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As George Williams pointed out in 1975, although evolutionary explanations, based on selection acting on individuals, have been developed for the advantages of simultaneous hermaphroditism, sequential hermaphroditism and gonochorism, none of these evolutionary explanations adequately explains the current distribution of these sexual systems within the Metazoa (Williams' Paradox). As Williams further pointed out, the current distribution of sexual systems is explained largely by phylogeny. Since 1975, we have made a great deal of empirical and theoretical progress in understanding sexual systems. However, we still lack a theory that explains the current distribution of sexual systems in animals and we do not understand the evolutionary transitions between hermaphroditism and gonochorism. Empirical data, collected over the past 40 years, demonstrate that gender may have more phenotypic plasticity than was previously realized. We know that not only sequential hermaphrodites, but also simultaneous hermaphrodites have phenotypic plasticity that alters sex allocation in response to social and environmental conditions. A focus on phenotypic plasticity suggests that one sees a continuum in animals between genetically determined gonochorism on the one hand and simultaneous hermaphroditism on the other, with various types of sequential hermaphroditism and environmental sex determination as points along the spectrum. Here I suggest that perhaps the reason we have been unable to resolve Williams' Paradox is because the problem was not correctly framed. First, because, for example, simultaneous hermaphroditism provides reproductive assurance or dioecy ensures outcrossing does not mean that there are no other evolutionary paths that can provide adaptive responses to those selective pressures. Second, perhaps the question we need to ask is: What selective forces favor increased versus reduced phenotypic plasticity in gender expression? It is time to begin to look at the question of sexual system as one of understanding the timing and degree of phenotypic plasticity in gender expression in the life history in terms of selection acting on a continuum, rather than on a set of discrete sexual systems.

Williams' Paradox and the Role of Phenotypic Plasticity in Sexual Systems