Is It an Ant or a Butterfly? Convergent Evolution in the Mitochondrial Gene Order of Hymenoptera and Lepidoptera

Abstract

Insect mitochondrial genomes (mtDNA) are usually double helical and circular molecules containing 37 genes that are encoded on both strands. The arrangement of the genes is not constant for all species, and produces distinct gene orders (GOs) that have proven to be diagnostic in defining clades at different taxonomic levels. In general, it is believed that distinct taxa have a very low chance of sharing identically arranged GOs. However, examples of identical, homoplastic local rearrangements occurring in distinct taxa do exist. In this study, we sequenced the complete mtDNAs of the ants Formica fusca and Myrmica scabrinodis (Formicidae, Hymenoptera) and compared their GOs with those of other Insecta. The GO of F. fusca was found to be identical to the GO of Dytrisia (the largest clade of Lepidoptera). This finding is the first documented case of an identical GO shared by distinct groups of Insecta, and it is the oldest known event of GO convergent evolution in animals. Both Hymenoptera and Lepidoptera acquired this GO early in their evolution. Using a phylogenetic approach combined with new bioinformatic tools, the chronological order of the evolutionary events that produced the diversity of the hymenopteran GOs was determined. Additionally, new local homoplastic rearrangements shared by distinct groups of insects were identified. Our study showed that local and global homoplasies affecting the insect GOs are more widespread than previously thought. Homoplastic GOs can still be useful for characterizing the various clades, provided that they are appropriately considered in a phylogenetic and taxonomic context.

Intraspecific rearrangement of mitochondrial genome suggests the prevalence of the tandem duplication-random loss (TDLR) mechanism in Quasipaa boulengeri

“…Our results indicate that the hotspot of gene rearrangement is adjacent to the origin of light-strand replication [6]. Homoplastic mitochondrial rearrangements are contiguous in the genome or they locate around the origin of replication [6, 30, 31]. Under these conditions, mitochondrial gene-orders appear susceptible to convergent or parallel evolution because of functional constraints or selective pressures [32–34].…”

The complete mitochondrial genomes of two globally invasive ants, the Argentine ant Linepithema humile and the little fire ant Wasmannia auropunctata

“…W. auropunctata differs from L. humile in that trnY is encoded on the light strand. The genomic arrangement of L. humile is identical to those of Formica fusca (Babbucci et al 2014), F. selysi (Yang et al 2016) and Leptomyrmex pallens (Berman et al 2014) (Fig. 1).…”

“…The mitochondrial genomes were assembled using the Assembly by Reduced Complexity (ARC) pipeline (http://ibest.github.io/ARC/) (Hunter et al 2015), with that of Solenopsis invicta (GenBank: HQ215538) (Gotzek et al 2010) as the reference. The resultant genomes were annotated by using the MITOS Web Server (Bernt et al 2013) and by aligning with other available formicid mitochondrial genomes (Babbucci et al 2014;Berman et al 2014;Gotzek et al 2010;Hasegawa et al 2011;Kim et al 2016;Liu et al 2016;Rodovalho et al 2014;Yang et al 2016). 2).…”

Mitochondrial genomes of four katydids (Orthoptera: Phaneropteridae): New gene rearrangements and their phylogenetic implications

“…Over long periods of evolutionary history, the gene order in the mitogenome has been relatively stable, especially regarding the arrangement of protein-coding genes and ribosomal RNA genes. Only the positions of a few transfer RNA genes are easily rearranged, particularly the positions of those close to the control region and in the tRNA gene cluster "trnA-trnR-trnN-trnS1-trnE-trnF" (Shao et al, 2001;Domes et al, 2008;Babbucci et al, 2014;San et al, 2006). The physical position of mitochondrial genes has been confirmed to influence their substitution rates (Cameron et al, 2007).…”