Massive gene rearrangements of mitochondrial genomes and implications for the phylogeny of Trichoptera (Insecta)

Mitochondrial genomes have been widely used for phylogenetic reconstruction and evolutionary analysis in various groups of Insecta. Gene rearrangements in the mitogenome can be informative characters for phylogenetic reconstruction and adaptive evolution. Trichoptera is one of the most important groups of aquatic insects. Prior to this study, complete mitogenomes from Trichoptera were restricted to eight families, resulting in a biased view of their mitogenome structure and evolution. Here, we assemble new mitogenomes for 66 species by high-throughput sequencing. The mitogenomes of 19 families and 47 genera are documented for the first time. Combined with 16 previously published mitogenomes of Trichoptera, we find 14 kinds of gene rearrangement patterns novel for Trichoptera, including rearrangement of protein-coding genes, tRNAs and control regions. Simultaneously, we provide evidence for the occurrence of tandem duplication and non-random loss events in the mitogenomes of three families. Phylogenetic analyses show that Hydroptilidae was recovered as a sister group to Annulipalpia. The increased nucleotide substitution rate and adaptive evolution may have affected the mitochondrial gene rearrangements in Trichoptera. Our study offers new insights into the mechanisms and patterns of mitogenome rearrangements in Insecta at large and into the usefulness of mitogenomic gene order as a phylogenetic marker within Trichoptera.

Automated summary

This study obtained new mitogenomes for 66 species of Trichoptera through high-throughput sequencing, documenting the mitogenomes of 19 families and 47 genera for the first time. A total of 14 novel gene rearrangement patterns in Trichoptera were discovered, including rearrangements of protein-coding genes, tRNAs, and control regions. Evidence for tandem duplication and non-random loss events in the mitogenomes of three families was also provided. Phylogenetic analysis revealed the relationship between Hydroptilidae and Annulipalpia. The increased nucleotide substitution rate and adaptive evolution may have influenced the mitochondrial gene rearrangements in Trichoptera. This study offers new insights into the mechanisms and patterns of mitogenome rearrangements in insects, as well as the usefulness of mitogenomic gene order as a phylogenetic marker within Trichoptera.