An integrative phylogenomic approach to elucidate the evolutionary history and divergence times of Neuropterida (Insecta: Holometabola).

Endopterygota Four-cluster likelihood mapping Megaloptera Multi-species coalescent Neuroptera RNA-seq Raphidioptera Supermatrices Transcriptomics

Journal

BMC evolutionary biology
ISSN: 1471-2148
Titre abrégé: BMC Evol Biol
Pays: England
ID NLM: 100966975

Informations de publication

Date de publication:
03 06 2020
Historique:
received: 22 10 2019
accepted: 19 05 2020
entrez: 5 6 2020
pubmed: 5 6 2020
medline: 26 9 2020
Statut: epublish

Résumé

The latest advancements in DNA sequencing technologies have facilitated the resolution of the phylogeny of insects, yet parts of the tree of Holometabola remain unresolved. The phylogeny of Neuropterida has been extensively studied, but no strong consensus exists concerning the phylogenetic relationships within the order Neuroptera. Here, we assembled a novel transcriptomic dataset to address previously unresolved issues in the phylogeny of Neuropterida and to infer divergence times within the group. We tested the robustness of our phylogenetic estimates by comparing summary coalescent and concatenation-based phylogenetic approaches and by employing different quartet-based measures of phylogenomic incongruence, combined with data permutations. Our results suggest that the order Raphidioptera is sister to Neuroptera + Megaloptera. Coniopterygidae is inferred as sister to all remaining neuropteran families suggesting that larval cryptonephry could be a ground plan feature of Neuroptera. A clade that includes Nevrorthidae, Osmylidae, and Sisyridae (i.e. Osmyloidea) is inferred as sister to all other Neuroptera except Coniopterygidae, and Dilaridae is placed as sister to all remaining neuropteran families. Ithonidae is inferred as the sister group of monophyletic Myrmeleontiformia. The phylogenetic affinities of Chrysopidae and Hemerobiidae were dependent on the data type analyzed, and quartet-based analyses showed only weak support for the placement of Hemerobiidae as sister to Ithonidae + Myrmeleontiformia. Our molecular dating analyses suggest that most families of Neuropterida started to diversify in the Jurassic and our ancestral character state reconstructions suggest a primarily terrestrial environment of the larvae of Neuropterida and Neuroptera. Our extensive phylogenomic analyses consolidate several key aspects in the backbone phylogeny of Neuropterida, such as the basal placement of Coniopterygidae within Neuroptera and the monophyly of Osmyloidea. Furthermore, they provide new insights into the timing of diversification of Neuropterida. Despite the vast amount of analyzed molecular data, we found that certain nodes in the tree of Neuroptera are not robustly resolved. Therefore, we emphasize the importance of integrating the results of morphological analyses with those of sequence-based phylogenomics. We also suggest that comparative analyses of genomic meta-characters should be incorporated into future phylogenomic studies of Neuropterida.

Sections du résumé

BACKGROUND
The latest advancements in DNA sequencing technologies have facilitated the resolution of the phylogeny of insects, yet parts of the tree of Holometabola remain unresolved. The phylogeny of Neuropterida has been extensively studied, but no strong consensus exists concerning the phylogenetic relationships within the order Neuroptera. Here, we assembled a novel transcriptomic dataset to address previously unresolved issues in the phylogeny of Neuropterida and to infer divergence times within the group. We tested the robustness of our phylogenetic estimates by comparing summary coalescent and concatenation-based phylogenetic approaches and by employing different quartet-based measures of phylogenomic incongruence, combined with data permutations.
RESULTS
Our results suggest that the order Raphidioptera is sister to Neuroptera + Megaloptera. Coniopterygidae is inferred as sister to all remaining neuropteran families suggesting that larval cryptonephry could be a ground plan feature of Neuroptera. A clade that includes Nevrorthidae, Osmylidae, and Sisyridae (i.e. Osmyloidea) is inferred as sister to all other Neuroptera except Coniopterygidae, and Dilaridae is placed as sister to all remaining neuropteran families. Ithonidae is inferred as the sister group of monophyletic Myrmeleontiformia. The phylogenetic affinities of Chrysopidae and Hemerobiidae were dependent on the data type analyzed, and quartet-based analyses showed only weak support for the placement of Hemerobiidae as sister to Ithonidae + Myrmeleontiformia. Our molecular dating analyses suggest that most families of Neuropterida started to diversify in the Jurassic and our ancestral character state reconstructions suggest a primarily terrestrial environment of the larvae of Neuropterida and Neuroptera.
CONCLUSION
Our extensive phylogenomic analyses consolidate several key aspects in the backbone phylogeny of Neuropterida, such as the basal placement of Coniopterygidae within Neuroptera and the monophyly of Osmyloidea. Furthermore, they provide new insights into the timing of diversification of Neuropterida. Despite the vast amount of analyzed molecular data, we found that certain nodes in the tree of Neuroptera are not robustly resolved. Therefore, we emphasize the importance of integrating the results of morphological analyses with those of sequence-based phylogenomics. We also suggest that comparative analyses of genomic meta-characters should be incorporated into future phylogenomic studies of Neuropterida.

Identifiants

pubmed: 32493355
doi: 10.1186/s12862-020-01631-6
pii: 10.1186/s12862-020-01631-6
pmc: PMC7268685
doi:

Banques de données

Dryad
['10.5061/dryad.1jwstqjrs']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

64

Subventions

Organisme : National Natural Science Foundation of China
ID : 31972871
Pays : International
Organisme : National Natural Science Foundation of China
ID : 31672322
Pays : International

Commentaires et corrections

Type : ErratumIn

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Auteurs

Alexandros Vasilikopoulos (A)

Centre for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, 53113, Bonn, Germany. alexvasilikop@gmail.com.

Bernhard Misof (B)

Centre for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, 53113, Bonn, Germany. b.misof@leibniz-zfmk.de.

Karen Meusemann (K)

Centre for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, 53113, Bonn, Germany.
Department of Evolutionary Biology and Ecology, Institute of Biology I (Zoology), Albert-Ludwigs-Universität Freiburg, 79104, Freiburg, Germany.
Australian National Insect Collection, National Research Collections Australia, Commonwealth Scientific and Industrial Research Organisation (CSIRO), Canberra, ACT 2601, Australia.

Doria Lieberz (D)

Centre for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, 53113, Bonn, Germany.

Tomáš Flouri (T)

Department of Genetics, Evolution and Environment, University College London, London, WC1E 6BT, UK.

Rolf G Beutel (RG)

Institut für Zoologie und Evolutionsforschung, Friedrich-Schiller-Universität Jena, 07743, Jena, Germany.

Oliver Niehuis (O)

Department of Evolutionary Biology and Ecology, Institute of Biology I (Zoology), Albert-Ludwigs-Universität Freiburg, 79104, Freiburg, Germany.

Torsten Wappler (T)

Natural History Department, Hessisches Landesmuseum Darmstadt, 64283, Darmstadt, Germany.

Jes Rust (J)

Steinmann-Institut für Geologie, Mineralogie und Paläontologie, Rheinische Friedrich-Wilhelms-Universität Bonn, 53115, Bonn, Germany.

Ralph S Peters (RS)

Centre for Taxonomy and Evolutionary Research, Arthropoda Department, Zoological Research Museum Alexander Koenig, 53113, Bonn, Germany.

Alexander Donath (A)

Centre for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, 53113, Bonn, Germany.

Lars Podsiadlowski (L)

Centre for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, 53113, Bonn, Germany.

Christoph Mayer (C)

Centre for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, 53113, Bonn, Germany.

Daniela Bartel (D)

Department of Evolutionary Biology, University of Vienna, 1090, Vienna, Austria.

Alexander Böhm (A)

Department of Evolutionary Biology, University of Vienna, 1090, Vienna, Austria.

Shanlin Liu (S)

Department of Entomology, China Agricultural University, 100193, Beijing, People's Republic of China.

Paschalia Kapli (P)

Department of Genetics, Evolution and Environment, University College London, London, WC1E 6BT, UK.

Carola Greve (C)

LOEWE Centre for Translational Biodiversity Genomics (LOEWE-TBG), 60325, Frankfurt, Germany.

James E Jepson (JE)

School of Biological, Earth and Environmental Sciences, University College Cork, Distillery Fields, North Mall, T23 N73K, Cork, Ireland.

Xingyue Liu (X)

Department of Entomology, China Agricultural University, 100193, Beijing, People's Republic of China.

Xin Zhou (X)

Department of Entomology, China Agricultural University, 100193, Beijing, People's Republic of China.

Horst Aspöck (H)

Institute of Specific Prophylaxis and Tropical Medicine, Medical Parasitology, Medical University of Vienna (MUW), 1090, Vienna, Austria.

Ulrike Aspöck (U)

Department of Evolutionary Biology, University of Vienna, 1090, Vienna, Austria.
Zoological Department II, Natural History Museum of Vienna, 1010, Vienna, Austria.

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