Evolution of shade tolerance is associated with attenuation of shade avoidance and reduced phenotypic plasticity in North American milkweeds.

Abstract

Mismatches between light conditions and light-capture strategy can reduce plant performance and prevent colonization of novel habitats. Although light-capture strategies tend to be highly conserved among closely related species, evolutionary transitions from shaded to unshaded habitats (and vice versa) occur in numerous plant lineages. We combined phylogenetic approaches with field and greenhouse experiments to investigate evolutionary constraints on light-capture strategy in North American milkweeds (genus Asclepias) and to determine whether colonization of shaded habitats in this heliophilic clade is associated with reduced plasticity and attenuation of the shade avoidance response. Colonization of shaded habitats has occurred at least 10 times in this genus, including at least once in each major North American clade. Evolutionary transitions between habitats exhibit strong directional bias, with shifts from full-sun to shaded habitats occurring at least three times as often as the opposite transition. In field and greenhouse experiments, sun species responded to shade by increasing internode length, height, and specific leaf area, consistent with the shade avoidance response; paired shade species exhibited reduced plasticity overall, and only one trait (specific leaf area) responded to experimental shade. Our results suggest that milkweeds colonized shaded environments multiple times using a light-capture strategy distinct from the ancestral (putatively shade avoidant) strategy, including a general attenuation of plasticity in response to variable light conditions. This pattern bolsters the notion that shade avoidance and tolerance represent divergent evolutionary strategies for maximizing performance under qualitatively different types of shade.