The Ancestral Modulation Hypothesis: Predicting Mechanistic Control of Sexually Heteromorphic Traits Using Evolutionary History.

AbstractAcross the animal kingdom there are myriad forms within a sex across, and even within, species, rendering concepts of universal sex traits moot. The mechanisms that regulate the development of these trait differences are varied, although in vertebrates, common pathways involve gonadal steroid hormones. Gonadal steroids are often associated with heteromorphic trait development, where the steroid found at higher circulating levels is the one involved in trait development for that sex. Occasionally, there are situations in which a gonadal steroid associated with heteromorphic trait development in one sex is involved in heteromorphic or monomorphic trait development in another sex. We propose a verbal hypothesis, the ancestral modulation hypothesis (AMH), that uses the evolutionary history of the trait-particularly which sex ancestrally possessed higher trait values-to predict the regulatory pathway that governs trait expression. The AMH predicts that the genomic architecture appears first to resolve sexual conflict in an initially monomorphic trait. This architecture takes advantage of existing sex-biased signals, the gonadal steroid pathway, to generate trait heteromorphism. In cases where the other sex experiences evolutionary pressure for the new phenotype, that sex will co-opt the existing architecture by altering its signal to match that of the original high-trait-value sex. We describe the integrated levels needed to produce this pattern and what the expected outcomes will be given the evolutionary history of the trait. We present this framework as a testable hypothesis for the scientific community to investigate and to create further engagement and analysis of both ultimate and proximate approaches to sexual heteromorphism.