TY - JOUR
T1 - Phylogenomics of Ichneumonoidea (Hymenoptera) and implications for evolution of mode of parasitism and viral endogenization
AU - Sharanowski, Barbara J.
AU - Ridenbaugh, Ryan D.
AU - Piekarski, Patrick K.
AU - Broad, Gavin R.
AU - Burke, Gaelen R.
AU - Deans, Andrew R.
AU - Lemmon, Alan R.
AU - Moriarty Lemmon, Emily C.
AU - Diehl, Gloria J.
AU - Whitfield, James B.
AU - Hines, Heather M.
N1 - Funding Information:
We are deeply thankful for specimens from Michael Sharkey, David Smith, and Dave Karlsson with the Swedish Malaise Trap Project (SMTP). We thank Geoff Allen (University of Tasmania), Andrew Austin (University of Adelaide), James Adams (La Ceiba, Honduras), and Bery Josue Almendares Romero and entomological researchers at the Universidad Nacional Autónoma de Honduras for hosting during collecting trips and assisting with permits. Our grateful thanks to Davide Dal Pos and Andrés Herrera-Flórez for some specimen identifications and to Davide Dal Pos for valuable comments on manuscript drafts. A special thank-you to Andrew Bennett for many discussions about relationships across the Ichneumonidae. We thank Terry Wheeler (deceased) and Chris Buddle for organizing a collecting trip to Yukon through the Northern Biodiversity Program (Canada). We would like to thank John Heraty for providing alignments for the probe design, which increased their utility across Hymenoptera. We are grateful to Michelle Kortyna and Alyssa Bigelow at FSU’s Center for Anchored Phylogenomics for assistance with sample processing. We gratefully thank the reviewers for insightful comments that greatly improved the manuscript. Funding support for this project was provided by the Natural Sciences and Engineering Research Council (NSERC) Discovery Program to BJS; the National Science Foundation (NSF) (Award Number: DEB-1916914) to BJS and GRB.
Funding Information:
We are deeply thankful for specimens from Michael Sharkey, David Smith, and Dave Karlsson with the Swedish Malaise Trap Project (SMTP). We thank Geoff Allen (University of Tasmania), Andrew Austin (University of Adelaide), James Adams (La Ceiba, Honduras), and Bery Josue Almendares Romero and entomological researchers at the Universidad Nacional Aut?noma de Honduras for hosting during collecting trips and assisting with permits. Our grateful thanks to Davide Dal Pos and Andr?s Herrera-Fl?rez for some specimen identifications and to Davide Dal Pos for valuable comments on manuscript drafts. A special thank-you to Andrew Bennett for many discussions about relationships across the Ichneumonidae. We thank Terry Wheeler (deceased) and Chris Buddle for organizing a collecting trip to Yukon through the Northern Biodiversity Program (Canada). We would like to thank John Heraty for providing alignments for the probe design, which increased their utility across Hymenoptera. We are grateful to Michelle Kortyna and Alyssa Bigelow at FSU's Center for Anchored Phylogenomics for assistance with sample processing. We gratefully thank the reviewers for insightful comments that greatly improved the manuscript. Funding support for this project was provided by the Natural Sciences and Engineering Research Council (NSERC) Discovery Program to BJS; the National Science Foundation (NSF) (Award Number: DEB-1916914) to BJS and GRB.
Publisher Copyright:
© 2020 The Authors
PY - 2021/3
Y1 - 2021/3
N2 - Ichneumonoidea is one of the most diverse lineages of animals on the planet with >48,000 described species and many more undescribed. Parasitoid wasps of this superfamily are mostly beneficial insects that attack and kill other arthropods and are important for understanding diversification and the evolution of life history strategies related to parasitoidism. Further, some lineages of parasitoids within Ichneumonoidea have acquired endogenous virus elements (EVEs) that are permanently a part of the wasp's genome and benefit the wasp through host immune disruption and behavioral control. Unfortunately, understanding the evolution of viral acquisition, parasitism strategies, diversification, and host immune disruption mechanisms, is deeply limited by the lack of a robust phylogenetic framework for Ichneumonoidea. Here we design probes targeting 541 genes across 91 taxa to test phylogenetic relationships, the evolution of parasitoid strategies, and the utility of probes to capture polydnavirus genes across a diverse array of taxa. Phylogenetic relationships among Ichneumonoidea were largely well resolved with most higher-level relationships maximally supported. We noted codon use biases between the outgroups, Braconidae, and Ichneumonidae and within Pimplinae, which were largely solved through analyses of amino acids rather than nucleotide data. These biases may impact phylogenetic reconstruction and caution for outgroup selection is recommended. Ancestral state reconstructions were variable for Braconidae across analyses, but consistent for reconstruction of idiobiosis/koinobiosis in Ichneumonidae. The data suggest many transitions between parasitoid life history traits across the whole superfamily. The two subfamilies within Ichneumonidae that have polydnaviruses are supported as distantly related, providing strong evidence for two independent acquisitions of ichnoviruses. Polydnavirus capture using our designed probes was only partially successful and suggests that more targeted approaches would be needed for this strategy to be effective for surveying taxa for these viral genes. In total, these data provide a robust framework for the evolution of Ichneumonoidea.
AB - Ichneumonoidea is one of the most diverse lineages of animals on the planet with >48,000 described species and many more undescribed. Parasitoid wasps of this superfamily are mostly beneficial insects that attack and kill other arthropods and are important for understanding diversification and the evolution of life history strategies related to parasitoidism. Further, some lineages of parasitoids within Ichneumonoidea have acquired endogenous virus elements (EVEs) that are permanently a part of the wasp's genome and benefit the wasp through host immune disruption and behavioral control. Unfortunately, understanding the evolution of viral acquisition, parasitism strategies, diversification, and host immune disruption mechanisms, is deeply limited by the lack of a robust phylogenetic framework for Ichneumonoidea. Here we design probes targeting 541 genes across 91 taxa to test phylogenetic relationships, the evolution of parasitoid strategies, and the utility of probes to capture polydnavirus genes across a diverse array of taxa. Phylogenetic relationships among Ichneumonoidea were largely well resolved with most higher-level relationships maximally supported. We noted codon use biases between the outgroups, Braconidae, and Ichneumonidae and within Pimplinae, which were largely solved through analyses of amino acids rather than nucleotide data. These biases may impact phylogenetic reconstruction and caution for outgroup selection is recommended. Ancestral state reconstructions were variable for Braconidae across analyses, but consistent for reconstruction of idiobiosis/koinobiosis in Ichneumonidae. The data suggest many transitions between parasitoid life history traits across the whole superfamily. The two subfamilies within Ichneumonidae that have polydnaviruses are supported as distantly related, providing strong evidence for two independent acquisitions of ichnoviruses. Polydnavirus capture using our designed probes was only partially successful and suggests that more targeted approaches would be needed for this strategy to be effective for surveying taxa for these viral genes. In total, these data provide a robust framework for the evolution of Ichneumonoidea.
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U2 - 10.1016/j.ympev.2020.107023
DO - 10.1016/j.ympev.2020.107023
M3 - Article
C2 - 33253830
AN - SCOPUS:85097732577
SN - 1055-7903
VL - 156
JO - Molecular Phylogenetics and Evolution
JF - Molecular Phylogenetics and Evolution
M1 - 107023
ER -