Neo sex chromosomes, colour polymorphism and male-killing in the African queen butterfly, Danaus chrysippus (L.)

Danaus chrysippus (L.), one of the world’s commonest butterflies, has an extensive range throughout the Old-World tropics. In Africa it is divided into four geographical subspecies which overlap and hybridise freely in the East African Rift: Here alone a male-killing (MK) endosymbiont, Spiroplasma ixodetis, has invaded, causing female-biased populations to predominate. In ssp. chrysippus, inside the Rift only, an autosome carrying a colour locus has fused with the W chromosome to create a neo-W chromosome. A total of 40–100% of Rift females are neo-W and carry Spiroplasma, thus transmitting a linked, matrilineal neo-W, MK complex. As neo-W females have no sons, half the mother’s genes are lost in each generation. Paradoxically, although neo-W females have no close male relatives and are thereby forced to outbreed, MK restricts gene flow between subspecies and may thus promote speciation. The neo-W chromosome originated in the Nairobi region around 2.2 k years ago and subsequently spread throughout the Rift contact zone in some 26 k generations, possibly assisted by not having any competing brothers. Our work on the neo-W chromosome, the spread of Spiroplasma and possible speciation is ongoing

Hybrid effects in field populations of the African monarch butterfly, Danaus chrysippus (L.) (Lepidoptera: Nymphalidae)

This is the final version. Available on open access from Oxford University Press via the DOI in this recordHeterosis, Haldane and Bateson-Dobzhansky-Muller effects have been widely documented amongst a range of plants and animals. However, typically these effects are shown by taking parents of known genotype into the laboratory and measuring components of the F1 progeny under laboratory conditions. This leaves in doubt the real significance of such effects in the field. Here we use the well-known colour pattern genotypes of the African Monarch or Queen (Danaus chrysippus), which also control wing length, to test these effects both in the laboratory and in a contact zone in the field. By measuring the wing lengths in animals of known colour pattern genotype we show clear evidence for all three hybrid effects at the A and BC colour patterning loci, and importantly, that these same effects persist in the same presumptive F1s when measured in hybrid populations in the field. This demonstrates the power of a system in which genotypes can be directly inferred in the field and highlights that all three hybrid effects can be seen in the east African contact zone of this fascinating butterfly

Global biogeography of warning coloration in the butterfly Danaus chrysippus

Warning coloration provides a textbook example of natural selection, but the frequent observation of polymorphism in aposematic species presents an evolutionary puzzle. We investigated biogeography and polymorphism of warning patterns in the widespread butterfly Danaus chrysippus using records from citizen science (n = 5467), museums (n = 8864) and fieldwork (n = 2586). We find that polymorphism in three traits controlled by known mendelian loci is extensive. Broad allele frequency clines, hundreds of kilometres wide, suggest a balance between long-range dispersal and predation of unfamiliar morphs. Mismatched clines for the white hindwing and forewing tip in East Africa are consistent with a previous finding that the black wingtip allele has spread recently in the region through hitchhiking with a heritable endosymbiont. Light/dark background coloration shows more extensive polymorphism. The darker genotype is more common in cooler regions, possibly reflecting a trade-off between thermoregulation and predator warning. Overall, our findings show how studying local adaptation at the global scale provides a more complete picture of the evolutionary forces involved

African queens find mates when males are rare

This is the final version. Available from Wiley via the DOI in this record. DATA AVAILABILITY STATEMENT: Sex ratio, spermatophore numbers and Rcode: Figshare doi:10.6084/ m9.figshare.21947729.In butterflies and moths, male-killing endosymbionts are transmitted from infected females via their eggs, and the male progeny then perish. This means that successful transmission of the parasite relies on the successful mating of the host. Paradoxically, at the population level, parasite transmission also reduces the number of adult males present in the final population for infected females to mate with. Here we investigate if successful female mating when males are rare is indeed a likely rate-limiting step in the transmission of male-killing Spiroplasma in the African Monarch, Danaus chrysippus. In Lepidoptera, successful pairings are hallmarked by the transfer of a sperm-containing spermatophore from the male to the female during copulation. Conveniently, this spermatophore remains detectable within the female upon dissection, and thus, spermatophore counts can be used to assess the frequency of successful mating in the field. We used such spermatophore counts to examine if altered sex ratios in the D. chrysippus do indeed affect female mating success. We examined two different field sites in East Africa where males were often rare. Surprisingly, mated females carried an average of 1.5 spermatophores each, regardless of male frequency, and importantly, only 10-20% remained unmated. This suggests that infected females will still be able to mate in the face of either Spiroplasma-mediated male killing and/or fluctuations in adult sex ratio over the wet-dry season cycle. These observations may begin to explain how the male-killing mollicute can still be successfully transmitted in a population where males are rare.National Geographic SocietyRoyal Societ

BJLS-2895.R1.Raw data set for tables 1-5

Excel data sheet giving all data on butterflies reared for this publicatio

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

Danaus chrysippus (L.) in Africa comprises four substantially isolated semispecies that are migratory and hybridize on a seasonal basis throughout the eastern and central part of the continent. In the hybrid zone (but not elsewhere), the butterfly is commonly host to a male killing endosymbiotic bacterium, Spiroplasma sp., which principally infects one semispecies, Danaus chrysippus chrysippus in Kenya. A W-autosome mutation, inherited strictly matrilinearly, links B and C colour gene loci, which have thus gained sex-linkage in chrysippus. We have monitored variation in sex ratio and genotype at the A and C colour gene loci for two extended periods of 18 months (2004–5) and 12 months (2009–10) in adults reared from wild eggs laid on trap plants in Kasarani, near Nairobi, Kenya. Additionally, in 2009–10, all surviving adult butterflies were screened for Spiroplasma infection. The hybridizing Kasarani population is highly atypical in three respects, and has apparently been so for some 30 years: first, the sex ratio is permanently female-biased (as expected), although subject to seasonal fluctuation, being lowest (male/female) when D. c. chrysippus (cc) peaks and highest when Danaus chrysippus dorippus (CC) predominates; second, the population is invariably dominated by Cc heterozygotes of both sexes but especially females; and third, cc males are always scarce because they are systematically eliminated by male killing, whereas the CC genotype is male-biased. It is this imbalance of sex versus genotype that determines the massive departure from Hardy–Weinberg equilibrium in the population, in part because cc females have little choice but to pair with C- males. We suggest that: first, Cc hybrids of both sexes fail to disperse in the company of either parental semispecies; second, Spiroplasma positive females carrying the W-autosome mutation have a selective advantage over females that lack the translocation; third, the endoparasite and the translocation create a ‘magic trait’ linkage group that underlies hologenomic reproductive isolation between two emerging species, D. c. chrysippus and D. c. dorippus; and, fourth, that the predominance of males in dorippus suggests that individuals must be protected by a male-killing suppressor gene. By contrast to the C locus, Aa heterozygotes are in substantial and permanent deficit, suggesting either assortative mating between AA (chrysippus and dorippus) and aa (Danaus chrysippus alcippus), or heterozygote unfitness, or both

BLJS 2895.R1. Sex ratio model revised

Data collected in the field for this publication, population genetic model and its parameter

BJLS-2895.R1.Raw data set for tables 1-5

Excel data sheet giving all data on butterflies reared for this publicatio