The Evolution of Sexual Systems in Animals

Abstract

A sexual system is the pattern of gender allocation that characterizes a species. In both plants and animals, simultaneous hermaphroditism and dioecy are the most common and stable sexual systems. Other sexual systems, sequential hermaphroditism, environmental sex determination, gynodioecy, androdioecy, and trioecy, are less stable and less widely distributed. The boundaries between these sexual systems are not always clear, largely because phenotypic plasticity is an important and prevalent component of sexual reproduction. One can view sexual systems in the Metazoa as lying on a gradient of phenotypic plasticity from simultaneous hermaphroditism at the high end through sequential hermaphroditism and environmental sex determination to genetically determined dioecy, which has a minimum of phenotypic plasticity in sex allocation. The distribution of sexual systems across the Metazoa gave rise to Williams’ Paradox, which states that the pattern is best explained by phylogeny rather than sex allocation theory. Today, sex allocation theory seems to explain transitions in sexual system in those taxa with labile sexual systems adequately. However, the stability of either dioecy or simultaneous hermaphroditism in many major taxa, such as phyla and classes, remains inexplicable. While in angiosperms the evolutionary pathways between dioecy and simultaneous hermaphroditism are fairly well understood, a plausible evolutionary sequence for transitions between dioecy and simultaneous hermaphroditism in animals has been lacking. Here, the proposal is made that it is useful to view transitions from simultaneous hermaphroditism to dioecy as the result of selection for decreasing phenotypic plasticity and vice versa. A scenario for evolutionary transitions between simultaneous hermaphroditism and dioecy, in animals, through intermediate stages of sequential hermaphroditism and environmental sex determination is proposed.