A neo-W chromosome in a tropical butterfly links colour pattern, male-killing, and speciation

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.

Karyotypes versus Genomes: The Nymphalid Butterflies <b><i>Melitaea cinxia, Danaus plexippus</i></b>, and <b><i>D. chrysippus</i></b>

“…Here, we confirm that the chromosome number for D. chrysippus is also n = 30 [de Lesse and Condamin, 1962;Gupta, 1964;Smith et al, 2016] for males from Southeast Asia, Israel, Ghana, Watamu (Kenya), and Kitengela (Kenya) (examples shown in Fig. 7 a, b).…”

“…The population is part of a large hybrid zone between the subspecies D. c. dorippus and D. c. chrysippus . Females from this population display a sex chromosome trivalent, neoW/Z 1 Z 2 , besides 28 bivalents in meiosis and are infected with a male-killing bacterium, Spiroplasma ixodetis [Smith et al, 2016]. The neoW is interpreted as the result of a fusion between the original W chromosome and an autosome, carrying the phenotypically defined wing colour gene C [Smith et al, 2010].…”

Whole-chromosome hitchhiking driven by a male-killing endosymbiont

“…1A). However, crosses with females from the contact zone revealed that the BC chromosome has become sex linked, forming a neo-W that is unique to this population [19,22]. Since female meiosis is achiasmatic (it lacks crossing-over) in the Lepidoptera, the formation of a neo-W would instantaneously cause perfect linkage, not just of the B and C loci, but of an entire nonrecombining chromosome, along with other maternally-inherited DNA.…”

“…What is particularly striking is that the presence of the neo-W coincides with infection by a maternally-inherited 'male killer' endosymbiont related to Spiroplasma ixodetis, which kills male offspring and leads to highly female-biased sex-ratios where infection is common [22][23][24]. The combination of neo-W and male killing is expected to dramatically alter the inheritance and evolution of the BC chromosome [22,25]: Infected females typically give rise to all-female broods who should always inherit the same colour patterning allele on their neo-W, along with the male-killer, while the other maternal allele is systematically eliminated in the dead sons ( Fig. 1B), forming a genetic sink for all colour pattern alleles not on the neo-W.…”

Ancestral and neo‐sex chromosomes contribute to population divergence in a dioecious plant

“…For both of these reasons, sex chromosome turnover may be a particularly important driver of population divergence and speciation. Indeed, associations between neo-sex chromosomes and speciation are reported in stickleback (Kitano et al 2009), swordtail (Franchini et al 2018), Hessian fly (Benatti et al 2010), mountain pine beetle (Bracewell et al 2017), and the African Queen butterfly (Smith et al 2016).…”