---
_id: '9375'
abstract:
- lang: eng
  text: 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.
acknowledgement: '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”).'
article_number: e2015005118
article_processing_charge: No
article_type: original
author:
- first_name: Joana I.
  full_name: Meier, Joana I.
  last_name: Meier
- first_name: Patricio A.
  full_name: Salazar, Patricio A.
  last_name: Salazar
- first_name: Marek
  full_name: Kučka, Marek
  last_name: Kučka
- first_name: Robert William
  full_name: Davies, Robert William
  last_name: Davies
- first_name: Andreea
  full_name: Dréau, Andreea
  last_name: Dréau
- first_name: Ismael
  full_name: Aldás, Ismael
  last_name: Aldás
- first_name: Olivia Box
  full_name: Power, Olivia Box
  last_name: Power
- first_name: Nicola J.
  full_name: Nadeau, Nicola J.
  last_name: Nadeau
- first_name: Jon R.
  full_name: Bridle, Jon R.
  last_name: Bridle
- first_name: Campbell
  full_name: Rolian, Campbell
  last_name: Rolian
- first_name: Nicholas H
  full_name: Barton, Nicholas H
  id: 4880FE40-F248-11E8-B48F-1D18A9856A87
  last_name: Barton
  orcid: 0000-0002-8548-5240
- first_name: W. Owen
  full_name: McMillan, W. Owen
  last_name: McMillan
- first_name: Chris D.
  full_name: Jiggins, Chris D.
  last_name: Jiggins
- first_name: Yingguang Frank
  full_name: Chan, Yingguang Frank
  last_name: Chan
citation:
  ama: Meier JI, Salazar PA, Kučka M, et al. Haplotype tagging reveals parallel formation
    of hybrid races in two butterfly species. <i>PNAS</i>. 2021;118(25). doi:<a href="https://doi.org/10.1073/pnas.2015005118">10.1073/pnas.2015005118</a>
  apa: 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. <i>PNAS</i>. Proceedings of the National Academy of
    Sciences. <a href="https://doi.org/10.1073/pnas.2015005118">https://doi.org/10.1073/pnas.2015005118</a>
  chicago: 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.” <i>PNAS</i>. Proceedings
    of the National Academy of Sciences, 2021. <a href="https://doi.org/10.1073/pnas.2015005118">https://doi.org/10.1073/pnas.2015005118</a>.
  ieee: J. I. Meier <i>et al.</i>, “Haplotype tagging reveals parallel formation of
    hybrid races in two butterfly species,” <i>PNAS</i>, vol. 118, no. 25. Proceedings
    of the National Academy of Sciences, 2021.
  ista: 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.
  mla: Meier, Joana I., et al. “Haplotype Tagging Reveals Parallel Formation of Hybrid
    Races in Two Butterfly Species.” <i>PNAS</i>, vol. 118, no. 25, e2015005118, Proceedings
    of the National Academy of Sciences, 2021, doi:<a href="https://doi.org/10.1073/pnas.2015005118">10.1073/pnas.2015005118</a>.
  short: J.I. Meier, P.A. Salazar, M. Kučka, R.W. Davies, A. Dréau, I. Aldás, O.B.
    Power, N.J. Nadeau, J.R. Bridle, C. Rolian, N.H. Barton, W.O. McMillan, C.D. Jiggins,
    Y.F. Chan, PNAS 118 (2021).
date_created: 2021-05-07T17:10:21Z
date_published: 2021-06-21T00:00:00Z
date_updated: 2023-08-08T13:33:09Z
day: '21'
ddc:
- '570'
department:
- _id: NiBa
doi: 10.1073/pnas.2015005118
external_id:
  isi:
  - '000671755600001'
  pmid:
  - '34155138'
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intvolume: '       118'
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language:
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license: https://creativecommons.org/licenses/by-nc-nd/4.0/
month: '06'
oa: 1
oa_version: Published Version
pmid: 1
publication: PNAS
publication_identifier:
  eissn:
  - 0027-8424
publication_status: published
publisher: Proceedings of the National Academy of Sciences
quality_controlled: '1'
scopus_import: '1'
status: public
title: Haplotype tagging reveals parallel formation of hybrid races in two butterfly
  species
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volume: 118
year: '2021'
...