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.

Highlights

  • Ernst Mayr defined evolutionary novelty as ‘any newly acquired structure or property that permits the performance of a new function, which, in turn, will open a new adaptive zone’ [1]

  • 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

  • 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 facilitated multiple independent shifts among diverse feeding habits and multiple independent colonizations of aquatic habitats

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Summary

Introduction

Ernst Mayr defined evolutionary novelty as ‘any newly acquired structure or property that permits the performance of a new function, which, in turn, will open a new adaptive zone’ [1]. With the advent of the Genomics Era, recent analyses have increasingly embraced the molecular resources to advance our understanding of the phylogeny of Hemiptera [10,11,12,13,15] Major issues such as the phylogenetic status (monophyly versus paraphyly) of Auchenorrhyncha and the position of Coleorrhyncha are still unsettled [10,12]. Our divergence time estimates were calculated for the two nucleotide and amino acid datasets using PHYLOBAYES 3.3f [38], the best fitting relaxed clock models, and the optimal tree used in the analysis of ancestral character state reconstruction.

Enicocephalomorpha water strider
Dinidoridae Acanthosomatidae
Heteropterodea Heteroptera
Aradidae feeding habit
Devonian Carboniferous
Findings
Hemiptera reveals adaptive innovations driving
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