Evolutionary insights from the mitochondrial genomes of invasive scale insects (Hemiptera: Coccomorpha): large-scale transfer RNA gene truncations and tandem repeat-driven intraspecific gene rearrangements

Coccomorphan mitochondrial genomes (mitogenomes) exhibit a suite of unconventional genomic features. However, the insufficient mitogenomic data from Coccomorpha, which includes numerous economically important plant pests, hampers not only the investigation of mitogenome evolution but also the molecular identification and population origin tracing of pest species. Here, we sequenced the complete mitogenomes of five invasive coccomorphans and compared the performances of short-read- and long-read-based assemblies. Moreover, the newly generated and 16 previously reported mitogenomes were subjected to comparative genomic and phylogenetic analyses. We found that an extremely high A + T content, large-scale tRNA gene truncation and frequent gene rearrangement were ubiquitous among the coccomorphan mitogenomes. Notably, our data reveal that massive tRNA arm loss and gene rearrangements provide informative phylogenetic characteristics within Coccomorpha. The rapid evolution of ATP8, driven by relaxed purifying selection, has resulted in divergent ATP8 gene lengths and relative genomic positions. Furthermore, long-read sequencing data revealed the heteroplasmic landscape of the repeat sequence copy numbers in two Icerya species, indicating that repeat sequences drive rapid intraspecific evolution of genome size, gene content, and gene rearrangement and increase mitogenomic plasticity. Our study supports the use of long-read sequencing as an efficient and useful approach for resolving complex genomic architectures and heteroplasmy. This study also identifies several potential genome-level phylogenetic markers and advances our understanding of mitogenome evolution within Coccomorpha.