Abstract

Substantial research has addressed adaptation of nonnative biota to novel environments, yet surprisingly little work has integrated population genetic structure and the mechanisms underlying phenotypic differentiation in ecologically important traits. We report on studies of the common milkweed Asclepias syriaca, which was introduced from North America to Europe over the past 400 years and which lacks most of its specialized herbivores in the introduced range. Using 10 populations from each continent grown in a common environment, we identified several growth and defense traits that have diverged, despite low neutral genetic differentiation between continents. We next developed a Bayesian modeling approach to account for relationships between molecular and phenotypic differences, confirming that continental trait differentiation was greater than expected from neutral genetic differentiation. We found evidence that growth-related traits adaptively diverged within and between continents. Inducible defenses triggered by monarch butterfly herbivory were substantially reduced in European populations, and this reduction in inducibility was concordant with altered phytohormonal dynamics, reduced plant growth, and a trade-off with constitutive investment. Freedom from the community of native and specialized herbivores may have favored constitutive over induced defense. Our replicated analysis of plant growth and defense, including phenotypically plastic traits, suggests adaptive evolution following a continental introduction.

Highlights

  • As Charles Elton observed more than 50 years ago, transcontinental species introductions offer remarkable natural experiments to test hypotheses about the ecology and evolution of organismal traits (Sax et al 2005)

  • We report on studies of the common milkweed Asclepias syriaca, which was introduced from North America to Europe over the past 400 years and which lacks most of its specialized herbivores in the introduced range

  • Using 10 populations from each continent grown in a common environment, we identified several growth and defense traits that have diverged, despite low neutral genetic differentiation between continents

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Summary

Introduction

As Charles Elton observed more than 50 years ago, transcontinental species introductions offer remarkable natural experiments to test hypotheses about the ecology and evolution of organismal traits (Sax et al 2005). Plants may adaptively evolve in response to the novel biotic environment, to the lack of coevolved enemies or competitors (Blossey and Nötzold 1995; Sakai et al 2001; Callaway et al 2004; Orians and Ward 2010) They may rapidly adapt to abiotic conditions (Maron et al 2004; Colautti et al 2009); for example, when species are transported across continents, populations in the introduced range often evolve adaptive latitudinal clines in their phenotype, mirroring the clines of their native range (Colautti et al 2009). These effects are not mutually exclusive, and unraveling the drivers of continental differentiation requires an integrative approach

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