A lethal mitonuclear incompatibility in complex I of natural hybrids

Benjamin M. Moran (), Cheyenne Y. Payne, Daniel L. Powell, Erik N. K. Iverson, Alexandra E. Donny, Shreya M. Banerjee, Quinn K. Langdon, Theresa R. Gunn, Rebecca A. Rodriguez-Soto, Angel Madero, John J. Baczenas, Korbin M. Kleczko, Fang Liu, Rowan Matney, Kratika Singhal, Ryan D. Leib, Osvaldo Hernandez-Perez, Russell Corbett-Detig, Judith Frydman, Casey Gifford, Manfred Schartl, Justin C. Havird and Molly Schumer ()
Additional contact information
Benjamin M. Moran: Stanford University
Cheyenne Y. Payne: Stanford University
Daniel L. Powell: Stanford University
Erik N. K. Iverson: University of Texas at Austin
Alexandra E. Donny: Stanford University
Shreya M. Banerjee: Stanford University
Quinn K. Langdon: Stanford University
Theresa R. Gunn: Stanford University
Rebecca A. Rodriguez-Soto: Stanford University
Angel Madero: Stanford University
John J. Baczenas: Stanford University
Korbin M. Kleczko: Stanford University
Fang Liu: Stanford University
Rowan Matney: Stanford University
Kratika Singhal: Stanford University
Ryan D. Leib: Stanford University
Osvaldo Hernandez-Perez: Centro de Investigaciones Científicas de las Huastecas ‘Aguazarca’, A.C., Calnali
Russell Corbett-Detig: University of California Santa Cruz
Judith Frydman: Stanford University
Casey Gifford: Stanford University
Manfred Schartl: Texas State University
Justin C. Havird: University of Texas at Austin
Molly Schumer: Stanford University

Nature, 2024, vol. 626, issue 7997, 119-127

Abstract: Abstract The evolution of reproductive barriers is the first step in the formation of new species and can help us understand the diversification of life on Earth. These reproductive barriers often take the form of hybrid incompatibilities, in which alleles derived from two different species no longer interact properly in hybrids1–3. Theory predicts that hybrid incompatibilities may be more likely to arise at rapidly evolving genes4–6 and that incompatibilities involving multiple genes should be common7,8, but there has been sparse empirical data to evaluate these predictions. Here we describe a mitonuclear incompatibility involving three genes whose protein products are in physical contact within respiratory complex I of naturally hybridizing swordtail fish species. Individuals homozygous for mismatched protein combinations do not complete embryonic development or die as juveniles, whereas those heterozygous for the incompatibility have reduced complex I function and unbalanced representation of parental alleles in the mitochondrial proteome. We find that the effects of different genetic interactions on survival are non-additive, highlighting subtle complexity in the genetic architecture of hybrid incompatibilities. Finally, we document the evolutionary history of the genes involved, showing signals of accelerated evolution and evidence that an incompatibility has been transferred between species via hybridization.

Date: 2024
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DOI: 10.1038/s41586-023-06895-8

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