A multigene phylogeny and timeline for Trichoptera (Insecta)

Jessica A. Thomas, Paul B. Frandsen, Elizabeth Prendini, Xin Zhou, Ralph W. Holzenthal

Research output: Contribution to journalArticlepeer-review

Abstract

The Trichoptera, or caddisflies, are traditionally split into two taxonomic subdivisions: the ‘retreat-making’ Annulipalpia and the ‘case-making’ Integripalpia (sensu Ross). The monophyly of these groups is well documented; however, the establishment of a third subdivision, ‘Spicipalpia’, and the positions of the five ‘spicipalpian’ families is much debated. In contrast to previous molecular studies using nuclear ribosomal RNA, a recent trichopteran study (using nuclear protein-coding genes) placed one of these ‘spicipalpian’ families, the free-living predatory Rhyacophilidae, as the sister taxon to the rest of Trichoptera, a result that has significant implications for both the understanding of trichopteran evolution and its timing. This paper sets out to investigate the relationships of Trichoptera using several newly sequenced genes, together with previously published gene sequences. This dataset is the largest trichopteran dataset to date, covering six independent genes and > 10 000 nucleotides, and containing 185 species representing 49 families. With all data included, likelihood and Bayesian analyses support a monophyletic Annulipalpia and a monophyletic Integripalpia, which includes the ‘spicipalpians’ as a paraphyletic grade at the base of this clade. However, an analysis of the protein-coding data alone using similar analytical methods recovers Rhyacophilidae as the most basal taxon in Trichoptera, with low support. A reanalysis correcting for nucleotide composition bias provides support for the placement of the ‘spicipalpian’ taxa as sister to the Integripalpia, consistent with the total data analysis, suggesting that the basal position of Rhyacophilidae in the uncorrected analysis could be (or is probably) an artefact of base composition. We find it likely that ancestral trichopterans made incipient cases and retreats, and these had independent origins as precocious pupal chambers. Molecular dating analysis in beast, using the birth-death model of speciation, with a relaxed-clock model of sequence evolution informed by 37 fossil constraints, suggests that the most recent common ancestor of Trichoptera appeared in the Permian (c. 275 Ma) in line with the first appearance of Trichoptera in the fossil record, and that vicariance explains the distribution of most trichopteran taxa. A new infraordinal name, Phryganides, is introduced for the tube-case-making families of Integripalpia.

Original languageEnglish (US)
Pages (from-to)670-686
Number of pages17
JournalSystematic Entomology
Volume45
Issue number3
DOIs
StatePublished - Jul 1 2020

Bibliographical note

Funding Information:
We would like to thank everyone who contributed trichopteran specimens and/or knowledge to this study as part of the Trichoptera Barcode of Life project, in particular: Trond Andersen, Roger Blahnik, Nuria Bonada, Joanquin Bueno-Soria, R.E. DeWalt, Ferdy deMoor, Oliver Flint Jr., C.J. Geraci, Gisli Gislason, Marcos Gonzales, Wolfram Graf, Kathy Hill, Kjell-Arne Johanson, Hans Malicky, David Marshall, Wolfram Mey, John Morse, Sylvester Ogbogu, Steffen Pauls, Andrew Rasmussen, David Ruiter, Michael Shakleton, Brian Smith, Tatyana Vshivkova, and Carmen Zamora, as well as Karl M. Kjer as the originator of this research. In addition, we thank Paul Hebert and the Centre for Biodiversity Genomics, Guelph, Canada, where many of the samples were sequenced (funded by the Ontario Ministry of Research and Innovation and by the Government of Canada through Genome Canada). Computation was performed on the Smithsonian High Performance Cluster (SI/HPC) and the Brigham Young University Fulton Supercomputing Lab. JAT and EP were supported by an NSF grant, DEB 0816865, awarded to K.M. Kjer and RWH. PBF was supported by the Rutgers Excellence Fellowship and the Rutgers Entomology Thomas J. Headlee Fellowship. RWH was supported by Minnesota Agricultural Experiment Station projects 17-079 and 17-094. We would also like to thank Meg Woolfit and two anonymous reviewers who provided extremely helpful comments on the manuscript. The authors declare that there are no conflicts of interest, and there are no disputes over the ownership of the data presented in the paper. All contributions are attributed appropriately, and as follows: lab work was performed by JAT, EP, PBF and XZ, with computational analysis by JAT and PBF. The paper was written by JAT and RWH with contributions from all authors. Figures were prepared by RWH.

Funding Information:
We would like to thank everyone who contributed trichopteran specimens and/or knowledge to this study as part of the Trichoptera Barcode of Life project, in particular: Trond Andersen, Roger Blahnik, Nuria Bonada, Joanquin Bueno‐Soria, R.E. DeWalt, Ferdy deMoor, Oliver Flint Jr., C.J. Geraci, Gisli Gislason, Marcos Gonzales, Wolfram Graf, Kathy Hill, Kjell‐Arne Johanson, Hans Malicky, David Marshall, Wolfram Mey, John Morse, Sylvester Ogbogu, Steffen Pauls, Andrew Rasmussen, David Ruiter, Michael Shakleton, Brian Smith, Tatyana Vshivkova, and Carmen Zamora, as well as Karl M. Kjer as the originator of this research. In addition, we thank Paul Hebert and the Centre for Biodiversity Genomics, Guelph, Canada, where many of the samples were sequenced (funded by the Ontario Ministry of Research and Innovation and by the Government of Canada through Genome Canada). Computation was performed on the Smithsonian High Performance Cluster (SI/HPC) and the Brigham Young University Fulton Supercomputing Lab. JAT and EP were supported by an NSF grant, DEB 0816865, awarded to K.M. Kjer and RWH. PBF was supported by the Rutgers Excellence Fellowship and the Rutgers Entomology Thomas J. Headlee Fellowship. RWH was supported by Minnesota Agricultural Experiment Station projects 17‐079 and 17‐094. We would also like to thank Meg Woolfit and two anonymous reviewers who provided extremely helpful comments on the manuscript. The authors declare that there are no conflicts of interest, and there are no disputes over the ownership of the data presented in the paper. All contributions are attributed appropriately, and as follows: lab work was performed by JAT, EP, PBF and XZ, with computational analysis by JAT and PBF. The paper was written by JAT and RWH with contributions from all authors. Figures were prepared by RWH.

Publisher Copyright:
© 2020 The Royal Entomological Society

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