Female-limited mimetic polymorphism: a review of theories and a critique of sexual selection as balancing selection

Mimicry theory played a prominent role in the development of natural selection theory, and sparked a long-lasting interest in the observation that Batesian mimicry in some butterflies is female limited and polymorphic. Mimetic females of polymorphic species clearly have a selective advantage due to reduced predation pressure, but the selective forces that maintain nonmimetic female forms remain unclear. Attention has lately been focused on three explanations based on sexual selection: (1) male mate preference, (2) pseudo-sexual selection and (3) sexual harassment avoidance. These are thought to favour nonmimetic female forms and allow them to persist in the population via balancing selection. Here I review the assumptions and evidence for each of these hypotheses and assess their relative merit. I find that: (a) key predictions of the hypotheses have not been tested, (b) the hypotheses interpret surrogate measures of fitness trade-offs implicit in balancing selection (e.g. mating frequency) differently, and (c) sexual selection may not maintain nonmimetic females at high mimic frequencies if male mate preference is frequency dependent. As a result, none of the hypotheses is unequivocally supported by available data. I show that a fourth, non-sexual selectionist hypothesis, namely that physiological trade-offs maintain mimetic female polymorphism, is based on unclear assumptions and probably explains minor variation in female polymorphism. Finally, I show that the basic framework of frequency-dependent mimetic advantage, independent of sexual selection, can adequately explain female-limited mimetic polymorphism in a broad range of species. Testing this framework should be a priority in resolving this problem.