Butterfly genome reveals promiscuous exchange of mimicry adaptations among species

Kanchon K. Dasmahapatra; James R. Walters; Adriana D. Briscoe; John W. Davey; Annabel Whibley; Nicola J. Nadeau; Aleksey V. Zimin; Camilo Salazar; Laura C. Ferguson; Simon H. Martin; James J. Lewis; Sebastian Adler; Seung Joon Ahn; Dean A. Baker; Simon W. Baxter; Nicola L. Chamberlain; Chauhan Ritika; Brian A. Counterman; Tamas Dalmay; Lawrence E. Gilbert; Karl Gordon; David G. Heckel; Heather M. Hines; Katharina J. Hoff; Peter W.H. Holland; Emmanuelle Jacquin-Joly; Francis M. Jiggins; Robert T. Jones; Durrell D. Kapan; Paul Kersey; Gerardo Lamas; Daniel Lawson; Daniel Mapleson; Luana S. Maroja; Arnaud Martin; Simon Moxon; William J. Palmer; Riccardo Papa; Alexie Papanicolaou; Yann ick Pauchet; David A. Ray; Neil Rosser; Steven L. Salzberg; Megan A. Supple; Alison Surridge; Ayse Tenger-Trolander; Heiko Vogel; Paul A. Wilkinson; Derek Wilson; James A. Yorke; Furong Yuan; Alexi L. Balmuth; Cathlene Eland; Karim Gharbi; Marian Thomson; Richard A. Gibbs; Yi Han; Joy C. Jayaseelan; Christie Kovar; Tittu Mathew; Donna M. Muzny; Fiona Ongeri; Ling Ling Pu; Jiaxin Qu; Rebecca L. Thornton; Kim C. Worley; Yuan Qing Wu; Mauricio Linares; Mark L. Blaxter; Richard H. ffrench-Constant; Mathieu Joron; Marcus R. Kronforst; Sean P. Mullen; Robert D. Reed; Steven E. Scherer; Stephen Richards; James Mallet; W. Owen Mc Millan; Chris D. Jiggins

doi:10.1038/nature11041

Butterfly genome reveals promiscuous exchange of mimicry adaptations among species

Kanchon K. Dasmahapatra, James R. Walters, Adriana D. Briscoe, John W. Davey, Annabel Whibley, Nicola J. Nadeau, Aleksey V. Zimin, Camilo Salazar, Laura C. Ferguson, Simon H. Martin, James J. Lewis, Sebastian Adler, Seung Joon Ahn, Dean A. Baker, Simon W. Baxter, Nicola L. Chamberlain, Chauhan Ritika, Brian A. Counterman, Tamas Dalmay, Lawrence E. GilbertKarl Gordon, David G. Heckel, Heather M. Hines, Katharina J. Hoff, Peter W.H. Holland, Emmanuelle Jacquin-Joly, Francis M. Jiggins, Robert T. Jones, Durrell D. Kapan, Paul Kersey, Gerardo Lamas, Daniel Lawson, Daniel Mapleson, Luana S. Maroja, Arnaud Martin, Simon Moxon, William J. Palmer, Riccardo Papa, Alexie Papanicolaou, Yann ick Pauchet, David A. Ray, Neil Rosser, Steven L. Salzberg, Megan A. Supple, Alison Surridge, Ayse Tenger-Trolander, Heiko Vogel, Paul A. Wilkinson, Derek Wilson, James A. Yorke, Furong Yuan, Alexi L. Balmuth, Cathlene Eland, Karim Gharbi, Marian Thomson, Richard A. Gibbs, Yi Han, Joy C. Jayaseelan, Christie Kovar, Tittu Mathew, Donna M. Muzny, Fiona Ongeri, Ling Ling Pu, Jiaxin Qu, Rebecca L. Thornton, Kim C. Worley, Yuan Qing Wu, Mauricio Linares, Mark L. Blaxter, Richard H. ffrench-Constant, Mathieu Joron, Marcus R. Kronforst, Sean P. Mullen, Robert D. Reed, Steven E. Scherer, Stephen Richards, James Mallet, W. Owen Mc Millan, Chris D. Jiggins

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Abstract

The evolutionary importance of hybridization and introgression has long been debated. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12, 669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.

Original language	American English
Pages (from-to)	94-98
Number of pages	5
Journal	Nature
Volume	487
Issue number	7405
DOIs	https://doi.org/10.1038/nature11041
State	Published - 5 Jun 2012

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Dasmahapatra, K. K., Walters, J. R., Briscoe, A. D., Davey, J. W., Whibley, A., Nadeau, N. J., Zimin, A. V., Salazar, C., Ferguson, L. C., Martin, S. H., Lewis, J. J., Adler, S., Ahn, S. J., Baker, D. A., Baxter, S. W., Chamberlain, N. L., Ritika, C., Counterman, B. A., Dalmay, T., ... Jiggins, C. D. (2012). Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature, 487(7405), 94-98. https://doi.org/10.1038/nature11041

@article{43ae654facc341f4b33b5de78732434a,

title = "Butterfly genome reveals promiscuous exchange of mimicry adaptations among species",

abstract = "The evolutionary importance of hybridization and introgression has long been debated. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12, 669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.",

author = "Dasmahapatra, {Kanchon K.} and Walters, {James R.} and Briscoe, {Adriana D.} and Davey, {John W.} and Annabel Whibley and Nadeau, {Nicola J.} and Zimin, {Aleksey V.} and Camilo Salazar and Ferguson, {Laura C.} and Martin, {Simon H.} and Lewis, {James J.} and Sebastian Adler and Ahn, {Seung Joon} and Baker, {Dean A.} and Baxter, {Simon W.} and Chamberlain, {Nicola L.} and Chauhan Ritika and Counterman, {Brian A.} and Tamas Dalmay and Gilbert, {Lawrence E.} and Karl Gordon and Heckel, {David G.} and Hines, {Heather M.} and Hoff, {Katharina J.} and Holland, {Peter W.H.} and Emmanuelle Jacquin-Joly and Jiggins, {Francis M.} and Jones, {Robert T.} and Kapan, {Durrell D.} and Paul Kersey and Gerardo Lamas and Daniel Lawson and Daniel Mapleson and Maroja, {Luana S.} and Arnaud Martin and Simon Moxon and Palmer, {William J.} and Riccardo Papa and Alexie Papanicolaou and Pauchet, {Yann ick} and Ray, {David A.} and Neil Rosser and Salzberg, {Steven L.} and Supple, {Megan A.} and Alison Surridge and Ayse Tenger-Trolander and Heiko Vogel and Wilkinson, {Paul A.} and Derek Wilson and Yorke, {James A.} and Furong Yuan and Balmuth, {Alexi L.} and Cathlene Eland and Karim Gharbi and Marian Thomson and Gibbs, {Richard A.} and Yi Han and Jayaseelan, {Joy C.} and Christie Kovar and Tittu Mathew and Muzny, {Donna M.} and Fiona Ongeri and Pu, {Ling Ling} and Jiaxin Qu and Thornton, {Rebecca L.} and Worley, {Kim C.} and Wu, {Yuan Qing} and Mauricio Linares and Blaxter, {Mark L.} and ffrench-Constant, {Richard H.} and Mathieu Joron and Kronforst, {Marcus R.} and Mullen, {Sean P.} and Reed, {Robert D.} and Scherer, {Steven E.} and Stephen Richards and James Mallet and {Mc Millan}, {W. Owen} and Jiggins, {Chris D.}",

year = "2012",

month = jun,

day = "5",

doi = "10.1038/nature11041",

language = "American English",

volume = "487",

pages = "94--98",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Publishing Group",

number = "7405",

}

Dasmahapatra, KK, Walters, JR, Briscoe, AD, Davey, JW, Whibley, A, Nadeau, NJ, Zimin, AV, Salazar, C, Ferguson, LC, Martin, SH, Lewis, JJ, Adler, S, Ahn, SJ, Baker, DA, Baxter, SW, Chamberlain, NL, Ritika, C, Counterman, BA, Dalmay, T, Gilbert, LE, Gordon, K, Heckel, DG, Hines, HM, Hoff, KJ, Holland, PWH, Jacquin-Joly, E, Jiggins, FM, Jones, RT, Kapan, DD, Kersey, P, Lamas, G, Lawson, D, Mapleson, D, Maroja, LS, Martin, A, Moxon, S, Palmer, WJ, Papa, R, Papanicolaou, A, Pauchet, YI, Ray, DA, Rosser, N, Salzberg, SL, Supple, MA, Surridge, A, Tenger-Trolander, A, Vogel, H, Wilkinson, PA, Wilson, D, Yorke, JA, Yuan, F, Balmuth, AL, Eland, C, Gharbi, K, Thomson, M, Gibbs, RA, Han, Y, Jayaseelan, JC, Kovar, C, Mathew, T, Muzny, DM, Ongeri, F, Pu, LL, Qu, J, Thornton, RL, Worley, KC, Wu, YQ, Linares, M, Blaxter, ML, ffrench-Constant, RH, Joron, M, Kronforst, MR, Mullen, SP, Reed, RD, Scherer, SE, Richards, S, Mallet, J, Mc Millan, WO & Jiggins, CD 2012, 'Butterfly genome reveals promiscuous exchange of mimicry adaptations among species', Nature, vol. 487, no. 7405, pp. 94-98. https://doi.org/10.1038/nature11041

TY - JOUR

T1 - Butterfly genome reveals promiscuous exchange of mimicry adaptations among species

AU - Dasmahapatra, Kanchon K.

AU - Walters, James R.

AU - Briscoe, Adriana D.

AU - Davey, John W.

AU - Whibley, Annabel

AU - Nadeau, Nicola J.

AU - Zimin, Aleksey V.

AU - Salazar, Camilo

AU - Ferguson, Laura C.

AU - Martin, Simon H.

AU - Lewis, James J.

AU - Adler, Sebastian

AU - Ahn, Seung Joon

AU - Baker, Dean A.

AU - Baxter, Simon W.

AU - Chamberlain, Nicola L.

AU - Ritika, Chauhan

AU - Counterman, Brian A.

AU - Dalmay, Tamas

AU - Gilbert, Lawrence E.

AU - Gordon, Karl

AU - Heckel, David G.

AU - Hines, Heather M.

AU - Hoff, Katharina J.

AU - Holland, Peter W.H.

AU - Jacquin-Joly, Emmanuelle

AU - Jiggins, Francis M.

AU - Jones, Robert T.

AU - Kapan, Durrell D.

AU - Kersey, Paul

AU - Lamas, Gerardo

AU - Lawson, Daniel

AU - Mapleson, Daniel

AU - Maroja, Luana S.

AU - Martin, Arnaud

AU - Moxon, Simon

AU - Palmer, William J.

AU - Papa, Riccardo

AU - Papanicolaou, Alexie

AU - Pauchet, Yann ick

AU - Ray, David A.

AU - Rosser, Neil

AU - Salzberg, Steven L.

AU - Supple, Megan A.

AU - Surridge, Alison

AU - Tenger-Trolander, Ayse

AU - Vogel, Heiko

AU - Wilkinson, Paul A.

AU - Wilson, Derek

AU - Yorke, James A.

AU - Yuan, Furong

AU - Balmuth, Alexi L.

AU - Eland, Cathlene

AU - Gharbi, Karim

AU - Thomson, Marian

AU - Gibbs, Richard A.

AU - Han, Yi

AU - Jayaseelan, Joy C.

AU - Kovar, Christie

AU - Mathew, Tittu

AU - Muzny, Donna M.

AU - Ongeri, Fiona

AU - Pu, Ling Ling

AU - Qu, Jiaxin

AU - Thornton, Rebecca L.

AU - Worley, Kim C.

AU - Wu, Yuan Qing

AU - Linares, Mauricio

AU - Blaxter, Mark L.

AU - ffrench-Constant, Richard H.

AU - Joron, Mathieu

AU - Kronforst, Marcus R.

AU - Mullen, Sean P.

AU - Reed, Robert D.

AU - Scherer, Steven E.

AU - Richards, Stephen

AU - Mallet, James

AU - Mc Millan, W. Owen

AU - Jiggins, Chris D.

PY - 2012/6/5

Y1 - 2012/6/5

N2 - The evolutionary importance of hybridization and introgression has long been debated. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12, 669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.

AB - The evolutionary importance of hybridization and introgression has long been debated. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12, 669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.

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U2 - 10.1038/nature11041

DO - 10.1038/nature11041

M3 - Article

SN - 0028-0836

VL - 487

SP - 94

EP - 98

JO - Nature

JF - Nature

IS - 7405

ER -

Butterfly genome reveals promiscuous exchange of mimicry adaptations among species

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