Phylogeny and evolution of hemipteran insects based on expanded genomic and transcriptomic data

Nan Song; Miao-Miao Wang; Wei-Chao Huang; Zhi-Yi Wu; Renfu Shao; Xin-Ming Yin

doi:10.1186/s12915-024-01991-1

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Phylogeny and evolution of hemipteran insects based on expanded genomic and transcriptomic data

Journal article

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Phylogeny and evolution of hemipteran insects based on expanded genomic and transcriptomic data

Nan Song, Miao-Miao Wang, Wei-Chao Huang, Zhi-Yi Wu, Renfu Shao and Xin-Ming Yin

BMC Biology, Vol.22, pp.1-16

2024

DOI: https://doi.org/10.1186/s12915-024-01991-1

PMCID: PMC11367992

PMID: 39218865

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Abstract

Hemiptera

Cicadomorpha

Phylogenomics

Single‑copy nuclear gene

Background Hemiptera is the fifth species-rich order of insects and the most species-rich order of hemimetabolous insects, including numerous insect species that are of agricultural or medical significance. Despite much effort and recent advance in inferring the Hemiptera phylogeny, some high-level relationships among superfamilies remain controversial. Results We sequenced the genomes of 64 hemipteran species from 15 superfamilies and the transcriptomes of two additional scale insect species, integrating them with existing genomic and transcriptomic data to conduct a comprehensive phylogenetic analysis of Hemiptera. Our datasets comprise an average of 1625 nuclear loci of 315 species across 27 superfamilies of Hemiptera. Our analyses supported Cicadoidea and Cercopoidea as sister groups, with Membracoidea typically positioned as the sister to Cicadoidea + Cercopoidea. In most analyses, Aleyrodoidea was recovered as the sister group of all other Sternorrhyncha. A sister-group relationship was supported between Coccoidea and Aphidoidea + Phylloxeroidea. These relationships were further supported by four-cluster likelihood mapping analyses across diverse datasets. Our ancestral state reconstruction indicates phytophagy as the primary feeding strategy for Hemiptera as a whole. However, predation likely represents an ancestral state for Heteroptera, with several phytophagous lineages having evolved from predatory ancestors. Certain lineages, like Lygaeoidea, have undergone a reversal transition from phytophagy to predation. Our divergence time estimation placed the diversification of hemipterans to be between 60 and 150 million years ago. Conclusions By expanding phylogenomic taxon sampling, we clarified the superfamily relationships within the infraorder Cicadomorpha. Our phylogenetic analyses supported the sister-group relationship between the superfamilies Cicadoidea and Cercopoidea, and the superfamily Membracoidea as the sister to Cicadoidea + Cercopoidea. Our divergence time estimation supported the close association of hemipteran diversification with the evolutionary success and adaptive radiation of angiosperms during the Cretaceous period.

Details

Title: Phylogeny and evolution of hemipteran insects based on expanded genomic and transcriptomic data
Authors: Nan Song (Author) - University of the Sunshine Coast, Queensland, Centre for Bioinnovation
Miao-Miao Wang (Author) - Henan Agricultural University
Wei-Chao Huang (Author) - Hangzhou Xiaoshan Airport Customs
Zhi-Yi Wu (Author) - Zhejiang Academy of Science & Technology for Inspection & Quarantine
Renfu Shao (Corresponding Author) - University of the Sunshine Coast, Queensland, Centre for Bioinnovation
Xin-Ming Yin (Corresponding Author) - Henan Agricultural University
Publication details: BMC Biology, Vol.22, pp.1-16
Publisher: BioMed Central Ltd.
Date published: 2024
DOI: 10.1186/s12915-024-01991-1
ISSN: 1741-7007
PMID: 39218865; PMC11367992
Copyright note: This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Data Availability: Raw Illumina reads have been deposited at the NCBI Sequence Read Archive (BioProject ID: PRJNA960956). The accession numbers for the whole-genome and transcriptome sequencing data obtained in this study are listed in Additional file 2: Table S1.
Grant note: This study was supported by the Earmarked Fund for China Agriculture Research System (NO. CARS-27) and National Natural Science Foundation of China (U1904104).
Organisation Unit: School of Science, Technology and Engineering; Centre for Bioinnovation
Language: English
Record Identifier: 991058098502621
Output Type: Journal article

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