Biased sex ratios and Aposematic polymorphism in African butterflies

In East and Central Africa, the nymphalid butterflies Danaus chrysippus, Acraea encedon and Acraea encedana are involved in a Müllerian mimicry complex. Unusually for aposematic mimetic organisms, the three species show extensive colour pattern polymorphism. Within the same geographic zone, the three species show female-biased sex ratios as a consequence of infection by maternally-inherited, male-killing bacteria. The co-occurrence of biased sex ratios and aposematic polymorphism within these three sympatric, mimetic butterfly species has led to the speculation that invasion by the male-killing bacteria and the subsequent female-biased sex ratios are the underlying reason for the maintenance of colour polymorphism in these species, following its establishment by periods of allopatry and monomorphism and hybridisation. In this paper, we present a novel hypothesis that describes a mechanism by which such causal link might have taken place; in our view, positive frequency-dependent selection favouring the most common colour form in the species is disrupted as a consequence of the recurrent extinction-recolonization cycles undergone at the level of the species populations following the spread of the male-killer. Likewise, extinctions and recolonizations taking place in the other mimics randomly change the direction of selection on each species, potentially leading to multiple selective pressures favouring different colour patterns in the mimicry complex. Thus, selection for monomorphism within each species as well as between the mimetic species will be continuously randomized by the enhanced metapopulation dynamics and the state of polymorphism will be maintained consequently.