Private parts for private property: Evolution of penis size with more valuable, easily stolen shells

Abstract

Evolution has generated enormous diversity in animal genitalia. However, the importance of private property in driving penis size evolution has rarely been explored. Here, I introduce a novel hypothesis, the 'private parts for private property' hypothesis, which posits that enlarged penises evolved to prevent the theft of property during sex. I tested this hypothesis in hermit crabs, which carry valuable portable property (a shell) and which must emerge from this shell during sex, risking social theft of their property by eavesdroppers. I measured relative penis size (penis-to-body ratio) for N = 328 specimens spanning nine closely related species. Species carrying more valuable, more easily stolen property had significantly larger penis size than species carrying less valuable, less easily stolen property, which, in turn, had larger penis size than species carrying no property at all. These patterns in penis size remained even when phylogeny was controlled for, and the patterns were not explained by alternative hypotheses. Instead, the results suggest larger penises evolved as morphological adaptations to facilitate safe sex, in which individuals retain their valuable property by extending a long penis outside the shell to copulate. This hypothesis may likewise apply to other taxa, including those with valuable but non-portable property.