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

Hu Li; John M. Leavengood; Eric G. Chapman; Daniel Burkhardt; Fan Song; Pei Jiang; Jinpeng Liu; Xuguo Zhou; Wanzhi Cai

doi:10.1098/rspb.2017.1223

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

Hu Li
, John M. Leavengood
, Eric G. Chapman
, Daniel Burkhardt
, Fan Song
, Pei Jiang
, Jinpeng Liu
, Xuguo Zhou
, Wanzhi Cai

Producción científica: Article › revisión exhaustiva

287 Citas (Scopus)

Resumen

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.

Idioma original	English
Número de artículo	20171223
Publicación	Proceedings of the Royal Society B: Biological Sciences
Volumen	284
N.º	1862
DOI	https://doi.org/10.1098/rspb.2017.1223
Estado	Published - sept 13 2017

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Publisher Copyright:
© 2017 The Authors.

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pteran insects have been deposited in GenBank (accession numbers shown in electronic supplementary material, table S1). The data supporting this article have been uploaded as the electronic supplementary material and the datasets used in the phylogenetic analyses are available in the Dryad Digital Repository: http://dx. doi.org/10.5061/dryad.13m7r [58]. Authors’ contributions. H.L., X.Z., and W.C. designed this study. H.L., F.S., and P.J. collected insect materials and performed the molecular experiments. H.L., E.C., F.S., and J.P.L. analysed the data. All authors discussed results and implications and read and approved the final manuscript. H.L., J.L., E.C., D.B., X.Z., and W.C. wrote the manuscript. Competing interests. We declare no competing interests. Funding. This work was supported by grants from the National Natural Science Foundation of China (nos. 31372229, 31401991 and 31420103902), the National Basic Research Program of China (no. 2013CB127600), the Chinese Universities Scientific Fund (nos. 2017QC100, 2017QC066 and 2017ZB002), and a start-up fund from the University of Kentucky. The information reported in this paper (no. 17-08-055) is part of a project of the Kentucky Agricultural Experiment Station and is published with the approval of the Director. These agencies had no role in study design, data collection/ analysis, manuscript preparation, or the decision to publish. Acknowledgements. We thank Tadashi Ishikawa (University of Tokyo, Japan) for providing samples of Dipsocoromorpha. We also thank Drs Thomas J. Henry (United States National Museum of Natural History, USA), Christiane Weirauch (University of California, USA), Guanyang Zhang (Arizona State University, USA), David Weisrock and John J. Obrycki (University of Kentucky, USA), Nicole Gunter

Financiadores	Número del financiador
University of Kentucky
National Natural Science Foundation of China (NSFC)	31372229, 31401991, 31420103902
National Natural Science Foundation of China (NSFC)
Chinese Universities Scientific Fund	2017ZB002, 2017QC066, 2017QC100
Chinese Universities Scientific Fund
National Basic Research Program of China (973 Program)	2013CB127600
National Basic Research Program of China (973 Program)

ASJC Scopus subject areas

General Immunology and Microbiology
General Biochemistry, Genetics and Molecular Biology
General Environmental Science
General Agricultural and Biological Sciences

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10.1098/rspb.2017.1223

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title = "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.",

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author = "Hu Li and Leavengood, \{John M.\} and Chapman, \{Eric G.\} and Daniel Burkhardt and Fan Song and Pei Jiang and Jinpeng Liu and Xuguo Zhou and Wanzhi Cai",

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doi = "10.1098/rspb.2017.1223",

language = "English",

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AU - Li, Hu

AU - Leavengood, John M.

AU - Chapman, Eric G.

AU - Burkhardt, Daniel

AU - Song, Fan

AU - Jiang, Pei

AU - Liu, Jinpeng

AU - Zhou, Xuguo

AU - Cai, Wanzhi

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N2 - 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.

AB - 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.

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KW - Mitochondrial genome

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

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