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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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2022-09, Vol.119 (36), p.e2206052119-e2206052119
Main Authors: 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
Format: Article
Language:English
Subjects:
Alfalfa
Animals
Biological evolution
Biological Sciences
Butterflies & moths
Butterflies - genetics
Caterpillars
Coevolution
Gardens & gardening
Genetic diversity
Genetic effects
Genetics
Genotype
Genotypes
Herbivory
Herbivory - genetics
Insects
Larva
Parasites
Peptides
Plants - genetics
Polygenic inheritance
Range extension
Saponins
Species
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Summary: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.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2206052119