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Exaptations Link Evolution of Plant-Herbivore and Plant-Pollinator Interactions: A Phylogenetic Inquiry

W. Scott Armbruster
Ecology
Vol. 78, No. 6 (Sep., 1997), pp. 1661-1672
Published by: Wiley
DOI: 10.2307/2266091
Stable URL: http://www.jstor.org/stable/2266091
Page Count: 12
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Exaptations Link Evolution of Plant-Herbivore and Plant-Pollinator Interactions: A Phylogenetic Inquiry
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Abstract

To evaluate possible evolutionary links between plant-herbivore and plant-pollinator relationships, defense and reward characteristics and pollination ecology were mapped onto a morphologically estimated phylogeny of 42 species of Dalechampia. This procedure generated detailed hypotheses about the evolution of anti-herbivore defense and pollination systems. These hypotheses were tested using the results of chemical analyses and bioassays of foliar and floral secretions. Multiple lines of defense appear to have evolved in sequence in Dalechampia. The first defense system to originate was deployment of triterpene resins to defend the staminate flowers. This feature was a preaptation (preadaptation) that allowed the evolution of a resinbased, pollinator-reward system. Thus pollination by resin-collecting bees originated as a "transfer exaptation" (a new function replaced the old). This hypothesis is supported by anti-herbivore activities of floral resins and by chemical similarity of floral defense and reward resins. After the resin defense of flowers was lost by conversion into a reward system, there followed (in evolutionary time) a sequence of defensive innovations. These included nocturnal closure of large, involucral bracts to protect both staminate and pistillate flowers. Phylogenetic analysis showed that the large bracts themselves probably originated as a floral advertisement system, and the bracts assumed a defensive function through "addition exaptation" (a new function was added to the old). Additional lines of defense to evolve were deployment of resin to defend the developing ovaries and seeds (an addition exaptation), deployment of sharp, detaching trichomes on enveloping sepals to defend developing seeds (apparent adaptations), closure of involucral bracts around the developing fruits and seeds (an addition exaptation), and deployment of resin to defend the leaves and growing shoot tips (also an addition exaptation). Support for this scenario also derives from the chemical similarities of sepal, foliar, and floral resins, and the anti-herbivore properties of foliar resins. It appears that at least one pollinator-reward system originated by modification of a defense system, and several defense systems originated by modification of pollinator reward and advertisement systems. Thus exaptations have been important in the origin of new defense and pollination systems, and each system has significantly influenced the evolution of the other on several occasions.

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