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Citation

Lushai G, Allen JA, Goulson D, Maclean N & Smith DAS (2005) The butterfly Danaus chrysippus (L.) in East Africa comprises polyphyletic, sympatric lineages that are, despite behavioural isolation, driven to hybridization by female-biased sex ratios. Biological Journal of the Linnean Society, 86 (1), pp. 117-131. https://doi.org/10.1111/j.1095-8312.2005.00526.x

Abstract
Mitochondrial and nuclear DNA information was analysed among four subspecies of the African Queen butterfly, Danaus (Anosia) chrysippus sensu lato (s.l.), along with four other Danaus species drawn from all three subgenera (D. (Danaus) plexippus, D. (Salatura) genutia, D. (A.) gilippus, D. (A.) eresimus) and two outgroup species from the same tribe, Tirumala septentrionis and Amauris niavius. A mitochondrial phylogeny derived from the 12S rRNA (347 bp) and COI (537 bp) loci indicates two very distinct haplotypes for subspecies D. (A.) c. dorippus, dorippus-1 and dorippus-2. Interestingly, dorippus-1, on the one hand, and all other D. (A.) chrysippus haplotypes, on the other, are the most distantly related clades within the genus and have different most recent ancestors from different subgenera, though sharing the common ancestor of the monophyletic genus. A phylogeny based on the EF1- nuclear locus (400 bp) shows that the two well-separated mitochondrial lineages of dorippus are identical for this gene and reciprocally monophyletic to the other D. (A.) chrysippus lineages. Thus, nuclear and cytoplasmic phylogenies are not only discordant, but also suggest that both D. (A.) chrysippus s.l. and subspecies dorippus are polyphyletic. Paradoxically, four African subspecies, chrysippus-orange, chrysippus-brown, alcippus and dorippus, though substantially vicariant, hybridize extensively in East Africa wherever the ranges of two or more of them overlap. Linkage disequilibrium, and hence sexual isolation, in sympatry between colour (nuclear) genes and unlinked mitochondrial (cytoplasmic) loci is consistent across populations and therefore indicates the operation of positive natural selection. Together with data from previous experimental and field work, our results suggest that extensive hybridization occurs among once allopatric or parapatric lineages, that are now nascent species. We deduce that hybridism among lineages in sympatry is currently enforced, in the face of assortative mate choice, by a bacterial symbiont, Spiroplasma, a male-killer that forces females in female-biased populations to pair with heterotypic males. In discussion we emphasize that neither D. (A.) chrysippus s.l. as presently circumscribed, nor its component clades, conform to any established concept of species.

Keywords
heterozygote excess; linkage disequilibrium; male-killing; mitochondrial DNA; non-random mating; nuclear DNA

Journal
Biological Journal of the Linnean Society: Volume 86, Issue 1