Positive Correlation of the Gene Rearrangements and Evolutionary Rates in the Mitochondrial Genomes of Thrips (Insecta: Thysanoptera)

SIMPLE SUMMARY: Aeolothrips, commonly known as banded thrips, is the largest genus of the family Aeolothripidae (predatory thrips). In the current study, we sequenced the mitochondrial genome (mitogenome) of the banded thrip species Aeolothrips xinjiangensis. We found a novel gene arrangement in this mitogenome that has not been reported in Thysanoptera. By comparing the gene order and rearrangement patterns, we found seven identical gene blocks and three identical rearrangement events in two mitogenomes of banded thrips. There was marked variation in the mitochondrial gene order across thrip species, with only two conserved gene blocks shared by all 14 thrips. In addition, we found a positive correlation between the degree of gene rearrangement and evolutionary rate. Our results suggested that the mitogenomes of thrips have tended to be stable since their massive rearrangement. ABSTRACT: Extensive gene rearrangement is characteristic in the mitogenomes of thrips (Thysanoptera), but the historical process giving rise to the contemporary gene rearrangement pattern remains unclear. To better understand the evolutionary processes of gene rearrangement in the mitogenomes of thrips, we sequenced the mitogenome of the banded thrip species Aeolothrips xinjiangensis. First, we found a novel mitochondrial gene order in this species. This mitogenome is 16,947 bp in length and encodes the typical 37 coding genes (13 protein-coding genes, 22 tRNA genes, and two rRNA genes) of insects. The gene arrangement was dramatically different from the putative ancestral mitogenome, with 26 genes being translocated, eight of which were inverted. Moreover, we found a novel, conserved gene block, trnC-trnY, which has not been previously reported in the mitogenomes of thrips. With this newly assembled mitogenome, we compared mitogenome sequences across Thysanoptera to assess the evolutionary processes giving rise to the current gene rearrangement pattern in thrips. Seven identical gene blocks were shared by two sequenced banded thrip mitogenomes, while the reversal of ND2 combined with TDRL events resulted in the different gene orders of these two species. In phylogenetic analysis, the monophyly of the suborders and families of Thysanoptera was well supported. Across the gene orders of 14 thrips, only two conserved gene blocks, ATP8-ATP6 and ND4-ND4L, could be found. Correlation analysis showed that the degree of gene rearrangement was positively correlated with the non-synonymous substitution rate in thrips. Our study suggests that the mitogenomes of thrips remain stable over long evolutionary timescales after massive rearrangement during early diversification.