Integrated phylogenomics and fossil data illuminate the evolution of beetles

Chenyang Cai; Erik Tihelka; Mattia Giacomelli; John F. Lawrence; Adam Ślipiński; Robin Kundrata; Shûhei Yamamoto; Margaret K. Thayer; Alfred F. Newton; Richard A.B. Leschen; Matthew Gimmel; Lü Liang; Michael S. Engel; Diying Huang; Davide Pisani; Philip C J Donoghue

doi:10.1098/rsos.211771

Integrated phylogenomics and fossil data illuminate the evolution of beetles

Chenyang Cai^*
, Erik Tihelka^*
, Mattia Giacomelli
, John F. Lawrence
, Adam Ślipiński
, Robin Kundrata
, Shûhei Yamamoto
, Margaret K. Thayer
, Alfred F. Newton
, Richard A.B. Leschen
, Matthew Gimmel
, Lü Liang
, Michael S. Engel
, Diying Huang
, Davide Pisani
, Philip C J Donoghue^*

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

285 Citations (Scopus)

276 Downloads (Pure)

Abstract

Beetles constitute the most biodiverse animal order with over 380,000 described species and possibly several million more yet unnamed. Recent phylogenomic studies have arrived at considerably incongruent topologies and widely varying estimates of divergence dates for major beetle clades. Here we use a dataset of 68 single-copy nuclear protein coding genes sampling 129 out of the 193 recognized extant families as well as the first comprehensive set of fully-justified fossil calibrations to recover a refined timescale of beetle evolution. Using phylogenetic methods that counter the effects of compositional and rate heterogeneity we recover a topology congruent with morphological studies, which we use, combined with other recent phylogenomic studies, to propose several formal changes in the classification of Coleoptera: Scirtiformia and Scirtoidea sensu nov., Clambiformia ser. nov. and Clamboidea sensu nov., Rhinorhipiformia ser. nov., Byrrhoidea sensu nov., Dryopoidea stat. res., Nosodendriformia ser. nov., and Staphyliniformia sensu nov., Erotyloidea stat. nov., Nitiduloidea stat. nov., and Cucujoidea sensu nov., alongside changes below the superfamily level. Our divergence time analyses recovered a late Carboniferous origin of Coleoptera, a late Paleozoic origin of all modern beetle suborders, and a Triassic–Jurassic origin of most extant families, while fundamental divergences within beetle phylogeny did not coincide with the hypothesis of a Cretaceous Terrestrial Revolution.

Original language	English
Article number	211771
Number of pages	19
Journal	Royal Society Open Science
Volume	9
Issue number	3
DOIs	https://doi.org/10.1098/rsos.211771
Publication status	Published - 23 Mar 2022

Bibliographical note

Funding Information:
Support for the present study was provided by the Strategic Priority Research Program of the Chinese Academy of Sciences (grant nos. XDB26000000 and XDB18000000), the National Natural Science Foundation of China (grant nos. 41672011 and 41688103), the Second Tibetan Plateau Scientific Expedition and Research (grant no. 2019QZKK0706), the Biotechnology and Biological Sciences Research Council (BBSRC) (grant no. BB/T012773/1), and a Newton International Fellowship from the Royal Society awarded to C.C. and P.C.J.D. This study was partly supported by a Grant-in-Aid for JSPS Fellows (grant no. 20J00159) given to S.Y. from the Japan Society for the Promotion of Science (JSPS) and the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement (764840 to D.P. and M.L.G.). R.A.B.L. was supported in part by the Core funding for Crown Research Institutes from the Ministry of Business, Innovation and Employment's Science and Innovation Group.

Publisher Copyright:
© 2022 The Authors.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 15 Life on Land

Research Groups and Themes

MSci Palaeontology and Evolution

Keywords

Coleoptera
classification
diversification
phylogenomics
substitution modelling
CAT-GTR

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Efficient Bayesian phylogenomic dating with new models of trait evolution and rich diversities of living and fossil species
Donoghue, P. C. J. (Principal Investigator)
1/10/20 → 30/09/23
Project: Research

HPC (High Performance Computing) and HTC (High Throughput Computing) Facilities
Alam, S. R. (Manager), Williams, D. A. G. (Manager), Eccleston, P. E. (Manager) & Greene, D. (Manager)
Facility/equipment: Facility

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Cai, C., Tihelka, E., Giacomelli, M., Lawrence, J. F., Ślipiński, A., Kundrata, R., Yamamoto, S., Thayer, M. K., Newton, A. F., Leschen, R. A. B., Gimmel, M., Liang, L., Engel, M. S., Huang, D., Pisani, D., & Donoghue, P. C. J. (2022). Integrated phylogenomics and fossil data illuminate the evolution of beetles. Royal Society Open Science, 9(3), Article 211771. https://doi.org/10.1098/rsos.211771

@article{1c518af35ac949feb3a8d5c2ec77dfc3,

title = "Integrated phylogenomics and fossil data illuminate the evolution of beetles",

abstract = "Beetles constitute the most biodiverse animal order with over 380,000 described species and possibly several million more yet unnamed. Recent phylogenomic studies have arrived at considerably incongruent topologies and widely varying estimates of divergence dates for major beetle clades. Here we use a dataset of 68 single-copy nuclear protein coding genes sampling 129 out of the 193 recognized extant families as well as the first comprehensive set of fully-justified fossil calibrations to recover a refined timescale of beetle evolution. Using phylogenetic methods that counter the effects of compositional and rate heterogeneity we recover a topology congruent with morphological studies, which we use, combined with other recent phylogenomic studies, to propose several formal changes in the classification of Coleoptera: Scirtiformia and Scirtoidea sensu nov., Clambiformia ser. nov. and Clamboidea sensu nov., Rhinorhipiformia ser. nov., Byrrhoidea sensu nov., Dryopoidea stat. res., Nosodendriformia ser. nov., and Staphyliniformia sensu nov., Erotyloidea stat. nov., Nitiduloidea stat. nov., and Cucujoidea sensu nov., alongside changes below the superfamily level. Our divergence time analyses recovered a late Carboniferous origin of Coleoptera, a late Paleozoic origin of all modern beetle suborders, and a Triassic–Jurassic origin of most extant families, while fundamental divergences within beetle phylogeny did not coincide with the hypothesis of a Cretaceous Terrestrial Revolution.",

keywords = "Coleoptera, classification, diversification, phylogenomics, substitution modelling, CAT-GTR",

author = "Chenyang Cai and Erik Tihelka and Mattia Giacomelli and Lawrence, \{John F.\} and Adam {\'S}lipi{\'n}ski and Robin Kundrata and Sh{\^u}hei Yamamoto and Thayer, \{Margaret K.\} and Newton, \{Alfred F.\} and Leschen, \{Richard A.B.\} and Matthew Gimmel and L{\"u} Liang and Engel, \{Michael S.\} and Diying Huang and Davide Pisani and Donoghue, \{Philip C J\}",

note = "Funding Information: Support for the present study was provided by the Strategic Priority Research Program of the Chinese Academy of Sciences (grant nos. XDB26000000 and XDB18000000), the National Natural Science Foundation of China (grant nos. 41672011 and 41688103), the Second Tibetan Plateau Scientific Expedition and Research (grant no. 2019QZKK0706), the Biotechnology and Biological Sciences Research Council (BBSRC) (grant no. BB/T012773/1), and a Newton International Fellowship from the Royal Society awarded to C.C. and P.C.J.D. This study was partly supported by a Grant-in-Aid for JSPS Fellows (grant no. 20J00159) given to S.Y. from the Japan Society for the Promotion of Science (JSPS) and the European Union's Horizon 2020 research and innovation programme under the Marie Sk{\l}odowska-Curie grant agreement (764840 to D.P. and M.L.G.). R.A.B.L. was supported in part by the Core funding for Crown Research Institutes from the Ministry of Business, Innovation and Employment's Science and Innovation Group. Publisher Copyright: {\textcopyright} 2022 The Authors.",

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doi = "10.1098/rsos.211771",

language = "English",

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T1 - Integrated phylogenomics and fossil data illuminate the evolution of beetles

AU - Cai, Chenyang

AU - Tihelka, Erik

AU - Giacomelli, Mattia

AU - Lawrence, John F.

AU - Ślipiński, Adam

AU - Kundrata, Robin

AU - Yamamoto, Shûhei

AU - Thayer, Margaret K.

AU - Newton, Alfred F.

AU - Leschen, Richard A.B.

AU - Gimmel, Matthew

AU - Liang, Lü

AU - Engel, Michael S.

AU - Huang, Diying

AU - Pisani, Davide

AU - Donoghue, Philip C J

N1 - Funding Information: Support for the present study was provided by the Strategic Priority Research Program of the Chinese Academy of Sciences (grant nos. XDB26000000 and XDB18000000), the National Natural Science Foundation of China (grant nos. 41672011 and 41688103), the Second Tibetan Plateau Scientific Expedition and Research (grant no. 2019QZKK0706), the Biotechnology and Biological Sciences Research Council (BBSRC) (grant no. BB/T012773/1), and a Newton International Fellowship from the Royal Society awarded to C.C. and P.C.J.D. This study was partly supported by a Grant-in-Aid for JSPS Fellows (grant no. 20J00159) given to S.Y. from the Japan Society for the Promotion of Science (JSPS) and the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement (764840 to D.P. and M.L.G.). R.A.B.L. was supported in part by the Core funding for Crown Research Institutes from the Ministry of Business, Innovation and Employment's Science and Innovation Group. Publisher Copyright: © 2022 The Authors.

PY - 2022/3/23

Y1 - 2022/3/23

N2 - Beetles constitute the most biodiverse animal order with over 380,000 described species and possibly several million more yet unnamed. Recent phylogenomic studies have arrived at considerably incongruent topologies and widely varying estimates of divergence dates for major beetle clades. Here we use a dataset of 68 single-copy nuclear protein coding genes sampling 129 out of the 193 recognized extant families as well as the first comprehensive set of fully-justified fossil calibrations to recover a refined timescale of beetle evolution. Using phylogenetic methods that counter the effects of compositional and rate heterogeneity we recover a topology congruent with morphological studies, which we use, combined with other recent phylogenomic studies, to propose several formal changes in the classification of Coleoptera: Scirtiformia and Scirtoidea sensu nov., Clambiformia ser. nov. and Clamboidea sensu nov., Rhinorhipiformia ser. nov., Byrrhoidea sensu nov., Dryopoidea stat. res., Nosodendriformia ser. nov., and Staphyliniformia sensu nov., Erotyloidea stat. nov., Nitiduloidea stat. nov., and Cucujoidea sensu nov., alongside changes below the superfamily level. Our divergence time analyses recovered a late Carboniferous origin of Coleoptera, a late Paleozoic origin of all modern beetle suborders, and a Triassic–Jurassic origin of most extant families, while fundamental divergences within beetle phylogeny did not coincide with the hypothesis of a Cretaceous Terrestrial Revolution.

AB - Beetles constitute the most biodiverse animal order with over 380,000 described species and possibly several million more yet unnamed. Recent phylogenomic studies have arrived at considerably incongruent topologies and widely varying estimates of divergence dates for major beetle clades. Here we use a dataset of 68 single-copy nuclear protein coding genes sampling 129 out of the 193 recognized extant families as well as the first comprehensive set of fully-justified fossil calibrations to recover a refined timescale of beetle evolution. Using phylogenetic methods that counter the effects of compositional and rate heterogeneity we recover a topology congruent with morphological studies, which we use, combined with other recent phylogenomic studies, to propose several formal changes in the classification of Coleoptera: Scirtiformia and Scirtoidea sensu nov., Clambiformia ser. nov. and Clamboidea sensu nov., Rhinorhipiformia ser. nov., Byrrhoidea sensu nov., Dryopoidea stat. res., Nosodendriformia ser. nov., and Staphyliniformia sensu nov., Erotyloidea stat. nov., Nitiduloidea stat. nov., and Cucujoidea sensu nov., alongside changes below the superfamily level. Our divergence time analyses recovered a late Carboniferous origin of Coleoptera, a late Paleozoic origin of all modern beetle suborders, and a Triassic–Jurassic origin of most extant families, while fundamental divergences within beetle phylogeny did not coincide with the hypothesis of a Cretaceous Terrestrial Revolution.

KW - Coleoptera

KW - classification

KW - diversification

KW - phylogenomics

KW - substitution modelling

KW - CAT-GTR

U2 - 10.1098/rsos.211771

DO - 10.1098/rsos.211771

M3 - Article (Academic Journal)

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SN - 2054-5703

VL - 9

JO - Royal Society Open Science

JF - Royal Society Open Science

IS - 3

M1 - 211771

ER -

Integrated phylogenomics and fossil data illuminate the evolution of beetles

Abstract

Bibliographical note

UN SDGs

Research Groups and Themes

Keywords

Access to Document

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Projects

Efficient Bayesian phylogenomic dating with new models of trait evolution and rich diversities of living and fossil species

Equipment

HPC (High Performance Computing) and HTC (High Throughput Computing) Facilities

Cite this