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

Heredity volume 130, pages 1–13 (2023)Cite this article

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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.

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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.

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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).

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  1. Ellen Nikelski

    Present address: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada

Authors and Affiliations

  1. Department of Zoology, and Biodiversity Research Centre, 6270 University Blvd., University of British Columbia, Vancouver, BC, Canada

    Ellen Nikelski & Darren Irwin

  2. State Darwin Museum, Moscow, Russia

    Alexander S. Rubtsov

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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.

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Correspondence to Ellen Nikelski.

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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

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