Female reproductive tract form drives the evolution of complex sperm morphology

The coevolution of female mate preferences and exaggerated male traits is a fundamental prediction of many sexual selection models, but has largely defied testing due to the challenges of quantifying the sensory and cognitive bases of female preferences. We overcome this difficulty by focusing on postcopulatory sexual selection, where readily quantifiable female reproductive tract structures are capable of biasing paternity in favor of preferred sperm morphologies and thus represent a proximate mechanism of female mate choice when ejaculates from multiple males overlap within the tract. Here, we use phylogenetically controlled generalized least squares and logistic regression to test whether the evolution of female reproductive tract design might have driven the evolution of complex, multivariate sperm form in a family of aquatic beetles. The results indicate that female reproductive tracts have undergone extensive diversification in diving beetles, with remodeling of size and shape of several organs and structures being significantly associated with changes in sperm size, head shape, gains/losses of conjugation and conjugate size. Further, results of Bayesian analyses suggest that the loss of sperm conjugation is driven by elongation of the female reproductive tract. Behavioral and ultrastructural examination of sperm conjugates stored in the female tract indicates that conjugates anchor in optimal positions for fertilization. The results underscore the importance of postcopulatory sexual selection as an agent of diversification.