Mitochondrial genome fragmentation is correlated with increased rates of molecular evolution

PLoS Genet. 2024 May 3;20(5):e1011266. doi: 10.1371/journal.pgen.1011266. eCollection 2024 May.

Abstract

While mitochondrial genome content and organization is quite diverse across all Eukaryotes, most bilaterian animal mitochondrial genomes (mitogenomes) exhibit highly conserved gene content and organisation, with genes typically encoded on a single circular chromosome. However, many species of parasitic lice (Insecta: Phthiraptera) are among the notable exceptions, having mitogenomes fragmented into multiple circular chromosomes. To better understand the process of mitogenome fragmentation, we conducted a large-scale genomic study of a major group of lice, Amblycera, with extensive taxon sampling. Analyses of the evolution of mitogenome structure across a phylogenomic tree of 90 samples from 53 genera revealed evidence for multiple independent origins of mitogenome fragmentation, some inferred to have occurred less than five million years ago. We leveraged these many independent origins of fragmentation to compare the rates of DNA substitution and gene rearrangement, specifically contrasting branches with fragmented and non-fragmented mitogenomes. We found that lineages with fragmented mitochondrial genomes had significantly higher rates of mitochondrial sequence evolution. In addition, lineages with fragmented mitochondrial genomes were more likely to have mitogenome gene rearrangements than those with single-chromosome mitochondrial genomes. By combining phylogenomics and mitochondrial genomics we provide a detailed portrait of mitogenome evolution across this group of insects with a remarkably unstable mitogenome structure, identifying processes of molecular evolution that are correlated with mitogenome fragmentation.

MeSH terms

  • Animals
  • DNA Fragmentation
  • DNA, Mitochondrial / genetics
  • Evolution, Molecular*
  • Gene Rearrangement
  • Genome, Mitochondrial* / genetics
  • Phthiraptera / classification
  • Phthiraptera / genetics
  • Phylogeny*

Grants and funding

TN's work was funded by project No. 22-04386O of the Czech Science Foundation (GAČR) "Coevolution of parasitic lice, their hosts and symbionts". JD was supported by the European Commission grant H2020-MSCA-IF-2019 (INTROSYM:886532). AB was supported by Czech Science Foundation (GAČR) grant Junior STAR No. 23-08010M. ADS was supported by NSF DEB-2328117. KPJ was supported by NSF DEB-1239788, NSF DEB-1925487, NSF DEB-1926919, and NSF DEB-2328118. This work was also supported by the Ministry of Education, Youth and Sports of the Czech Republic through the e-INFRA CZ infrastructure (ID:90140). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.