A lethal mitonuclear incompatibility in complex I of natural hybrids

• 成果类型: Article
• 署名作者: Moran, Benjamin M.; Payne, Cheyenne Y.; Powell, Daniel L.; Iverson, Erik N. K.; Donny, Alexandra E.; Banerjee, Shreya M.; Langdon, Quinn K.; Gunn, Theresa R.; Rodriguez-Soto, Rebecca A.; Madero, Angel; Baczenas, John J.; Kleczko, Korbin M.; Liu, Fang; Matney, Rowan; Singhal, Kratika; Leib, Ryan D.; Hernandez-Perez, Osvaldo; Corbett-Detig, Russell; Frydman, Judith; Gifford, Casey; Schartl, Manfred; Havird, Justin C.; Schumer, Molly
• 署名单位: Stanford University; University of Texas System; University of Texas Austin; Stanford University; University of California System; University of California Santa Cruz; University of California System; University of California Santa Cruz; Stanford University; Stanford University; Stanford University; Texas State University System; Texas State University San Marcos; University of Wurzburg; Howard Hughes Medical Institute
• 刊物名称: Nature
• ISSN/ISSBN: 0028-5737
• DOI: 10.1038/s41586-023-06895-8
• 发表日期: 2024-02-01
• 页码: 119-+
• 关键词: mitochondrial dysfunction; compensatory evolution; darwins corollary; genomes; hybridization; speciation; selection; genetics; insights; dna

摘要

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 hybrids(1-3). Theory predicts that hybrid incompatibilities may be more likely to arise at rapidly evolving genes(4-6) and that incompatibilities involving multiple genes should be common(7,8), 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.