence of a songbird. Mol Ecol 23:4757–4769

    Article  Google Scholar 

  • Sackton TB, Corbett-Detig RB, Nagaraju J, Vaishna L, Arunkumar KP, Hartl DL (2014) Positive selection drives faster-z evolution in silkmoths. Evolution 68:2331–2342

    Google Scholar 

  • Sackton TB, Haney RA, Rand DM (2003) Cytonuclear coadaptation in Drosophila: Disruption of cytochrome c oxidase activity in backcross genotypes. Evolution 57:2315–2325

    CAS  Google Scholar 

  • Saraste M (1999) Oxidative phosphorylation at the fin de siècle. Science 283:1488–1493

    Article  CAS  Google Scholar 

  • Scordato ESC, Wilkins MR, Semenov G, Rubtsov AS, Kane NC, Safran RJ (2017) Genomic variation across two barn swallow hybrid zones reveals traits associated with divergence in sympatry and allopatry. Mol Ecol 26:5676–5691

    Article  Google Scholar 

  • Sloan DB, Havird JC, Sharbrough J (2017) The on-again, off-again relationship between mitochondrial genomes and species boundaries. Mol Ecol 26:2212–2236

    Article  Google Scholar 

  • Sloan DB, Triant DA, Wu M, Taylor DR (2014) Cytonuclear interactions and relaxed selection accelerate sequence evolution in organelle ribosomes. Mol Biol Evol 31:673–682

    Article  CAS  Google Scholar 

  • Smukowski CS, Noor MAF (2011) Recombination rate variation in closely related species. Heredity 107:496–508

    Article  CAS  Google Scholar 

  • Stacklies W, Redestig H, Scholz M, Walther D, Selbig J (2007) PcaMethods-a bioconductor package providing PCA methods for incomplete data. Bioinformatics 23:1164–1167

    Article  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    Article  CAS  Google Scholar 

  • Thornton K, Long M (2002) Rapid divergence of gene duplicates on the Drosophila melanogaster X chromosome. Mol Biol Evol 19:918–925

    Article  CAS  Google Scholar 

  • Toews DPL, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21:3907–3930

    Article  CAS  Google Scholar 

  • Turner S (2018) Qqman: An R package for visualizing GWAS results using Q-Q and Manhattan plots. J Open Source Softw 3:731

    Article  Google Scholar 

  • Wang S, Ore MJ, Mikkelsen EK, Lee-Yaw J, Toews DPL, Rohwer S et al. (2021) Signatures of mitonuclear coevolution in a warbler species complex. Nat Commun 12:4279–4279

    Article  CAS  Google Scholar 

  • Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW, Künstner A et al. (2010) The genome of a songbird. Nature 464:757–762

    Article  CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  Google Scholar 

  • Wu C (2001) The genic view of the process of speciation. J Evol Biol 14:851–865

    Article  Google Scholar 

  • Yannic G, Dubey S, Hausser J, Basset P (2010) Additional data for nuclear DNA give new insights into the phylogenetic position of Sorex granarius within the Sorex araneus group. Mol Phylogenet Evol 57:1062–1071

    Article  CAS  Google Scholar 

Download references

Acknowledgements

For providing valuable feedback, we thank Dolph Schluter, Eric Taylor, Judith Mank, Elizabeth Natola, Rashika Ranasinghe, Kenneth Askelson, Finola Fogarty, Quinn McCallum, Ana Barreira, Jamie Clarke, Armando Geraldes, Jessica Irwin and several anonymous reviewers. For their kindness and support during field work, we thank the Tazeev family and Madelyn Ore. For providing additional samples, we thank The Bell Museum, The Burke Museum of Natural History and Culture, The Field Museum, The State Darwin Museum, The Swedish Museum of Natural History, The Zoological Museum of the Zoological Institute of the Russian Academy of Sciences, and the Zoological Museum of the University of Copenhagen and their accompanying personnel. Major research funding was provided by the Natural Sciences and Engineering Research Council of Canada (NSERC CGSM award to EN, Discovery Grants RGPIN-2017-03919 and RGPAS-2017-507830 awarded to DI) and by the Werner and Hildegard Hesse research awards (Research award in Ornithology and Fellowship in Ornithology awarded to EN by the University of British Columbia).

Author information

Authors and Affiliations

Authors

Contributions

EN, DI, and ASR conceived of this study. ASR collected samples. EN and ASR completed molecular techniques. EN conducted data analysis and wrote this paper with input from DI and ASR.

Corresponding author

Correspondence to Ellen Nikelski.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Associate editor: Paul Sunnucks.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nikelski, E., Rubtsov, A.S. & Irwin, D. High heterogeneity in genomic differentiation between phenotypically divergent songbirds: a test of mitonuclear co-introgression. Heredity 130, 1–13 (2023). https://doi.org/10.1038/s41437-022-00580-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41437-022-00580-8

Search

Quick links