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Keywords:

  • adaptation to arid environments;
  • aldehydes;
  • cardenolides;
  • cuticular waxes;
  • monarch butterfly caterpillar (Danaus plexippus);
  • plant defense syndromes;
  • trichomes;
  • water use efficiency

Summary

  • • 
    The leaf surface is the contact point between plants and the environment and plays a crucial role in mediating biotic and abiotic interactions. Here, we took a phylogenetic approach to investigate the function, trade-offs, and evolution of leaf surface traits in the milkweeds (Asclepias).
  • • 
    Across 47 species, we found trichome densities of up to 3000 trichomes cm−2 and epicuticular wax crystals (glaucousness) on 10 species. Glaucous species had a characteristic wax composition dominated by very-long-chain aldehydes.
  • • 
    The ancestor of the milkweeds was probably a glaucous species, from which there have been several independent origins of glabrous and pubescent types. Trichomes and wax crystals showed negatively correlated evolution, with both surface types showing an affinity for arid habitats. Pubescent and glaucous milkweeds had a higher maximum photosynthetic rate and lower stomatal density than glabrous species. Pubescent and glaucous leaf surfaces impeded settling behavior of monarch caterpillars and aphids compared with glabrous species, although surface types did not show consistent differentiation in secondary chemistry.
  • • 
    We hypothesize that pubescence and glaucousness have evolved as alternative mechanisms with similar functions. The glaucous type, however, appears to be ancestral, lost repeatedly, and never regained; we propose that trichomes are a more evolutionarily titratable strategy.