Loss of male outcrossing ability in simultaneous hermaphrodites: Phylogenetic analyses of pulmonate snails

Phally, a genital polymorphism found in some species of self-compatible pulmonates (Mollusca: Gastropoda), presents an opportunity to examine factors maintaining outcrossing within an animal species in the presence of recombination. Euphallics, aphallics, and hemiphallics can self-fertilize but only euphallics develop a functional penis and prostate allowing them to donate sperm. Taxa containing aphallics and/or hemiphallics are rare within pulmonates (occurring in about 0-3% of species and genera) and are found near the tips of the phylogenetic tree at the species and genus level, suggesting that the loss of male outcrossing ability is unstable and has limited evolutionary potential. Phylogenetic analysis based on parsimony reveals that male outcrossing ability has been lost a minimum of 13 times. We find no unambiguous evidence of reversions from aphally and/or hemiphally back to pure euphally. In plants, self-fertilization is often associated with habitat and geographic range, and these variables, together with body size, have been hypothesized as factors facilitating the evolution of aphally. When we control for phylogeny using comparisons of sister taxa, loss of male outcrossing ability is associated with geographic range but not body size or habitat. Furthermore, polyploidy is not associated with the loss of male outcrossing ability, contrary to predictions that low levels of inbreeding depression in polyploids will facilitate the evolution of aphally and or hemiphally.