Energetics and the evolution of carnivorous plants—Darwin's ‘most wonderful plants in the world’

Aaron M. Ellison 1 Nicholas J. Gotelli 0 0 Department of Biology, University of Vermont , 120 Marsh Life Sciences Building, Burlington, VT 05405 , USA 1 Harvard Forest, Harvard University , 324 North Main Street, Petersham, MA 01366 , USA 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 analysed; and the energetic costs and benefits of botanical carnivory were re-evaluated. 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 those of non-carnivorous plants. - This plant, commonly called Venus fly-trap, from the rapidity and force of its movements, is one of the most wonderful in the world. (C. Darwin, Insectivorous plants, p. 231)1 Carnivorous plants have evolved multiple times among the angiosperms (Fig. 1), and the degree of morphological and physiological convergence across carnivorous taxa is remarkable. Molecular sequence data have revealed the * To whom correspondence should be addressed. E-mail: Abbreviations: Amass, mass-based photosynthetic rate in nmol CO2 g 1 s 1; ANOVA, analysis of variance; atpB, chloroplast gene encoding the b chain of membrane-bound ATP synthase; C-value, amount of DNA in a haploid nucleus [in millions of base pairs (Mbp)]; coxI, mitochondrial gene encoding subunit 1 of cyctochrome c oxidase; ITS, internal transcribed spacer; JChao, the ChaoJaccard abundance-weighted index of similarity; nrITS, nuclear ribosomal ITS; matK, chloroplast gene believed to encode a maturase, it is located within the trnK intron; PIE, probability of interspecific encounter, used here as a measure of specialization on prey by carnivorous plants; PRT1, nuclear gene encoding peptide transferase 1; rbcL, chloroplast gene encoding ribulose-bisphosphate carboxylase; rps16, a non-coding chloroplast intron; RRTree, software for comparing sequence divergence rates among related lineages (by extension, it has also come to mean the statistical relative-rate test between groups of sequences on a phylogenetic tree); trnK, a non-coding chloroplast intron; it includes the matK exon; trnF and trnL, two other non-coding chloroplast introns; trnL-F, intergenic spacer between the trnL and trnF introns. 1 All quotations from Darwins Insectivorous plants are from the second (1898) edition. The Author [2008]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: phylogenetic history of the angiosperms (Stevens, 2007) and have yielded a better understanding of the patterns of evolution of carnivorous plants. The availability of reliable phylogenies, new observations and experiments, costbenefit models (Givnish et al., 1984; Laakkonen et al., 2006), and contemporary statistical methods have allowed carnivorous plants to emerge as model systems that can be used to address a wide range of questions arising from plant molecular genetics to physiology and evolutionary ecology (Ellison and Gotelli, 2001; Ellison et al., 2003). Charles Darwin laid the foundation for modern research on carnivorous plants. In Insectivorous plants, Darwin (1875) applied his then relatively new conception of homology to illustrate evolutionary and functional convergence across seemingly unrelated taxa. He provided the first detailed descriptions of the structures by which eight genera of plants could entrap insects. With careful observations and clever experiments, Darwin determined for the first time that these plants directly dissolved animal protein using enzymes whose action was similar to pepsin and other proteases (see also Hepburn et al., 1919, 1927). He further showed that dissolved nutrients were directly absorbed by carnivorous plants and that captured prey contributes significantly to plant growth (Darwin, 1875). Drawing on >125 years of subsequent research, this review surveys recent progress in three areas of inquiry that Darwin initiated in Insectivorous plants: (i) the tempo and mode of carnivorous plant evolution; (ii) patterns and processes of prey capture; and (iii) the energetic costs and benefits of botanical carnivory. These three research fronts are unified by stable phylogenetic placement of carnivorous taxa, new data on gene evolution in carnivorous plants (Jobson and Albert, 2002; Mu ller et al., 2004), and the refinement by Laakkonen et al. (2006) of the costbenefit model for the evolution of botanical carnivory originally formulated by Givnish et al. (1984). Current understanding of the phylogenetic placement of carnivorous plants re-affirms the occurrence of convergence in trapping mechanisms. Genomic data suggest biochemical, physiological, and ecological mechanisms that could have led to the rapid diversification of at least some carnivorous plant lineages. New analyses of published data on prey capture permit the evaluation of the degree of specialization among carnivorous plant genera and link evolutionarily convergent traits with the ecologically important process of predation. The use of carbon to measure both costs and benefits of carnivory allows carnivorous plants to be placed into the universal spectrum of leaf traits (Wright et al., 2004, 2005) that reflects fundamental trade-offs associated with the allocation of carbon to structural tissues and photosynthesis (Shipley et al., 2006). The tempo and mode of carnivorous plant evolution By comparing the structure of the leaves, their degree of complication, and their rudimentary parts in the six genera [Drosophyllum, Roridula, Byblis, Dr (...truncated)