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

Abstract

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 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.

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

“…L. melissa caterpillars generally spend 20 to 30 d as larvae ( 17 ), and weight and lifetime fecundity are highly correlated in L. melissa ( 26 ). We then considered the following nine performance metrics: 8-d caterpillar weight (milligrams), 14-d caterpillar weight (milligrams), weight at pupation (milligrams), survival to 8 d (binary), survival to 14 d (binary), survival to pupation (binary), survival to adult (binary), total survival time (integer-valued), and truncated survival time (integer-valued) ( 55 ). For truncated survival time, we truncated survival at the maximum number of days required for any of the caterpillars to reach eclosion; this avoids caterpillars that developed slowly, but never pupated or eclosed, from having longer survival times than the caterpillars that successfully eclosed as adults.…”

“…We measured a series of morphological traits potentially associated with plant vigor or resistance to insects (e.g., putative structural plant defenses) ( 17 , 74 , 75 ) for each of the 1,080 M. sativa plants in the Greenville Experimental Farm common garden: plant height, leaf length, leaf width, leaf area, leaf shape, leaf weight, SLA, leaf toughness, trichome density, levels of herbivory on the plants in the field, and 1,750 plant chemistry metabolites, which were quantified and characterized by using LC-MS. See SI Appendix , Plant Trait Measurements and Sample Extraction and Phytochemical Analysis for details ( 55 ). We further annotated the 20 phytochemicals that were most strongly associated with caterpillar performance ( SI Appendix , Structural Annotations of Phytochemicals ).…”

“…PRJNA866185 , PRJNA866184 , PRJNA866152 , and PRJNA866133 ) ( 57 – 60 ). Phenotypic data are available from Dryad ( https://doi.org/10.5061/dryad.cvdncjt6x ) ( 55 ). Computer scripts are available from GitHub ( https://github.com/zgompert/DimensionsExperiment ) ( 76 ).…”

Host association, environment, and geography underlie genomic differentiation in a major forest pest

“…Additionally, genomic regions that appear neutral may still be under selection if selection acts upon highly polygenic traits, such that signatures of selection on individual genomic regions are too small to be detected (Balkenhol et al, 2017 ). Genomic architectures of complex traits, such as those related to host association, are increasingly recognized as polygenic in nature and may be associated with genomic variants besides single nucleotide substitutions (Allio et al, 2021 ; Boyle et al, 2017 ; Doellman & Feder, 2019 ; Gompert et al, 2015 , 2022 ; Sella & Barton, 2019 ; Vertacnik & Linnen, 2017 ). For example, structural rearrangements, gene amplifications, and transposable element insertions underpin an adaptive host shift in the aphid pest Myzus persicae (Singh et al, 2020 ), which encompassed both widespread and localized mutational events.…”