Contingency, Determinism, and Constraint in the Evolution of Elaborate Courtship Phenotypes.

Abstract

Natural selection is broadly considered to be a deterministic process, though the roles of historical contingency and constraint are increasingly being recognised as key factors shaping the diversity of life on earth. Sexual selection through mate choice is similarly deterministic and there is increasing evidence that processes such as sensory drive may produce predictable evolutionary outcomes in the design features of sexual signals. However, much variation amid the extraordinary diversity of courtship phenotypes among animals is left unexplained by purely deterministic processes. Since evolution acts without foresight, the elaboration of phenotypes-including those involved in sexual signalling-is analogous to a tinkering process, meaning that nuanced historical contingencies in an organism's phylogenetic history set the stage for unique constraints in the future. Even in famously diverse 'ornamental' radiations, such as the birds of paradise-which feature numerous unique courtship traits or evolutionary "one-offs"-they also exhibit exceptional convergence in signalling traits despite strikingly diverse signal production mechanisms. While comparative research often focuses on signaller phenotypes, a clear distinction between signal production mechanisms (i.e., the mechanical or physiological basis of display) and their perceptual effects for signal receivers (i.e., signal design features) is critical to understand the deterministic processes shaping signal evolution. Furthermore, while there may be disparate evolutionary trajectories to similar elaborate signalling phenotypes, the resulting unique mechanisms of display can impose equally unique constraints on signalling phenotypes. These and other findings suggest that, to understand the evolution of elaborate courtship phenotypes, comparative research should address the interacting effects of deterministic processes, historical contingencies, and biological constraints.