Mitochondrial phylogenomics of Hemiptera reveals adaptive innovations driving the diversification of true bugs

Abstract

Hemiptera, the largest non-holometabolous order of insects, represents approximately 7% of metazoan diversity. With extraordinary life histories and highly specialized morphological adaptations, hemipterans have exploited diverse habitats and food sources through approximately 300 Myr of evolution. To elucidate the phylogeny and evolutionary history of Hemiptera, we carried out the most comprehensive mitogenomics analysis on the richest taxon sampling to date covering all the suborders and infraorders, including 34 newly sequenced and 94 published mitogenomes. With optimized branch length and sequence heterogeneity, Bayesian analyses using a site-heterogeneous mixture model resolved the higher-level hemipteran phylogeny as (Sternorrhyncha, (Auchenorrhyncha, (Coleorrhyncha, Heteroptera))). Ancestral character state reconstruction and divergence time estimation suggest that the success of true bugs (Heteroptera) is probably due to angiosperm coevolution, but key adaptive innovations (e.g. prognathous mouthpart, predatory behaviour, and haemelytron) facilitated multiple independent shifts among diverse feeding habits and multiple independent colonizations of aquatic habitats.

Higher‐level phylogeny and evolutionary history of Pentatomomorpha (Hemiptera: Heteroptera) inferred from mitochondrial genome sequences

“…By contrast, Hua et al () analysed mitochondrial genome sequences of 13 species and recovered Lygaeoidea as the closest relative of Coreoidea, a result also obtained by Weirauch et al (). Furthermore, a sister relationship between Lygaeoidea and Pyrrhocoroidea was supported by analyses using a concatenated dataset of 21 nuclear and mitochondrial loci from 28 species (Li et al ., ) and sequences of mitochondrial genomes under site‐heterogeneous models (Song et al ., ; Li et al ., ; Yang et al ., ). These conflicting topologies may be the result of using different strategies for taxon sampling, different types of data and different phylogenetic methods (e.g.…”

“…Our results suggest that Pentatomomorpha split from Cimicomorpha 242 Ma (95% CI: 247–235 Ma), which is congruent with recent estimates based on multilocus (Wang et al ., ; Li et al ., ) and transcriptome data (Wang et al ., ). The origin of the common ancestor of Pentatomomorpha occurred during a period from 242 to 237 Ma.…”

“…Pentatomomorpha is monophyletic and comprises five superfamilies [Aradoidea, Pentatomoidea, Coreoidea, Lygaeoidea and Pyrrhocoroidea (Schaefer, 1993;Schuh & Slater, 1995)] or six superfamilies [Aradoidea, Pentatomoidea, Coreoidea, Lygaeoidea, Pyrrhocoroidea and Idiostoloidea (Henry, 1997;Weirauch et al, 2019)]. Morphological and molecular phylogenetic analyses have demonstrated broad agreement regarding the position of Aradoidea as the sister group of the rest of the Pentatomomorpha (=Trichophora) and the sister relationship between Pentatomoidea and Eutrichophora (Coreoidea + Lygaeoidea + Pyrrhocoroidea) (Henry, 1997;Li et al, 2005;Xie et al, 2005;Hua et al, 2008;Yao et al, 2012;Yuan et al, 2015;Li et al, 2016;Li et al, 2017;Weirauch et al, 2019). However, the relationships within Eutrichophora remain contentious.…”

Telomere structure in insects: A review

“…Nevertheless, Pita et al (2016) showed that the cimicomorphan family Reduviidae, namely members of the subfamily Triatominae, possessed the telomeric motif (TTAGG) n . Phylogeny and relationships within and between families of Cimicomorpha are still uncertain (Li et al, 2017;Schuh, Weirauch, & Wheeler, 2009). Nevertheless, the DNA sequence data, alone and in concert with morphology, invariably treat the Reduviidae as part of the Cimicomorpha, with Reduvioidea (Reduviidae + Pachynomidae) apparently being basal within the group (Schuh et al, 2009).…”

Repeated evolution of bacteriocytes in lygaeoid stinkbugs

“…One appropriate insect group for studying the evolution of bacteriocytes is the order Hemiptera, which is characterized by bacteriocyte-associated symbioses (hereafter, bacteriocyte symbioses) present among all four suborders Sternorrhyncha, Auchenorrhyncha, Coleorrhyncha and Heteroptera, containing over 82,000 species in total (Henry, 2017;Li et al, 2017;Sudakaran et al, 2017;Wang et al, 2017). The heteropteran stinkbug group called lygaeoid bugs (superfamily Lygaeoidea) and their intracellular symbiotic systems (Schneider, 1940;Kuechler et al, 2010Kuechler et al, , 2011Kuechler et al, , 2012Matsuura et al, 2012;Santos-Garcia et al, 2017) might be particularly suitable for studying bacteriocyte evolution.…”