Abstract
Sexually antagonistic selection can drive both the evolution of sex chromosomes and speciation itself. The tropical butterfly the African Queen, Danaus chrysippus, shows two such sexually antagonistic phenotypes, the first being sex-linked colour pattern, the second, susceptibility to a male-killing, maternally inherited mollicute, Spiroplasma ixodeti, which causes approximately 100% mortality in male eggs and first instar larvae. Importantly, this mortality is not affected by the infection status of the male parent and the horizontal transmission of Spiroplasma is unknown. In East Africa, male-killing of the Queen is prevalent in a narrow hybrid zone centred on Nairobi. This hybrid zone separates otherwise allopatric subspecies with different colour patterns. Here we show that a neo-W chromosome, a fusion between the W (female) chromosome and an autosome that controls both colour pattern and male-killing, links the two phenotypes thereby driving speciation across the hybrid zone. Studies of the population genetics of the neo-W around Nairobi show that the interaction between colour pattern and male-killer susceptibility restricts gene flow between two subspecies of D. chrysippus. Our results demonstrate how a complex interplay between sex, colour pattern, male-killing, and a neo-W chromosome, has set up a genetic ‘sink' that keeps the two subspecies apart. The association between the neo-W and male-killing thus provides a ‘smoking gun' for an ongoing speciation process.
Highlights
Many arthropod species are infected with maternally inherited endosymbionts that induce a shift in the sex ratio of their hosts by killing males, so-called ‘male-killing’
We have found within the hybrid zone that chrysippus females and their transiens daughters are all infected with the male-killing Spiroplasma and produce all-female broods whereas, by contrast, dorippus females are largely uninfected by Spiroplasma and, continue to produce both males and females
We show that in a femaledominated hybrid zone site at Kitengela, immigrant dorippus males are relatively immune to male-killing and that most females are inseminated despite outnumbering males by around 5 : 1
Summary
Many arthropod species are infected with maternally inherited endosymbionts that induce a shift in the sex ratio of their hosts by killing males, so-called ‘male-killing’. Male-killing can increase infected female fitness at the expense of non-transmitting infected males by increasing the resources available to females, either by reducing inter-sibling competition or via cannibalism [1]. Endosymbionts that have near-perfect transmission may reduce the effective population size (Ne) by a factor that approximates to the proportion of uninfected individuals in the population [2]. Theoretical studies of male-killing endosymbionts, where hybridizing subpopulations interbreed, have shown that local adaptation can be strongly impeded in the subpopulation with the more biased population sex ratio [3]. It has been shown that both genetic drift and genetic influx are enhanced.
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