Satellite DNA dynamics across phylogenetic scales in ground beetles and other insects

Abstract

Satellite DNAs (satDNAs) are tandemly repeated sequences that can comprise large fractions of eukaryotic genomes. For decades, we have known that satellite DNAs are among the most rapidly evolving genomic components, yet few studies have examined their dynamics across broad evolutionary frameworks--likely in part because their rapid evolution complicates or precludes homology identification. We investigated satDNA dynamics across 50 ground beetle (Carabidae) species, sampling above and below the species level in the subgenus Plataphus of Bembidion. We used RepeatExplorer2 and a novel homology detection pipeline, which we validated using species of Drosophila for which satDNAs are well-documented, to study satDNA dynamics in a comparative framework. We show that satDNAs comprise large genomic fractions (mean = 25.7%, range = 3.2%-53%), with individual satDNA motifs accounting for >30% of total DNA within some species. We quantify major satDNA turnover among closely related species which drives extensive repatterning of repeat content over short evolutionary scales. To place our findings in a broader context, we also surveyed satDNA diversity across the beetle suborder (Adephaga), the beetle order (Coleoptera), and the next six largest insect orders (Lepidoptera, Diptera, Hymenoptera, Hemiptera, Orthoptera, Trichoptera), representing 400 additional species. While satDNA abundance was significantly elevated in the focal subgenus (Plataphus), high genomic proportions were also found in species across Adephaga, Coleoptera, Hymenoptera, and Diptera. Conversely, satDNA proportions were notably reduced in Lepidoptera and Trichoptera. Our investigation of satDNA dynamics at narrow and broad taxonomic scales provides a quantitative illustration of satDNA turnover across a well-sampled clade. It also identifies new high-potential systems for gaining mechanistic insights into the drivers and impacts of satDNA evolution, and raises questions regarding potential links between satDNA turnover, speciation, and core strategies of chromosome and genome architecture in diverse clades.