Sex role preferences, gender conflict and sperm trading in simultaneous hermaphrodites: a new framework

A key issue in the study of the behaviour of copulating simultaneous hermaphrodites concerns the decision about which sexual role to adopt in a mating encounter. If two mates share a preference to adopt the same sexual role, mating interests are inherently incompatible. We review previous models that have explored the origin of, and resolutions to, such gender conflicts: (1) sex allocation models; (2) risk-averse models; (3) costly male function models; and (4) game-theoretical models. None of these satisfactorily accounts for the diversity found in hermaphrodite mating systems, either because the assumptions of the model reflect lifetime decisions rather than single mating decisions, or because only a narrow set of environmental conditions is considered. Furthermore, some often cited predictions such as a preference for copulating in the female role or a prevalence of conditional sperm exchange (‘sperm trading’) face limited empirical support. To reconcile and extend these previous ideas, we propose the gender ratio hypothesis as a more general model framework. Here, sex role preferences derive from the potential fitness gain per mating event. Preferences can thus vary considerably within and between individuals, but are predicted to be usually male biased. By combining sex role preference with mating rate, our hypothesis can explain the existence of a wide range of hermaphrodite mating systems, including unconditional reciprocity in systems where sperm trading has been predicted but not found.