Genetic variation segregates as linked sets of variants, or haplotypes. Haplotypes and linkage are central to genetics and underpin virtually all genetic and selection analysis. And yet, genomic data often lack haplotype information, due to constraints in sequencing technologies. Here we present “haplotagging”, a simple, low-cost linked-read sequencing technique that allows sequencing of hundreds of individuals while retaining linkage information. We apply haplotagging to construct megabase-size haplotypes for over 600 individual butterflies (Heliconius erato and H. melpomene), which form overlapping hybrid zones across an elevational gradient in Ecuador. Haplotagging identifies loci controlling distinctive high- and lowland wing color patterns. Divergent haplotypes are found at the same major loci in both species, while chromosome rearrangements show no parallelism. Remarkably, in both species the geographic clines for the major wing pattern loci are displaced by 18 km, leading to the rise of a novel hybrid morph in the centre of the hybrid zone. We propose that shared warning signalling (Müllerian mimicry) may couple the cline shifts seen in both species, and facilitate the parallel co-emergence of a novel hybrid morph in both co-mimetic species. Our results show the power of efficient haplotyping methods when combined with large-scale sequencing data from natural populations.
We thank Felicity Jones for input into experimental design, helpful discussion and improving the manuscript. We thank the Rolian, Jiggins, Chan and Jones Labs members for support, insightful scientific discussion and improving the manuscript. We thank the Rolian lab members, the Animal Resource Centre staff at the University of Calgary, and Caroline Schmid and Ann-Katrin Geysel at the Friedrich Miescher Laboratory for animal husbandry. We thank Christa Lanz, Rebecca Schwab and Ilja Bezrukov for assistance with high-throughput sequencing and associated data processing; Andre Noll and the MPI Tübingen IT team for computational support. We thank Ben Haller and Richard Durbin for helpful discussions. We thank David M. Kingsley for thoughtful input that has greatly improved our manuscript. J.I.M. is supported by a Research Fellowship from St. John’s College, Cambridge. A.D. was supported by a European Research Council Consolidator Grant (No. 617279 “EvolRecombAdapt”, P/I Felicity Jones). C.R. is supported by Discovery Grant #4181932 from the Natural Sciences and Engineering Research Council of Canada and by the Faculty of Veterinary Medicine at the University of Calgary. C.D.J. is supported by a BBSRC grant BB/R007500 and a European Research Council Advanced Grant (No. 339873 “SpeciationGenetics”). M.K. and Y.F.C. are supported by the Max Planck Society and a European Research Council Starting Grant (No. 639096 “HybridMiX”).
Meier JI, Salazar PA, Kučka M, et al. Haplotype tagging reveals parallel formation of hybrid races in two butterfly species. PNAS. 2021;118(25). doi:10.1073/pnas.2015005118
Meier, J. I., Salazar, P. A., Kučka, M., Davies, R. W., Dréau, A., Aldás, I., … Chan, Y. F. (2021). Haplotype tagging reveals parallel formation of hybrid races in two butterfly species. PNAS. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.2015005118
Meier, Joana I., Patricio A. Salazar, Marek Kučka, Robert William Davies, Andreea Dréau, Ismael Aldás, Olivia Box Power, et al. “Haplotype Tagging Reveals Parallel Formation of Hybrid Races in Two Butterfly Species.” PNAS. Proceedings of the National Academy of Sciences, 2021. https://doi.org/10.1073/pnas.2015005118.
J. I. Meier et al., “Haplotype tagging reveals parallel formation of hybrid races in two butterfly species,” PNAS, vol. 118, no. 25. Proceedings of the National Academy of Sciences, 2021.
Meier JI, Salazar PA, Kučka M, Davies RW, Dréau A, Aldás I, Power OB, Nadeau NJ, Bridle JR, Rolian C, Barton NH, McMillan WO, Jiggins CD, Chan YF. 2021. Haplotype tagging reveals parallel formation of hybrid races in two butterfly species. PNAS. 118(25), e2015005118.
Meier, Joana I., et al. “Haplotype Tagging Reveals Parallel Formation of Hybrid Races in Two Butterfly Species.” PNAS, vol. 118, no. 25, e2015005118, Proceedings of the National Academy of Sciences, 2021, doi:10.1073/pnas.2015005118.
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