Whole-chromosome hitchhiking driven by a male-killing endosymbiont

Abstract

Neo-sex chromosomes are found in many taxa, but the forces driving their emergence and spread are poorly understood. The female-specific neo-W chromosome of the African monarch (or queen) butterfly Danaus chrysippus presents an intriguing case study because it is restricted to a single 'contact zone' population, involves a putative colour patterning supergene, and cooccurs with infection by the the male-killing endosymbiont Spiroplasma. We investigated the origin and evolution of this system using whole genome sequencing. We first identify the 'BC supergene', a broad region of suppressed recombination across nearly half a chromosome, which links two colour patterning loci. Association analysis suggests that the genes yellow and arrow in this region control the forewing colour pattern differences between D. chrysippus subspecies. We then show that the same chromosome has recently formed a neo-W that has spread through the contact zone within ~2200 years. We also assembled the genome of the male-killing Spiroplasma, and find that it shows perfect genealogical congruence with the neo-W, suggesting that the neo-W has hitchhiked to high frequency as the male killer has spread through the population. The complete absence of female crossing-over in the Lepidoptera causes wholechromosome hitchhiking of a single neo-W haplotype, carrying a single allele of the BC supergene, and dragging multiple non-synonymous mutations to high frequency. This has created a population of infected females that all carry the same recessive colour patterning allele, making the phenotypes of each successive generation highly dependent on uninfected male immigrants. Our findings show how hitchhiking can occur between the unlinked genomes of host and endosymbiont, with dramatic consequences. . Smith DAS, Owen DF, Gordon IJ, Lowis NK. The butterfly Danaus chrysippus ( L .) in East Afiica : polymorphism and morph-ratio clines within a complex , extensive and dynamic hybrid zone. Zool J Linn Soc. 1997;120: 51-78. 17. Smith DAS. Heterosis, epistasis and linkage disequilibrium in a wild population of the polymorphic butterfly Danaus chrysippus ( L .). Zool J Linn Soc. 1980;69: 87-109. 18. Smith D a S, Owen DF, Gordon IJ, Owiny AM. Polymorphism and evolution in the butterfly Danaus chrysippus (L.) (Lepidoptera: Danainae).

Neo Sex Chromosomes, Colour Polymorphism and Male-Killing in the African Queen Butterfly, Danaus chrysippus (L.)

“…The recombination estimate is based only on males as meiosis in female Lepidoptera is achiasmate and crossing-over therefore absent [70,71,72]. Our recent work supports the hypothesis that B and C are two separate genes linked via complex rearrangements on chromosome 15 [73]. The combination of dominant alleles in coupling— BC —has not been found in any males from which we have bred, whereas one of the other three combinations is fixed in each of the subspecies, chrysippus ( bc ), orientis ( Bc ) and dorippus ( bC ).…”

“…Eventually, an opportunity to cross African with Indian D. chrysippus in 2006 produced a single brood that was sex-linked for the BC locus and this prompted us to re-examine previous rare cases. In just one lineage we were able to prove by classical analysis that W-linkage of the BC locus was the correct interpretation [80] and this has since been amply confirmed both cytologically [83] and from DNA sequencing [73]. We found karyotypes (25 counts) for both sexes of D. chrysippus from South-east Asia, Israel, South Africa, Ghana and several sites in Kenya to be 2 n = 60 [8].…”

“…The cause of male-killing was finally established when Jiggins and colleagues [77], working in exactly the same part of Uganda as had Owen and Chanter, identified the endoparasite in D. chrysippus as a bacterium close to Spiroplasma ixodetis and detectable by PCR; the long delay in its discovery was because endoparasites cannot be cultured in vitro and thereby identified by obedience to Koch’s postulates. However, it has been shown [73,77] that Spiroplasma -infected caterpillars can be ‘cured’ by feeding them on leaves which have been painted with a weak solution of the antibiotic tetracycline. We have shown by PCR that cured females are Spiroplasma -free and that their ability to bear sons is thereby restored [73].…”

“…However, it has been shown [73,77] that Spiroplasma -infected caterpillars can be ‘cured’ by feeding them on leaves which have been painted with a weak solution of the antibiotic tetracycline. We have shown by PCR that cured females are Spiroplasma -free and that their ability to bear sons is thereby restored [73]. Jiggins’ discovery of Spiroplasma was confirmed by PCR in Kenya [78] and in Uganda [79]; no other causative organism has been found in subsequent searches.…”

“…Furthermore, screening by PCR for Spiroplasma outside this area has proved overwhelmingly, though not absolutely, negative (Table 3). Our evidence then is that Spiroplasma and MK are tightly, perhaps even obligately, linked [73].…”