Biased sex ratios and aposematic polymorphism in African butterflies: A hypothesis

Abstract

In East and Central Africa, the nymphalid butterflies Danaus chrysippus, Acraea encedon and A. 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 femalebiased 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 extinctionrecolonisation cycles undergone at the level of the species populations following the spread of the malekiller. Likewise, extinctions and recolonisations 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 randomised by the enhanced metapopulation dynamics and the state of polymorphism will be maintained consequently.

Diversity in warning coloration: selective paradox or the norm?

“…In summary, disease has the potential to cause continuous variation in the chromatic and achromatic parts of an aposematic signal due to current infection, plastic changes at the individual level where infection stimulates increase in melanisation, and local adaptation via correlated trait responses if coloration is linked to factors such as immunocompetence and if the level of infection risk varies spatially. Pathogens may also cause local extinctions, or repeated bottlenecks, which can disrupt purifying selection and maintain colour variation (Gordon, ; Idris & Hassan, ). Meanwhile, parasitism is likely to influence both morph abundance and within‐morph conspicuousness in populations of aposematic species.…”

Whole-chromosome hitchhiking driven by a male-killing endosymbiont

“…The future of the neo-W and Spiroplasma outbreak is uncertain. A lack of males could lead to local extinctions [27], but extinction of the entire infected lineage is unlikely given the high dispersal ability and seasonal influxes of males in the contact zone. Indeed, it is notable that Spiroplasma infection has only been recorded within the contact zone population (with the exception of a single South African female reported here, S12 Table), especially given theory showing that male killers should spread very rapidly across the geographical range of a panmictic population if they provide even a very weak selective advantage [49].…”

“…1B), forming a genetic sink for all colour pattern alleles not on the neo-W. It has been suggested that the restriction of male killing to females with the neo-W, and only in the region in which hybridisation occurs between subspecies, may not be a coincidence [19,22,[25][26][27]. However, the genomic underpinnings of this system -the genetic controllers of colour pattern, the source and spread of the neo-W, and its relationship with the male killer -have until now remained a mystery.…”

Hologenomic speciation: synergy between a male-killing bacterium and sex-linkage creates a ‘magic trait’ in a butterfly hybrid zone

“…Genetic drift has been invoked by Idris & Hassan () who propose that male killers are responsible for a recurring series of bottlenecks, local extinctions, and founder effects, with stochastic genetic drift leading to changes in the frequencies of the colour pattern genes that sustain the polymorphism. Smith () and Gordon (), in their commentaries on the study by Idris & Hassan (), note that, although it may be appropriate for a second, co‐mimetic species ( Acraea encedon ) that also shows male killing and polymorphism, it cannot apply to D . chrysippus because this butterfly is widely dispersed and does not form local colonies that could be driven extinct in the manner proposed.…”