Revisiting habitat and lifestyle transitions in Heteroptera (Insecta: Hemiptera): insights from a combined morphological and molecular phylogeny

Abstract

Heteroptera, the true bugs, are part of the largest clade of non-holometabolous insects, the Hemiptera, and include > 42 000 described species in about 90 families. Despite progress in resolving phylogenetic relationships between and within infraorders since the first combined morphological and molecular analysis published in 1993 (29 taxa, 669 bp, 31 morphological characters), recent hypotheses have relied entirely on molecular data. Weakly supported nodes along the backbone of Heteroptera made these published phylogenies unsuitable for investigations into the evolution of habitats and lifestyles across true bugs. Here we present the first combined morphological and molecular analyses of Heteroptera since 1993, using 135 taxa in 60 families, 4018 aligned bp of ribosomal DNA and 81 morphological characters, and various analytical approaches. The sister-group relationship of the predominantly aquatic Nepomorpha with all remaining Heteroptera is supported in all analyses, and a clade formed by Enicocephalomorpha, Dipsocoromorpha and Gerromorpha in some. All analyses recover Leptopodomorpha + (Cimicomorpha + Pentatomomorpha), mostly with high support. Parsimony-and likelihood-based ancestral state reconstructions of habitats and lifestyles on the combined likelihood phylogeny provide new insights into the evolution of true bugs. The results indicate that aquatic and semi-aquatic true bugs invaded these habitats three times independently from terrestrial habitats in contrast to a recent hypothesis. They further suggest that the most recent common ancestor of Heteroptera was predacious, and that the two large predominantly phytophagous clades (Trichophora and Miroidea) are likely to have derived independently from predatory ancestors. We conclude that by combining morphological and molecular data and employing various analytical methods our analyses have converged on a relatively well-supported hypothesis of heteropteran infraordinal relationships that now requires further testing using phylogenomic and more extensive morphological datasets.

Phylogenomic analysis suggests Coreidae and Alydidae (Hemiptera: Heteroptera) are not monophyletic

“…The monophyly of the Coreoidea has largely been supported by previous phylogenetic studies (Table ), although, as in our case, most have not included Stenocephalidae and Hyocephalidae. That we strongly recovered monophyly of Coreoidea suggests that in those cases where monophyly has not been supported, it may be due to limited power (too few characters), loci selected (e.g., leading to gene trees that may not have matched the species tree or with little power to resolve short internodes), sequence quality, or analytical approaches employed (Li et al, ; Xie, Bu, & Zheng, ; Weirauch et al, ; see Tian et al () for explanation of issues in some previous analyses). As putative sister group sampling increases, previous hypotheses on morphological apomorphies for Coreoidea, such as those proposed by Li (; excluding Stenocephalidae and Hyocephalidae) and Henry (), can be better evaluated.…”

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

“…The relationships among Coreoidea, Lygaeoidea and Pyrrhocoroidea (Eutrichophora) remain more contentious: Henry (1997) established a close relationship between Coreoidea and Pyrrhocoroidea based on morphological characters, which was also supported by molecular analyses of 27 species using six Hox genes (Tian et al, 2011) and 25 species using mitochondrial genome sequences under homogeneous models (Yuan et al, 2015). By contrast, Hua et al (2008) analysed mitochondrial genome sequences of 13 species and recovered Lygaeoidea as the closest relative of Coreoidea, a result also obtained by Weirauch et al (2019). 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, 2016) and sequences of mitochondrial genomes under site-heterogeneous models (Song et al, 2016a;Li et al, 2017;Yang et al, 2018).…”

“…sequence length) and additional genes improved the resolution of the phylogenetic analyses. However, different molecular markers and phylogenetic methods produced contradictory relationships within Eutrichophora: phylogenetic analyses based on six Hox gene fragments supported the relationship (Lygaeoidea + (Coreoidea + Pyrrhocoroidea)) (Tian et al, 2011); analysis of a concatenated dataset (18S rRNA, 28S rRNA, Hox, and mitochondrial genes totaling 21 loci and 12 528 bp) supported the relationship (Coreoidea + (Lygaeoidea + Pyrrhocoroidea)) (Li et al, 2016); and analysis of combined morphological and molecular data supported the relationship (Pyrrhocoroidea + (Lygaeoidea + Coreoidea)) (Weirauch et al, 2019). Topological conflicts have frequently resulted from mitochondrial phylogenomic studies, e.g.…”

“…The bugs are economically important in agriculture and forestry as they exploit host plant resources from the roots to the seeds (Weirauch & Schuh, 2011). 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).…”

Repeated evolution of bacteriocytes in lygaeoid stinkbugs

“…In the suborder Heteroptera, the observations of bacteriocytes and bacteriomes are rather exceptional, in contrast to their prevalence in the other hemipteran suborders. Presumably, the ancestor of the stink bugs lost the bacteriocyte symbiosis in association with the evolution of predatory lifestyles (Matsuura et al, 2015;Ohbayashi et al, 2015;Weirauch et al, 2019). Only within bed bugs (Cimicoidea; Cimicidae) and in several lineages of lygaeoid bugs (Lygaeoidea), bacteriocyte symbioses appeared again long after the expansion into new ecological niches such as vertebrate blood feeding or plant sap/seed feeding lifestyles.…”