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Additive genetic effects in interacting species jointly determine the outcome of caterpillar herbivory

Plant–insect interactions are common and important in basic and applied biology. Trait and genetic variation can affect the outcome and evolution of these interactions, but the relative contributions of plant and insect genetic variation and how these interact remain unclear and are rarely subject t...

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Autores principales: Gompert, Zachariah, Saley, Tara, Philbin, Casey, Yoon, Su’ad A., Perry, Eva, Sneck, Michelle E., Harrison, Joshua G., Buerkle, C. Alex, Fordyce, James A., Nice, Chris C., Dodson, Craig D., Lebeis, Sarah L., Lucas, Lauren K., Forister, Matthew L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9456756/
https://www.ncbi.nlm.nih.gov/pubmed/36037349
http://dx.doi.org/10.1073/pnas.2206052119
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author Gompert, Zachariah
Saley, Tara
Philbin, Casey
Yoon, Su’ad A.
Perry, Eva
Sneck, Michelle E.
Harrison, Joshua G.
Buerkle, C. Alex
Fordyce, James A.
Nice, Chris C.
Dodson, Craig D.
Lebeis, Sarah L.
Lucas, Lauren K.
Forister, Matthew L.
author_facet Gompert, Zachariah
Saley, Tara
Philbin, Casey
Yoon, Su’ad A.
Perry, Eva
Sneck, Michelle E.
Harrison, Joshua G.
Buerkle, C. Alex
Fordyce, James A.
Nice, Chris C.
Dodson, Craig D.
Lebeis, Sarah L.
Lucas, Lauren K.
Forister, Matthew L.
author_sort Gompert, Zachariah
collection PubMed
description Plant–insect interactions are common and important in basic and applied biology. Trait and genetic variation can affect the outcome and evolution of these interactions, but the relative contributions of plant and insect genetic variation and how these interact remain unclear and are rarely subject to assessment in the same experimental context. Here, we address this knowledge gap using a recent host-range expansion onto alfalfa by the Melissa blue butterfly. Common garden rearing experiments and genomic data show that caterpillar performance depends on plant and insect genetic variation, with insect genetics contributing to performance earlier in development and plant genetics later. Our models of performance based on caterpillar genetics retained predictive power when applied to a second common garden. Much of the plant genetic effect could be explained by heritable variation in plant phytochemicals, especially saponins, peptides, and phosphatidyl cholines, providing a possible mechanistic understanding of variation in the species interaction. We find evidence of polygenic, mostly additive effects within and between species, with consistent effects of plant genotype on growth and development across multiple butterfly species. Our results inform theories of plant–insect coevolution and the evolution of diet breadth in herbivorous insects and other host-specific parasites.
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spelling pubmed-94567562023-03-01 Additive genetic effects in interacting species jointly determine the outcome of caterpillar herbivory Gompert, Zachariah Saley, Tara Philbin, Casey Yoon, Su’ad A. Perry, Eva Sneck, Michelle E. Harrison, Joshua G. Buerkle, C. Alex Fordyce, James A. Nice, Chris C. Dodson, Craig D. Lebeis, Sarah L. Lucas, Lauren K. Forister, Matthew L. Proc Natl Acad Sci U S A Biological Sciences Plant–insect interactions are common and important in basic and applied biology. Trait and genetic variation can affect the outcome and evolution of these interactions, but the relative contributions of plant and insect genetic variation and how these interact remain unclear and are rarely subject to assessment in the same experimental context. Here, we address this knowledge gap using a recent host-range expansion onto alfalfa by the Melissa blue butterfly. Common garden rearing experiments and genomic data show that caterpillar performance depends on plant and insect genetic variation, with insect genetics contributing to performance earlier in development and plant genetics later. Our models of performance based on caterpillar genetics retained predictive power when applied to a second common garden. Much of the plant genetic effect could be explained by heritable variation in plant phytochemicals, especially saponins, peptides, and phosphatidyl cholines, providing a possible mechanistic understanding of variation in the species interaction. We find evidence of polygenic, mostly additive effects within and between species, with consistent effects of plant genotype on growth and development across multiple butterfly species. Our results inform theories of plant–insect coevolution and the evolution of diet breadth in herbivorous insects and other host-specific parasites. National Academy of Sciences 2022-08-29 2022-09-06 /pmc/articles/PMC9456756/ /pubmed/36037349 http://dx.doi.org/10.1073/pnas.2206052119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Gompert, Zachariah
Saley, Tara
Philbin, Casey
Yoon, Su’ad A.
Perry, Eva
Sneck, Michelle E.
Harrison, Joshua G.
Buerkle, C. Alex
Fordyce, James A.
Nice, Chris C.
Dodson, Craig D.
Lebeis, Sarah L.
Lucas, Lauren K.
Forister, Matthew L.
Additive genetic effects in interacting species jointly determine the outcome of caterpillar herbivory
title Additive genetic effects in interacting species jointly determine the outcome of caterpillar herbivory
title_full Additive genetic effects in interacting species jointly determine the outcome of caterpillar herbivory
title_fullStr Additive genetic effects in interacting species jointly determine the outcome of caterpillar herbivory
title_full_unstemmed Additive genetic effects in interacting species jointly determine the outcome of caterpillar herbivory
title_short Additive genetic effects in interacting species jointly determine the outcome of caterpillar herbivory
title_sort additive genetic effects in interacting species jointly determine the outcome of caterpillar herbivory
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9456756/
https://www.ncbi.nlm.nih.gov/pubmed/36037349
http://dx.doi.org/10.1073/pnas.2206052119
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