Ecology and sexual conflict drive the macroevolutionary dynamics of female-limited colour polymorphisms

Abstract

Sexual conflict over mating has been documented in many species, both in the field and in experimental studies. In pond damselflies (family Coenagrionidae), sexual conflict maintains female-limited colour poly-morphisms, with one female morph typically being a male mimic. However, it is not known whether sexual conflict can also explain the evolutionary origin of novel female morphs, and if so, what ecological factors play a role in this macroevolutionary transition, by modulating the strength of the conflict. Furthermore, the effects of sexual conflict on phylogenetic diversification remain controversial, with studies arguing that the evolution of alternative reproductive morphs, such as female-limited colour morphs, could either hinder or accelerate speciation. Here, we use phylogenetic comparative methods to show that female colour polymorphisms are more likely to evolve when population densities at breeding sites are high, and that these demographic conditions are more common at high latitudes and in open landscapes. We show that female-limited polymorphisms typically evolve from sexually dimorphic ancestors through the addition of a male-like female morph, consistent with the hypothesis of selection for male mimicry. Female polymorphic and sexually dimorphic lineages diversify at a higher rate than sexually monomorphic lineages, suggesting a broad diversity-promoting role of inter-sexual interactions based on visual signals. We conclude that female colour polymorphisms evolve in a predictable fashion, and are likely driven by ecological conditions that increase the rate of pre-mating interactions and thus the intensity of sexual conflict.