Is biased mutation sufficient to save runaway sexual selection?

Abstract

Abstract In the 1980s, groundbreaking theoretical studies showed that ornaments displayed during courtship can coevolve with preferences for such ornaments, leading to extreme exaggeration of both traits. Later models cast doubt on such “runaway” sexual selection, showing that even a small cost of preferences can prevent exaggerated ornaments from persisting long-term. It was subsequently shown that if mutations acting on the ornament are biased—tending to produce smaller rather than larger ornaments—then exaggeration can persist even in the presence of preference costs, seemingly vindicating the original models. Here, we unpack an implicit assumption of these “biased mutation” models: Mutations are assumed to lead, on average, to both smaller and less costly ornaments. Biased mutation consequently generates both a fitness cost (due to reduced mating success) and a fitness benefit (due to increased survival). We lift this assumption by separating an individual’s investment in an ornament from their efficiency in converting such investment into ornament size. We assume that biased mutation acts only on efficiency but not on investment, and discuss the plausibility of this alternative assumption. Our model predicts that exaggerated ornaments and preferences can persist stably once they arise, but that strong initial preferences are needed to kick-start the runaway process. Consequently, biased mutation alone may not always be sufficient to save runaway sexual selection.