Evolutionary biology of plant defenses against herbivory and their predictive implications for endocrine disruptor susceptibility in vertebrates.

Abstract

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 man-made 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 c) 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.

Estrogenic plant consumption predicts red colobus monkey (Procolobus rufomitratus) hormonal state and behavior

“…Based on these studies and the relationships found here, it is possible that M. dura exerted an important influence on the red colobus endocrine system. However, as red colobus have had a long evolutionary relationship with this native species, it is possible that they have evolved adaptations to protect against any potential endocrine disruption caused by ingesting leaves of M. dura (Wynne-Edwards, 2001). …”

“…Effects include modifying the developing reproductive system (e.g., genital deformation) and altering steroid hormone profiles, gamete production, and sex-typical behaviors in exposed adults (Hayes et al, 2002; Milnes et al, 2006). Much less is known about the effects of consuming natural plant-produced estrogenic compounds (i.e., phytoestrogens; Wynne-Edwards, 2001). Most primates depend heavily on a plant-based diet, thus the consumption of estrogenic plants may have important implications for their behavior, ecology, and evolution.…”

“…Most primates depend heavily on a plant-based diet, thus the consumption of estrogenic plants may have important implications for their behavior, ecology, and evolution. Further, as half of all primate species are at risk of extinction (Chapman and Peres, 2001), a better understanding of the relationship between primates and naturally occurring phytoestrogens present in their foods is needed because such compounds have the potential to alter fertility and mating behavior (Cederroth et al, 2010a; Simon et al, 2004; Whitten and Patisaul, 2001; Wynne-Edwards, 2001). …”

From phytoestrogens to obesity and the metabolic syndrome: Health from food and food for health

“…Starting from this original receptor progenitor, evolution proceeded by ligand exploitation and serial genome expansion, but the ability to interact with the environment was maintained both in plants and plant-eaters, in a classical example of co-evolution. The ability of a plant to disrupt estrogen-mediated response in herbivorous represents, in fact, an expedient strategy aimed at discouraging from being eaten (Wynne-Edwards 2001). If this hypothesis is true, the conceptual distance between specific endogenous hormones and exogenous environmental molecules able to either mimic or modulate nuclear receptor-mediated signaling is probably closer than previously thought.…”

Phytoestrogen signaling and symbiotic gene activation are disrupted by endocrine-disrupting chemicals.

“…Leguminous plants such as soybean and alfalfa produce phytoestrogens to deter herbivores, to ward against fungal and bacterial pathogens, and as signaling agents to recruit soil bacteria to the plant's root system for nitrogen-fixing symbiosis (Koes et al 1994;Wynne-Edwards 2001). Symbiosis occurs when host plants release small polyphenolic compounds known as flavonoids or phytoestrogens into the soil.…”