Endocrine disruption of male mating signals: Ecological and evolutionary implications

Endocrine disrupting chemicals (EDCs) are chemicals that interfere with proper hormonal functioning in exposed animals. They enter the natural environment through multiple sources, and many non-target wildlife species are exposed to them via several modes. Exposure causes altered hormone levels, importantly gonadal hormones, resulting in changed reproductive characteristics. Vertebrate male mating signals convey important mate quality information to females. These signals are dependent on androgens for their production and maintenance. Female responses to signals depend on oestrogens. Disrupting these pathways jeopardizes signal production and reception, which has implications for mating system ecology. Besides affecting various aspects of the vertebrate physiology, EDCs can impair hormonal functioning by binding to or blocking hormone receptors, or by altering production and function of hormones or hormone receptors. We consider the ecological implications of multi-generational signal disruption by EDCs. Altered signals can influence population dynamics and sex ratios; local extinctions are possible. Community-level dynamics may be affected via interspecific dependence on signals or population fluctuations. We then address the evolutionary effects of EDC-altered male mating signals in vertebrates and discuss how females may respond to altered signals over evolutionary time. Trans-generational reduction in signal reliability can lead to reduced preference and eventual loss of the signal trait and to the evolution of new traits as signals of mate quality. Genetic divergence between endocrine disrupted and undisrupted populations may result, perhaps giving rise to speciation. Finally, we recommend areas of research to further explore some of the issues addressed in this review. We suggest field surveys to document existing alterations in mating systems and genetic divergence in endocrine disrupted populations. Long-term mesocosm studies and mathematical models would be useful to predict the fate of mating signals and female responses as a result of prolonged endocrine disruption. EDCs have been the focus of ecotoxicology for some time now, and we feel that this analysis should now enter the realm of evolutionary biology to determine the subtle, yet far-reaching effects on exposed non-target wildlife.