Evolutionary Biology of Plant Defenses against Herbivory and Their Predictive Implications for Endocrine Disruptor Susceptibility in Vertebrates
Wynne-Edwards, Katherine E., Environmental Health Perspectives
Hormone disruption is a major, underappreciated component of the plant chemical arsenal, and the historical coevolution between hormone-disrupting plants and herbivores will have both increased the susceptibility of carnivores and diversified the sensitivities of herbivores to manmade endocrine disruptors. Here I review diverse evidence of the influence of plant secondary compounds on vertebrate reproduction, including human reproduction. Three of the testable hypotheses about the evolutionary responses of vertebrate herbivores to hormone-disrupting challenges from their diet are developed. Specifically, the hypotheses are that a) vertebrate herbivores will express steroid hormone receptors in the buccal cavity and/or the vomeronasal organ; b) absolute sex steroid concentrations will be lower in carnivores than in herbivores; and e) herbivore steroid receptors should be more diverse in their binding affinities than carnivore lineages. The argument developed in this review, if empirically validated by support for the specific hypotheses, suggests that a) carnivores will be more susceptible than herbivores to endocrine-disrupting compounds of anthropogenic origin entering their bodies, and b) diverse herbivore lineages will be variably susceptible to any given natural or synthetic contaminant. As screening methods for hormone-disrupting potential are compared and adopted, comparative endocrine physiology research is urgently needed to develop models that predict the broad applicability of those screening results in diverse vertebrate species. Key words: endocrine disruptors, estrogen receptor, evolution, diet, fertility, plant-herbivore coevolution, sex steroids. [Online 24 April 2001]
Developing a coherent science and policy agenda to define the reproductive threat posed by man-made environmental contaminants is an immense task (1). A key component of any scientific and policy response to the threat of endocrine disruptors will be an ability to predict the effects of diverse chemical compounds on wildlife, as well as on humans (2,3). Hormone disruption is an underappreciated component of plant chemical arsenals. The ability to disrupt vertebrate reproduction is clearly present in plants, the relevant biochemical pathways are available to plants, and the risks to plant reproduction are minimal. An evolutionary history of hormone-disruptor activity in plants and the coevolutionary responses of herbivores will manifest itself in variable responses of herbivores to the same contaminant, overall increases in steroid concentration in herbivores relative to carnivores, and sensitive abilities to adjust contaminant ingestion in herbivores. If the hypotheses developed in this analysis are empirically validated, then ecology and diet will predict susceptibility to anthropogenic hormone disruptors across a wide range of vertebrate species.
Plants Do Not Want to Be Eaten
Plants do not benefit from having their foliage and structural support (e.g., shoots, roots, tubers) eaten. They respond to damage (or pruning) by regrowth, altered patterns of growth, and flowering, but losses to herbivory are expensive in terms of lost photosynthetic capacity, lost mechanical strength, lost moisture (through wounds), lost investment in the foliage that must be replaced, and lost energetic reserves to devote to reproduction and survival (4-6).
Plants have evolved a broad array of defenses to reduce the damage caused by herbivory. Some of those defenses are physical, from thorns to fiber bulk that defies vertebrate digestive capacity (4), but the majority are chemical (5,6). The array of chemical defenses is staggeringly large (7). For example, plants can release volatile turpenes that relieve herbivory pressure on the plant by attracting carnivores to eat the insect herbivores (8,9). Similarly, bitter-tasting repellents (10), mammalian cardiac glycosides (11), severe skin irritants (12), and cyanides or oxygen radicals released upon mastication (13,14) are well-characterized components of the plant chemical arsenal. …