Evaluating evidence of mitonuclear incompatibilities with the sex chromosomes in an avian hybrid zone

Kelsie A. Lopez, Callum S. McDiarmid, Simon C. Griffith, Irby J. Lovette, Daniel M. Hooper*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

The exploration of hybrid zones and the intergenomic conflicts exposed through hybridization provide windows into the processes of divergence and speciation. Sex chromosomes and mitonuclear incompatibilities have strong associations with the genetics of hybrid dysfunction. In ZW sex-determining systems, maternal co-inheritance of the mitochondrial and W chromosomes immediately exposes incompatibilities between these maternal contributions of one species and the Z chromosome of another. We analyze mitochondrial and Z chromosome admixture in the long-tailed finch (Poephila acuticauda) of Australia, where hybridizing subspecies differ prominently in Z chromosome genotype and in bill color, yet the respective centers of geographic admixture for these two traits are offset by 350 km. We report two well-defined mitochondrial clades that diverged ∼0.5 million years ago. Mitochondrial contact is geographically co-located within a hybrid zone of Z chromosome admixture and is displaced from bill color admixture by nearly 400 km. Consistent with Haldane's rule expectations, hybrid zone females are significantly less likely than males to carry an admixed Z chromosome or have mismatched Z-mitochondrial genotypes. Furthermore, there are significantly fewer than expected mitonuclear mismatches in hybrid zone females and paternal backcross males. Results suggest a potential for mitonuclear/sex chromosome incompatibilities in the emergence of reproductive isolation in this system.

Original languageEnglish
Number of pages20
JournalEvolution
Early online date28 Apr 2021
DOIs
Publication statusE-pub ahead of print - 28 Apr 2021

Bibliographical note

Funding Information:
We are grateful to the management teams of all stations listed in Table 1 for allowing us to conduct research on their properties. Emma Greig and Kyle Kostrzewa were essential help with fieldwork. Leo Joseph approved loans of tissue and blood samples from the CSIRO collections. Trevor Price provided valuable feedback on the manuscript. This research was funded by a Discovery Grant from the Australian Research Council (DP0881019), a Cornell Lab of Ornithology Rose Postdoctoral Fellowship, the Bernard F. Iliff Undergraduate Research Fund at the Cornell Lab of Ornithology, and the Sally Merrill Sutcliffe Endowment for Cornell Students. We declare no conflicts of interest in the publication of this manuscript.

Publisher Copyright:
© 2021 The Authors. Evolution © 2021 The Society for the Study of Evolution.

Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.

Keywords

  • Haldane's rule
  • hybrid zone
  • mitonuclear incompatibility
  • Poephila
  • sex chromosome

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