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Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both
Quantifying the frequency of shifts to new host plants within diverse clades of specialist herbivorous insects is critically important to understand whether and how host shifts contribute to the origin of species. Oak gall wasps (Hymenoptera: Cynipidae: Cynipini) comprise a tribe of ∼1000 species of...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley and Sons Inc.
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9541853/ https://www.ncbi.nlm.nih.gov/pubmed/35819249 http://dx.doi.org/10.1111/evo.14562 |
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author | Ward, Anna K. G. Bagley, Robin K. Egan, Scott P. Hood, Glen Ray Ott, James R. Prior, Kirsten M. Sheikh, Sofia I. Weinersmith, Kelly L. Zhang, Linyi Zhang, Y. Miles Forbes, Andrew A. |
author_facet | Ward, Anna K. G. Bagley, Robin K. Egan, Scott P. Hood, Glen Ray Ott, James R. Prior, Kirsten M. Sheikh, Sofia I. Weinersmith, Kelly L. Zhang, Linyi Zhang, Y. Miles Forbes, Andrew A. |
author_sort | Ward, Anna K. G. |
collection | PubMed |
description | Quantifying the frequency of shifts to new host plants within diverse clades of specialist herbivorous insects is critically important to understand whether and how host shifts contribute to the origin of species. Oak gall wasps (Hymenoptera: Cynipidae: Cynipini) comprise a tribe of ∼1000 species of phytophagous insects that induce gall formation on various organs of trees in the family Fagacae—primarily the oaks (genus Quercus; ∼435 sp.). The association of oak gall wasps with oaks is ancient (∼50 my), and most oak species are galled by one or more gall wasp species. Despite the diversity of both gall wasp species and their plant associations, previous phylogenetic work has not identified the strong signal of host plant shifting among oak gall wasps that has been found in other phytophagous insect systems. However, most emphasis has been on the Western Palearctic and not the Nearctic where both oaks and oak gall wasps are considerably more species rich. We collected 86 species of Nearctic oak gall wasps from most of the major clades of Nearctic oaks and sequenced >1000 Ultraconserved Elements (UCEs) and flanking sequences to infer wasp phylogenies. We assessed the relationships of Nearctic gall wasps to one another and, by leveraging previously published UCE data, to the Palearctic fauna. We then used phylogenies to infer historical patterns of shifts among host tree species and tree organs. Our results indicate that oak gall wasps have moved between the Palearctic and Nearctic at least four times, that some Palearctic wasp clades have their proximate origin in the Nearctic, and that gall wasps have shifted within and between oak tree sections, subsections, and organs considerably more often than previous data have suggested. Given that host shifts have been demonstrated to drive reproductive isolation between host‐associated populations in other phytophagous insects, our analyses of Nearctic gall wasps suggest that host shifts are key drivers of speciation in this clade, especially in hotspots of oak diversity. Although formal assessment of this hypothesis requires further study, two putatively oligophagous gall wasp species in our dataset show signals of host‐associated genetic differentiation unconfounded by geographic distance, suggestive of barriers to gene flow associated with the use of alternative host plants. |
format | Online Article Text |
id | pubmed-9541853 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | John Wiley and Sons Inc. |
record_format | MEDLINE/PubMed |
spelling | pubmed-95418532022-10-14 Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both Ward, Anna K. G. Bagley, Robin K. Egan, Scott P. Hood, Glen Ray Ott, James R. Prior, Kirsten M. Sheikh, Sofia I. Weinersmith, Kelly L. Zhang, Linyi Zhang, Y. Miles Forbes, Andrew A. Evolution Original Articles Quantifying the frequency of shifts to new host plants within diverse clades of specialist herbivorous insects is critically important to understand whether and how host shifts contribute to the origin of species. Oak gall wasps (Hymenoptera: Cynipidae: Cynipini) comprise a tribe of ∼1000 species of phytophagous insects that induce gall formation on various organs of trees in the family Fagacae—primarily the oaks (genus Quercus; ∼435 sp.). The association of oak gall wasps with oaks is ancient (∼50 my), and most oak species are galled by one or more gall wasp species. Despite the diversity of both gall wasp species and their plant associations, previous phylogenetic work has not identified the strong signal of host plant shifting among oak gall wasps that has been found in other phytophagous insect systems. However, most emphasis has been on the Western Palearctic and not the Nearctic where both oaks and oak gall wasps are considerably more species rich. We collected 86 species of Nearctic oak gall wasps from most of the major clades of Nearctic oaks and sequenced >1000 Ultraconserved Elements (UCEs) and flanking sequences to infer wasp phylogenies. We assessed the relationships of Nearctic gall wasps to one another and, by leveraging previously published UCE data, to the Palearctic fauna. We then used phylogenies to infer historical patterns of shifts among host tree species and tree organs. Our results indicate that oak gall wasps have moved between the Palearctic and Nearctic at least four times, that some Palearctic wasp clades have their proximate origin in the Nearctic, and that gall wasps have shifted within and between oak tree sections, subsections, and organs considerably more often than previous data have suggested. Given that host shifts have been demonstrated to drive reproductive isolation between host‐associated populations in other phytophagous insects, our analyses of Nearctic gall wasps suggest that host shifts are key drivers of speciation in this clade, especially in hotspots of oak diversity. Although formal assessment of this hypothesis requires further study, two putatively oligophagous gall wasp species in our dataset show signals of host‐associated genetic differentiation unconfounded by geographic distance, suggestive of barriers to gene flow associated with the use of alternative host plants. John Wiley and Sons Inc. 2022-07-18 2022-08 /pmc/articles/PMC9541853/ /pubmed/35819249 http://dx.doi.org/10.1111/evo.14562 Text en © 2022 The Authors. Evolution published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made. |
spellingShingle | Original Articles Ward, Anna K. G. Bagley, Robin K. Egan, Scott P. Hood, Glen Ray Ott, James R. Prior, Kirsten M. Sheikh, Sofia I. Weinersmith, Kelly L. Zhang, Linyi Zhang, Y. Miles Forbes, Andrew A. Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both |
title | Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both |
title_full | Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both |
title_fullStr | Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both |
title_full_unstemmed | Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both |
title_short | Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both |
title_sort | speciation in nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both |
topic | Original Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9541853/ https://www.ncbi.nlm.nih.gov/pubmed/35819249 http://dx.doi.org/10.1111/evo.14562 |
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