Hybrid lizards with introgressed MtDNA show increased resistance to DNA damage from reactive oxygen species

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Hybrids can experience genetic incompatibilities that lead to cellular dysfunction and infertility. Selection against hybrids can reinforce species boundaries, while compensatory mechanisms that support hybrid survival can lead to gene flow across species boundaries. Previous analyses of mitochondrial function of the hybrid lizards between Urosaurus graciosus and Urosaurus ornatus, which have introgressed mtDNA, showed evidence of mitochondrial dysfunction (e.g. higher oxygen consumption during ATP production) likely leading to higher reactive oxygen species (ROS) production, one of the main causes of damage to DNA. Hybrid populations of these lizards have persisted so we predicted they may have mechanisms for protecting their DNA from damage. To test this hypothesis, we exposed liver cells of these lizards to hydrogen peroxide, a source of ROS, and compared DNA damage using single-cell gel electrophoresis. Cells from hybrid individuals showed significantly less DNA damage. We then examined potential mechanisms to explain this result by comparing melanin content of livers and expression levels of antioxidant and DNA repair genes using gene set enrichment analyses. Melanin content of livers was highly variable among U. graciosus individuals and therefore not highest in hybrids as expected but was lowest in the U. ornatus which had the highest levels of DNA damage. The overall gene expression profiles of hybrids and U. graciosus were very similar while that of the mtDNA donor species, U. ornatus, was highly divergent from both. Three DNA repair and antioxidant related gene sets showed significant levels of enrichment in hybrids (Reactome gap filling DNA repair synthesis and ligation in global genome nucleotide excision repair, Glutathione metabolism, and GOMF Antioxidant activity). Antioxidant genes contributing to high enrichment scores in multiple gene sets in hybrids warrant further study. These results show how species can compensate for mtDNA introgression and highlight the complexity of genetic interactions encountered when closely related species exchange genetic material in zones of secondary contact.