Energetics and the evolution of carnivorous plants - Darwin's "most wonderful plants in the world"

Abstract

Carnivory has evolved independently at least six times in five angiosperm orders. In spite of these independent origins, there is a remarkable morphological convergence of carnivorous plant traps and physiological convergence of mechanisms for digesting and assimilating prey. These convergent traits have made carnivorous plants model systems for addressing questions in plant molecular genetics, physiology, and evolutionary ecology. New data show that carnivorous plant genera with morphologically complex traps have higher relative rates of gene substitutions than do those with simple sticky traps. This observation suggests two alternative mechanisms for the evolution and diversification of carnivorous plant lineages. The “energetics hypothesis” posits rapid morphological evolution resulting from a few changes in regulatory genes responsible for meeting the high energetic demands of active traps. The “predictable prey capture hypothesis” further posits that complex traps yield more predictable and frequent prey captures. To evaluate these hypotheses, available data on the tempo and mode of carnivorous plant evolution were reviewed; patterns of prey capture by carnivorous plants were analyzed; and the energetic costs and benefits of botanical carnivory were reevaluated. Collectively, the data are more supportive of the energetics hypothesis than the predictable prey capture hypothesis. The energetics hypothesis is consistent with a phenomenological cost-benefit model for the evolution of botanical carnivory and also accounts for data suggesting that carnivorous plants have leaf construction costs and scaling relationships among leaf traits that are substantially different from non-carnivorous plants.