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The role of mitonuclear incompatibilities in allopatric speciation

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Abstract

Aerobic metabolism in eukaryotic cells requires extensive interactions between products of the nuclear and mitochondrial genomes. Rapid evolution of the mitochondrial genome, including fixation of both adaptive and deleterious mutations, creates intrinsic selection pressures favoring nuclear gene mutations that maintain mitochondrial function. As this process occurs independently in allopatry, the resulting divergence between conspecific populations can subsequently be manifest in mitonuclear incompatibilities in inter-population hybrids. Such incompatibilities, mitonuclear versions of Bateson–Dobzhansky–Muller incompatibilities that form the standard model for allopatric speciation, can potentially restrict gene flow between populations, ultimately resulting in varying degrees of reproductive isolation. The potential role of mitonuclear incompatibilities in speciation is further enhanced where mtDNA substitution rates are elevated compared to the nuclear genome and where population structure maintains allopatry for adequate time to evolve multiple mitonuclear incompatibilities. However, the fact that mitochondrial introgression occurs across species boundaries has raised questions regarding the efficacy of mitonuclear incompatibilities in reducing gene flow. Several scenarios now appear to satisfactorily explain this phenomenon, including cases where differences in mtDNA genetic load may drive introgression or where co-introgression of coadapted nuclear genes may support the function of introgressed mtDNA. Although asymmetries in reproductive isolation between taxa are consistent with mitonuclear incompatibilities, interactions between autosomes and sex chromosomes yield similar predictions that are difficult to disentangle. With regard to establishing reproductive isolation while in allopatry, existing studies clearly suggest that mitonuclear incompatibilities can contribute to the evolution of barriers to gene flow. However, there is to date relatively little definitive evidence supporting a primary role for mitonuclear incompatibilities in the speciation process.

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Acknowledgements

The author gratefully acknowledges discussions with T. Healy on the content of this paper and the helpful comments from two anonymous reviewers.

Funding

The author gratefully acknowledges support from the US National Science Foundation (Grant Number: IOS 1754347).

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  1. Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA, 92093-0202, USA

    Ronald S. Burton

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RSB wrote this invited review paper as sole author and prepared Figs. 1 and 2. Permission for reuse of Fig. 3 is granted under the blanket permissions from the Proceedings of the National Academy of Sciences for author reuse: "PNAS authors need not obtain permission for the following cases: (1) to use their original figures or tables in their future works."

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Correspondence to Ronald S. Burton.

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Burton, R.S. The role of mitonuclear incompatibilities in allopatric speciation. Cell. Mol. Life Sci. 79, 103 (2022). https://doi.org/10.1007/s00018-021-04059-3

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