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Proc Natl Acad Sci U S A. 2009 Oct 27;106(43):18085-90. doi: 10.1073/pnas.0907051106. Epub 2009 Oct 19.

Macroevolutionary patterns of defense and pollination in Dalechampia vines: adaptation, exaptation, and evolutionary novelty.

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School of Biological Sciences, University of Portsmouth, Portsmouth PO1 2DY, United Kingdom.


We conducted phylogenetically informed comparative analyses of 81 taxa of Dalechampia (Euphorbiaceae) vines and shrubs to assess the roles of historical contingency and trait interaction in the evolution of plant-defense and pollinator-attraction systems. We asked whether defenses can originate by exaptation from preexisting pollinator attractants, or vice versa, whether plant defenses show escalation, and if so, whether by enhancing one line of defense or by adding new lines of defense. Two major patterns emerged: (i) correlated evolution of several complementary lines of defense of flowers, seeds, and leaves, and (ii) 5 to 6 losses of the resin reward, followed by redeployment of resin for defense of male flowers in 3 to 4 lineages, apparently in response to herbivore-mediated selection for defense of staminate flowers upon relaxation of pollinator-mediated selection on resin. In all cases, redeployment of resin involved reversion to the inferred ancestral arrangement of flowers and resiniferous bractlets. Triterpene resin has also been deployed for defense of leaves and developing seeds. Other unique defenses against florivores include nocturnal closure of large involucral bracts around receptive flowers and permanent closure around developing fruits (until opening again upon dehiscence). Escalation in one major clade occurred through an early dramatic increase in the number of lines of defense and in the other major clade by more limited increases throughout the group's evolution. We conclude that preaptations played important roles in the evolution of unique defense and attraction systems, and that the evolution of interactions with herbivores can be influenced by adaptations for pollination, and vice versa.

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