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Essential, broadly conserved DNA repair pathways actively preserve genome integrity. However, many DNA repair proteins evolve adaptively. Ecological forces like UV exposure are classically cited drivers of DNA repair evolution. Intrinsic forces like repetitive DNA, which also imperil genome integrity, have received less attention. We recently reported that a Drosophila melanogaster-specific DNA satellite array triggered species-specific, adaptive evolution of a DNA repair protein called Spartan\/MH. The Spartan family of proteases cleave hazardous, covalent crosslinks that form between DNA and proteins (\u201cDNA\u2013protein crosslink repair\u201d). Appreciating that DNA satellites are both ubiquitous and universally fast-evolving, we hypothesized that satellite DNA turnover spurs adaptive evolution of DNA\u2013protein crosslink repair beyond a single gene and beyond the D. melanogaster lineage. This hypothesis predicts pervasive Spartan gene family diversification across Drosophila species. To study the evolutionary history of the Drosophila Spartan gene family, we conducted population genetic, molecular evolution, phylogenomic, and tissue-specific expression analyses. We uncovered widespread signals of positive selection across multiple Spartan family genes and across multiple evolutionary timescales. We also detected recurrent Spartan family gene duplication, divergence, and gene loss. Finally, we found that ovary-enriched parent genes consistently birthed functionally diverged, testis-enriched daughter genes. To account for Spartan family diversification, we introduce a novel mechanistic model of antagonistic coevolution that links DNA satellite evolution and adaptive regulation of Spartan protease activity. This framework promises to accelerate our understanding of how DNA repeats drive recurrent evolutionary innovation to preserve genome integrity.<\/jats:p>","DOI":"10.1093\/molbev\/msae113","type":"journal-article","created":{"date-parts":[[2024,6,12]],"date-time":"2024-06-12T04:14:38Z","timestamp":1718165678000},"source":"Crossref","is-referenced-by-count":6,"title":["Recurrent Duplication and Diversification of a Vital DNA Repair Gene Family Across Drosophila"],"prefix":"10.1093","volume":"41","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3559-1790","authenticated-orcid":false,"given":"Cara L","family":"Brand","sequence":"first","affiliation":[{"name":"Department of Biology and Epigenetics Institute, University of Pennsylvania , Philadelphia, PA 19104 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-6823-5743","authenticated-orcid":false,"given":"Genevieve 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USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4311-7535","authenticated-orcid":false,"given":"Mia T","family":"Levine","sequence":"additional","affiliation":[{"name":"Department of Biology and Epigenetics Institute, University of Pennsylvania , Philadelphia, PA 19104 , USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,6,12]]},"reference":[{"key":"2024062716343099400_msae113-B1","doi-asserted-by":"crossref","first-page":"e26176","DOI":"10.7554\/eLife.26176","article-title":"Post-meiotic DNA double-strand breaks occur in Tetrahymena, and require topoisomerase II and Spo11","volume":"6","author":"Akematsu","year":"2017","journal-title":"eLife"},{"issue":"5","key":"2024062716343099400_msae113-B2","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1093\/sysbio\/syr041","article-title":"Survey of branch support methods demonstrates accuracy, power, and robustness of 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