Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies

Huber B, Whibley A, Poul YL, Navarro N, Martin A, Baxter S, Shah A, Gilles B, Wirth T, McMillan WO, Joron M (2015)
Heredity 114(5): 515-524.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Huber, B.; Whibley, A.; Poul, Y. L.; Navarro, N.; Martin, A.; Baxter, S.; Shah, AbhijeetUniBi; Gilles, B.; Wirth, T.; McMillan, W. O.; Joron, M.
Abstract / Bemerkung
Understanding the genetic architecture of adaptive traits has been at the centre of modern evolutionary biology since Fisher; however, evaluating how the genetic architecture of ecologically important traits influences their diversification has been hampered by the scarcity of empirical data. Now, high-throughput genomics facilitates the detailed exploration of variation in the genome-to-phenotype map among closely related taxa. Here, we investigate the evolution of wing pattern diversity in Heliconius, a clade of neotropical butterflies that have undergone an adaptive radiation for wing-pattern mimicry and are influenced by distinct selection regimes. Using crosses between natural wing-pattern variants, we used genome-wide restriction site-associated DNA (RAD) genotyping, traditional linkage mapping and multivariate image analysis to study the evolution of the architecture of adaptive variation in two closely related species: Heliconius hecale and H. ismenius. We implemented a new morphometric procedure for the analysis of whole-wing pattern variation, which allows visualising spatial heatmaps of genotype-to-phenotype association for each quantitative trait locus separately. We used the H. melpomene reference genome to fine-map variation for each major wing-patterning region uncovered, evaluated the role of candidate genes and compared genetic architectures across the genus. Our results show that, although the loci responding to mimicry selection are highly conserved between species, their effect size and phenotypic action vary throughout the clade. Multilocus architecture is ancestral and maintained across species under directional selection, whereas the single-locus (supergene) inheritance controlling polymorphism in H. numata appears to have evolved only once. Nevertheless, the conservatism in the wing-patterning toolkit found throughout the genus does not appear to constrain phenotypic evolution towards local adaptive optima.
Page URI


Huber B, Whibley A, Poul YL, et al. Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies. Heredity. 2015;114(5):515-524.
Huber, B., Whibley, A., Poul, Y. L., Navarro, N., Martin, A., Baxter, S., Shah, A., et al. (2015). Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies. Heredity, 114(5), 515-524. doi:10.1038/hdy.2015.22
Huber, B., Whibley, A., Poul, Y. L., Navarro, N., Martin, A., Baxter, S., Shah, Abhijeet, et al. 2015. “Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies”. Heredity 114 (5): 515-524.
Huber, B., Whibley, A., Poul, Y. L., Navarro, N., Martin, A., Baxter, S., Shah, A., Gilles, B., Wirth, T., McMillan, W. O., et al. (2015). Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies. Heredity 114, 515-524.
Huber, B., et al., 2015. Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies. Heredity, 114(5), p 515-524.
B. Huber, et al., “Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies”, Heredity, vol. 114, 2015, pp. 515-524.
Huber, B., Whibley, A., Poul, Y.L., Navarro, N., Martin, A., Baxter, S., Shah, A., Gilles, B., Wirth, T., McMillan, W.O., Joron, M.: Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies. Heredity. 114, 515-524 (2015).
Huber, B., Whibley, A., Poul, Y. L., Navarro, N., Martin, A., Baxter, S., Shah, Abhijeet, Gilles, B., Wirth, T., McMillan, W. O., and Joron, M. “Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies”. Heredity 114.5 (2015): 515-524.

15 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Diversity in warning coloration: selective paradox or the norm?
Briolat ES, Burdfield-Steel ER, Paul SC, Rönkä KH, Seymoure BM, Stankowich T, Stuckert AMM., Biol Rev Camb Philos Soc 94(2), 2019
PMID: 30152037
Discrete or indiscrete? Redefining the colour polymorphism of the land snail Cepaea nemoralis.
Davison A, Jackson HJ, Murphy EW, Reader T., Heredity (Edinb) 123(2), 2019
PMID: 30804571
Complex modular architecture around a simple toolkit of wing pattern genes.
Van Belleghem SM, Rastas P, Papanicolaou A, Martin SH, Arias CF, Supple MA, Hanly JJ, Mallet J, Lewis JJ, Hines HM, Ruiz M, Salazar C, Linares M, Moreira GRP, Jiggins CD, Counterman BA, McMillan WO, Papa R., Nat Ecol Evol 1(3), 2017
PMID: 28523290
Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?
Jiggins CD, Wallbank RW, Hanly JJ., Philos Trans R Soc Lond B Biol Sci 372(1713), 2017
PMID: 27994126
Young inversion with multiple linked QTLs under selection in a hybrid zone.
Lee CR, Wang B, Mojica JP, Mandáková T, Prasad KVSK, Goicoechea JL, Perera N, Hellsten U, Hundley HN, Johnson J, Grimwood J, Barry K, Fairclough S, Jenkins JW, Yu Y, Kudrna D, Zhang J, Talag J, Golser W, Ghattas K, Schranz ME, Wing R, Lysak MA, Schmutz J, Rokhsar DS, Mitchell-Olds T., Nat Ecol Evol 1(5), 2017
PMID: 28812690
Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures.
Chouteau M, Llaurens V, Piron-Prunier F, Joron M., Proc Natl Acad Sci U S A 114(31), 2017
PMID: 28673971
Macroevolutionary shifts of WntA function potentiate butterfly wing-pattern diversity.
Mazo-Vargas A, Concha C, Livraghi L, Massardo D, Wallbank RWR, Zhang L, Papador JD, Martinez-Najera D, Jiggins CD, Kronforst MR, Breuker CJ, Reed RD, Patel NH, McMillan WO, Martin A., Proc Natl Acad Sci U S A 114(40), 2017
PMID: 28923954
Crossing fitness valleys: empirical estimation of a fitness landscape associated with polymorphic mimicry.
Arias M, le Poul Y, Chouteau M, Boisseau R, Rosser N, Théry M, Llaurens V., Proc Biol Sci 283(1829), 2016
PMID: 27122560
The genetic basis of discrete and quantitative colour variation in the polymorphic lizard, Ctenophorus decresii.
Rankin KJ, McLean CA, Kemp DJ, Stuart-Fox D., BMC Evol Biol 16(), 2016
PMID: 27600682
The diversification of Heliconius butterflies: what have we learned in 150 years?
Merrill RM, Dasmahapatra KK, Davey JW, Dell'Aglio DD, Hanly JJ, Huber B, Jiggins CD, Joron M, Kozak KM, Llaurens V, Martin SH, Montgomery SH, Morris J, Nadeau NJ, Pinharanda AL, Rosser N, Thompson MJ, Vanjari S, Wallbank RW, Yu Q., J Evol Biol 28(8), 2015
PMID: 26079599
Replaying the tape of life in the twenty-first century.
Orgogozo V., Interface Focus 5(6), 2015
PMID: 26640652

57 References

Daten bereitgestellt von Europe PubMed Central.

Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation?
Arendt J, Reznick D., Trends Ecol. Evol. (Amst.) 23(1), 2007
PMID: 18022278
A general model for the evolution of recombination.
Barton NH., Genet. Res. 65(2), 1995
PMID: 7605514
Butterfly speciation and the distribution of gene effect sizes fixed during adaptation.
Baxter SW, Johnston SE, Jiggins CD., Heredity (Edinb) 102(1), 2008
PMID: 18985063

R/qtl: QTL mapping in experimental crosses
The biology of Heliconius and related genera
Adaptive polymorphism associated with multiple Müllerian mimicry in Heliconius numata (Lepid. Nymph.)
The role of epistatic gene interactions in the response to selection and the evolution of evolvability.
Carter AJ, Hermisson J, Hansen TF., Theor Popul Biol 68(3), 2005
PMID: 16122771
Stacks: an analysis tool set for population genomics.
Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA., Mol. Ecol. 22(11), 2013
PMID: 23701397
A framework for variation discovery and genotyping using next-generation DNA sequencing data.
DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ., Nat. Genet. 43(5), 2011
PMID: 21478889
An experimental test for synergistic epistasis and its application in Chlamydomonas.
de Visser JA, Hoekstra RF, van den Ende H., Genetics 145(3), 1997
PMID: 9055090
Adaptation in the age of ecological genomics: insights from parallelism and convergence.
Elmer KR, Meyer A., Trends Ecol. Evol. (Amst.) 26(6), 2011
PMID: 21459472
Characterization of a hotspot for mimicry: assembly of a butterfly wing transcriptome to genomic sequence at the HmYb/Sb locus.
Ferguson L, Lee SF, Chamberlain N, Nadeau N, Joron M, Baxter S, Wilkinson P, Papanicolaou A, Kumar S, Kee TJ, Clark R, Davidson C, Glithero R, Beasley H, Vogel H, Ffrench-Constant R, Jiggins C., Mol. Ecol. 19 Suppl 1(), 2010
PMID: 20331783
Adaptive novelty through introgression in Heliconius wing patterns: evidence for shared genetic ‘tool box' from synthetic hybrid zones and a theory of diversification
The evolution of genetic architecture
Butterfly genome reveals promiscuous exchange of mimicry adaptations among species.
Heliconius Genome Consortium, Dasmahapatra KK, Walters JR, Briscoe AD, Davey JW, Whibley A, Nadeau NJ, Zimin AV, Hughes DS, Ferguson LC, Martin SH, Salazar C, Lewis JJ, Adler S, Ahn SJ, Baker DA, Baxter SW, Chamberlain NL, Chauhan R, Counterman BA, Dalmay T, Gilbert LE, Gordon K, Heckel DG, Hines HM, Hoff KJ, Holland PW, 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 Y, 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, McMillan W, Jiggins CD., Nature 487(7405), 2012
PMID: 22722851

A genetic linkage map of the mimetic butterfly Heliconius melpomene.
Jiggins CD, Mavarez J, Beltran M, McMillan WO, Johnston JS, Bermingham E., Genetics 171(2), 2004
PMID: 15489522
Reproductive isolation caused by colour pattern mimicry.
Jiggins CD, Naisbit RE, Coe RL, Mallet J., Nature 411(6835), 2001
PMID: 11357131
The genetic basis of an adaptive radiation: warning colour in two Heliconius species
Evolution of a mimicry supergene from a multilocus architecture.
Jones RT, Salazar PA, ffrench-Constant RH, Jiggins CD, Joron M., Proc. Biol. Sci. 279(1727), 2011
PMID: 21676976
Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry.
Joron M, Frezal L, Jones RT, Chamberlain NL, Lee SF, Haag CR, Whibley A, Becuwe M, Baxter SW, Ferguson L, Wilkinson PA, Salazar C, Davidson C, Clark R, Quail MA, Beasley H, Glithero R, Lloyd C, Sims S, Jones MC, Rogers J, Jiggins CD, ffrench-Constant RH., Nature 477(7363), 2011
PMID: 21841803
A conserved supergene locus controls colour pattern diversity in Heliconius butterflies.
Joron M, Papa R, Beltran M, Chamberlain N, Mavarez J, Baxter S, Abanto M, Bermingham E, Humphray SJ, Rogers J, Beasley H, Barlow K, ffrench-Constant RH, Mallet J, McMillan WO, Jiggins CD., PLoS Biol. 4(10), 2006
PMID: 17002517
Variable selection and the coexistence of multiple mimetic forms of the butterfly Heliconius numata
Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless.
Kronforst MR, Young LG, Kapan DD, McNeely C, O'Neill RJ, Gilbert LE., Proc. Natl. Acad. Sci. U.S.A. 103(17), 2006
PMID: 16611733
Evolution of dominance mechanisms at a butterfly mimicry supergene.
Le Poul Y, Whibley A, Chouteau M, Prunier F, Llaurens V, Joron M., Nat Commun 5(), 2014
PMID: 25429605
The Sequence Alignment/Map format and SAMtools.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R; 1000 Genome Project Data Processing Subgroup., Bioinformatics 25(16), 2009
PMID: 19505943
The genetics of the mimetic coloration in the butterfly Heliconius cydno weymeri
The genetics of warning colour in peruvian hybrid zones of Heliconius erato and H. melpomene
Convergence in pigmentation at multiple levels: mutations, genes and function
Multiple recent co-options of Optix associated with novel traits in adaptive butterfly wing radiations.
Martin A, McCulloch KJ, Patel NH, Briscoe AD, Gilbert LE, Reed RD., Evodevo 5(1), 2014
PMID: 24499528
Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand.
Martin A, Papa R, Nadeau NJ, Hill RI, Counterman BA, Halder G, Jiggins CD, Kronforst MR, Long AD, McMillan WO, Reed RD., Proc. Natl. Acad. Sci. U.S.A. 109(31), 2012
PMID: 22802635
Population genomics of parallel hybrid zones in the mimetic butterflies, H. melpomene and H. erato.
Nadeau NJ, Ruiz M, Salazar P, Counterman B, Medina JA, Ortiz-Zuazaga H, Morrison A, McMillan WO, Jiggins CD, Papa R., Genome Res. 24(8), 2014
PMID: 24823669
Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing.
Nadeau NJ, Whibley A, Jones RT, Davey JW, Dasmahapatra KK, Baxter SW, Quail MA, Joron M, ffrench-Constant RH, Blaxter ML, Mallet J, Jiggins CD., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 367(1587), 2012
PMID: 22201164
Mimicry: developmental genes that contribute to speciation.
Naisbit RE, Jiggins CD, Mallet J., Evol. Dev. 5(3), 2003
PMID: 12752766
An analysis of the phenotypic effects of certain colour pattern genes in Heliconius (Lepidoptera: Nymphalidae)
Multi-allelic major effect genes interact with minor effect QTLs to control adaptive color pattern variation in Heliconius erato.
Papa R, Kapan DD, Counterman BA, Maldonado K, Lindstrom DP, Reed RD, Nijhout HF, Hrbek T, McMillan WO., PLoS ONE 8(3), 2013
PMID: 23533571
Genomic hotspots of adaptation in butterfly wing pattern evolution.
Papa R, Martin A, Reed RD., Curr. Opin. Genet. Dev. 18(6), 2008
PMID: 19135357
Adaptive introgression across species boundaries in Heliconius butterflies.
Pardo-Diaz C, Salazar C, Baxter SW, Merot C, Figueiredo-Ready W, Joron M, McMillan WO, Jiggins CD., PLoS Genet. 8(6), 2012
PMID: 22737081
optix drives the repeated convergent evolution of butterfly wing pattern mimicry.
Reed RD, Papa R, Martin A, Hines HM, Counterman BA, Pardo-Diaz C, Jiggins CD, Chamberlain NL, Kronforst MR, Chen R, Halder G, Nijhout HF, McMillan WO., Science 333(6046), 2011
PMID: 21778360
Genetics and the evolution of muellerian mimicry in Heliconius Butterflies
The genetic causes of convergent evolution.
Stern DL., Nat. Rev. Genet. 14(11), 2013
PMID: 24105273
Genomic architecture of adaptive color pattern divergence and convergence in Heliconius butterflies.
Supple MA, Hines HM, Dasmahapatra KK, Lewis JJ, Nielsen DM, Lavoie C, Ray DA, Salazar C, McMillan WO, Counterman BA., Genome Res. 23(8), 2013
PMID: 23674305
Supergenes and their role in evolution.
Thompson MJ, Jiggins CD., Heredity (Edinb) 113(1), 2014
PMID: 24642887
Butterfly mimicry: the genetical evolution of an adaptation
Absence of crossing-over in female butterflies (Heliconius).
Turner JR, Sheppard PM., Heredity (Edinb) 34 Part 2(), 1975
PMID: 1055712
Joinmap Version 3.0, software for the calculation of genetic linkage maps

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

PMID: 25806542
PubMed | Europe PMC

Suchen in

Google Scholar