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Delimiting the cryptic diversity and host preferences of Sycophila parasitoid wasps associated with oak galls using phylogenomic data

View ORCID ProfileY. Miles Zhang, View ORCID ProfileSofia I. Sheikh, View ORCID ProfileAnna K.G. Ward, View ORCID ProfileAndrew A. Forbes, Kirsten M. Prior, View ORCID ProfileGraham N. Stone, View ORCID ProfileMichael W. Gates, Scott P. Egan, View ORCID ProfileLinyi Zhang, Charles Davis, View ORCID ProfileKelly L. Weinersmith, George Melika, View ORCID ProfileAndrea Lucky
doi: https://doi.org/10.1101/2022.01.21.477213
Y. Miles Zhang
1Systematic Entomology Laboratory, USDA-ARS, c/o National Museum of Natural History, Washington, DC, USA
2Entomology and Nematology Department, University of Florida, Gainesville, FL, USA
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  • For correspondence: Yuanmeng.zhang@gmail.com
Sofia I. Sheikh
3Department of Biology, University of Iowa, Iowa City, IA, 52242, USA
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Anna K.G. Ward
3Department of Biology, University of Iowa, Iowa City, IA, 52242, USA
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Andrew A. Forbes
3Department of Biology, University of Iowa, Iowa City, IA, 52242, USA
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Kirsten M. Prior
4Department of Biological Sciences, Binghamton University, Binghamton, NY, USA
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Graham N. Stone
5Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, UK
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Michael W. Gates
1Systematic Entomology Laboratory, USDA-ARS, c/o National Museum of Natural History, Washington, DC, USA
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Scott P. Egan
6Department of BioSciences, Rice University, Houston, TX, USA
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Linyi Zhang
6Department of BioSciences, Rice University, Houston, TX, USA
7Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON, Canada
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Charles Davis
6Department of BioSciences, Rice University, Houston, TX, USA
8Department of Entomology, Pennsylvania State University, University Park, PA, USA
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Kelly L. Weinersmith
6Department of BioSciences, Rice University, Houston, TX, USA
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George Melika
9Plant Health and Molecular Biology Laboratory, Directorate of Plant Protection, Budapest, Hungary
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Andrea Lucky
2Entomology and Nematology Department, University of Florida, Gainesville, FL, USA
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Abstract

Cryptic species diversity is a major challenge for the species-rich community of parasitoids attacking oak gall wasps due to a high degree of sexual dimorphism, morphological plasticity, small size, and poorly known biology. As such, we know very little about the number of species present, nor the evolutionary forces responsible for generating this diversity. One hypothesis is that trait diversity in the gall wasps, including the morphology of the galls they induce, has evolved in response to selection imposed by the parasitoid community, with reciprocal selection driving diversification of the parasitoids. Using a rare, continental-scale data set of Sycophila parasitoid wasps reared from 44 species of cynipid galls from 18 species of oak across the US, we combined mitochondrial DNA barcodes, Ultraconserved Elements (UCEs), morphological, and natural history data to delimit putative species. Using these results, we generate the first large-scale assessment of ecological specialization and host association in this species-rich group, with implications for evolutionary ecology and biocontrol. We find most Sycophila target specific subsets of available cynipid host galls with similar morphologies, and generally attack larger galls. Our results suggest that parasitoid wasps such as Sycophila have adaptations allowing them to exploit particular host trait combinations, while hosts with contrasting traits are resistant to attack. These findings support the tritrophic niche concept for the structuring of plant-herbivore-parasitoid communities.

Competing Interest Statement

The authors have declared no competing interest.

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Delimiting the cryptic diversity and host preferences of Sycophila parasitoid wasps associated with oak galls using phylogenomic data
Y. Miles Zhang, Sofia I. Sheikh, Anna K.G. Ward, Andrew A. Forbes, Kirsten M. Prior, Graham N. Stone, Michael W. Gates, Scott P. Egan, Linyi Zhang, Charles Davis, Kelly L. Weinersmith, George Melika, Andrea Lucky
bioRxiv 2022.01.21.477213; doi: https://doi.org/10.1101/2022.01.21.477213
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Delimiting the cryptic diversity and host preferences of Sycophila parasitoid wasps associated with oak galls using phylogenomic data
Y. Miles Zhang, Sofia I. Sheikh, Anna K.G. Ward, Andrew A. Forbes, Kirsten M. Prior, Graham N. Stone, Michael W. Gates, Scott P. Egan, Linyi Zhang, Charles Davis, Kelly L. Weinersmith, George Melika, Andrea Lucky
bioRxiv 2022.01.21.477213; doi: https://doi.org/10.1101/2022.01.21.477213

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