Abstract

Phenotypic variability results from interactions between genotype and environment and is a major driver of ecological and evolutionary interactions. Measuring the relative contributions of genetic variation, the environment, and their interaction to phenotypic variation remains a fundamental goal of evolutionary ecology.In this study, we assess the question: How do genetic variation and local environmental conditions interact to influence phenotype within a single population? We explored this question using seed from a single population of common milkweed, Asclepias syriaca, in northern Michigan. We first measured resistance and resistance traits of 14 maternal lines in two common garden experiments (field and greenhouse) to detect genetic variation within the population. We carried out a reciprocal transplant experiment with three of these maternal lines to assess effects of local environment on phenotype. Finally, we compared the phenotypic traits measured in our experiments with the phenotypic traits of the naturally growing maternal genets to be able to compare relative effect of genetic and environmental variation on naturally occurring phenotypic variation. We measured defoliation levels, arthropod abundances, foliar cardenolide concentrations, foliar latex exudation, foliar carbon and nitrogen concentrations, and plant growth.We found a striking lack of correlation in trait expression of the maternal lines between the common gardens, or between the common gardens and the naturally growing maternal genets, suggesting that environment plays a larger role in phenotypic trait variation of this population. We found evidence of significant genotype‐by‐environment interactions for all traits except foliar concentrations of nitrogen and cardenolide. Milkweed resistance to chewing herbivores was associated more strongly with the growing environment. We observed no variation in foliar cardenolide concentrations among maternal lines but did observe variation among maternal lines in foliar latex exudation.Overall, our data reveal powerful genotype‐by‐environment interactions on the expression of most resistance traits in milkweed.

Highlights

  • Phenotypic variability, resulting from both genotype and environment, drives many ecological and evolutionary processes (Via & Lande 1985; Hahn et al 2019; Zirbel & Brudvig 2020)

  • Drivers of Variation in Defoliation Maternal lines grown in the field common garden expressed genetic variation for resistance, accumulating defoliation at different rates (Week*Maternal line, F13, 2746 = 2.30, P = 0.0051, Figure 2a)

  • Defoliation of the maternal lines in the field common garden was uncorrelated with defoliation experienced by their naturally-growing maternal genets (y = -0.146x + 4.2767, R2 = 0.0056, P = 0.7992), suggesting that there may be determinants of resistance in addition to genetic variation, for naturally-growing milkweeds

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Summary

Introduction

Phenotypic variability, resulting from both genotype and environment, drives many ecological and evolutionary processes (Via & Lande 1985; Hahn et al 2019; Zirbel & Brudvig 2020). Plant-herbivore interactions provide interesting systems for investigating the causes and consequences of phenotypic variation because they are ubiquitous in terrestrial systems and mediate numerous indirect effects with other herbivores (Ali & Agrawal 2014), pollinators (Moreira et al 2019), soil microbial associates (Peschel et al 2015) and other trophic levels (Price et al 1980; Hunter 2016). Because plants are sessile during significant portions of their lifecycles, they experience strong selection to adapt to their local environment (Cipollini 2002; Bossdorf et al 2005; Jay et al 2012; Weißhuhn et al 2012; Bucharova et al 2017), including in defense traits against their herbivores (Coley 1987; Agrawal & Van Zandt 2003; Agrawal 2005; Vannette & Hunter 2011)

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