Herbivore release drives parallel patterns of evolutionary divergence in invasive plant phenotypes

Abstract

Herbivory can drive rapid evolution of plant chemical traits mediating defensive and competitive ability. At a geographic scale, plant populations that escape selection from their ancestral herbivores may evolve decreased defence and increased competitiveness. While contrasts between native and invasive populations of plants lend support to this hypothesis, such experiments cannot establish causal links between herbivory and evolved invasive phenotypes. Here, we conducted geographic contrasts, and coupled these with long-term selection experiments that directly test for evolutionary responses to herbivore exclusion. In common gardens, we contrasted Solidago altissima genotypes that were historically exposed or protected from herbivory across two experimental time-scales: (i) a natural experiment where plant populations evolved either with native herbivory (in Minnesota and New York) or evolved relatively free from herbivory for 100 years in Japan, and (ii) a 12-year manipulative experiment where plants were either exposed to ambient herbivory or treated with insecticide. In both experiments, plant populations responded to herbivore release by evolving increased production of root allelochemicals and interspecific competitive ability against Poa pratensis. While plant resistance to a beetle herbivore did not diverge between plant origins, we still observed parallel evolutionary shifts in leaf secondary metabolite and protease inhibitor production, which may confer resistance to diverse herbivore species. Synthesis. Observed evolutionary convergence for multiple plant traits, between the natural and manipulative experiments, emphasizes the role of insect herbivores as key drivers of plant adaptation and geographic differentiation. Escape from herbivory was hypothesized to drive plant adaptation in invasive ranges. By combining native-invasive contrasts with long-term herbivore-exclusion experiments, we established a direct link between herbivory and evolution of invasive phenotypes in Solidago altissima.