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

Heredity

Volumn 114, Issue 5, 2015, Pages 515-524

  Huber, B ^a,b,c   Whibley, A ^a   Poul, Y L ^a   Navarro, N ^b,d   Martin, A ^e   Baxter, S ^f,g   Shah, A ^a,h   Gilles, B ^a,c   Wirth, T ^a,b   McMillan, W O ^c   Joron, M ^a,c  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b PSL RESEARCH UNIVERSITY   (France)

^c SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^d UNIVERSITÉ DE BOURGOGNE   (France)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF ADELAIDE   (Australia)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^h BIELEFELD UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; BUTTERFLY; CLADISTICS; CONSERVATION GENETICS; GENOTYPE; MULTIVARIATE ANALYSIS; PHENOTYPIC PLASTICITY;

HELICONIUS; HELICONIUS HECALE; HELICONIUS ISMENIUS; HELICONIUS MELPOMENE; HELICONIUS NUMATA; PAPILIONOIDEA;

ADAPTATION; ANATOMY AND HISTOLOGY; ANIMAL; BUTTERFLY; CHROMOSOME MAP; COLOR; CROSS BREEDING; EVOLUTION; FORELIMB; GENETICS; GENOTYPE; PHENOTYPE; QUANTITATIVE TRAIT LOCUS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; BUTTERFLIES; CHROMOSOME MAPPING; COLOR; CROSSES, GENETIC; GENOTYPE; PHENOTYPE; QUANTITATIVE TRAIT LOCI; WING;

EID: 84928207795     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2015.22     Document Type: Article

References (57)

1. Arendt J, Reznick D (2008). Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol Evol 23: 26-32.
2. Barton NH (1995). A general model for the evolution of recombination. Genet Res 65: 123-145.
3. Baxter SW, Johnston SE, Jiggins CD (2008). Butterfly speciation and the distribution of gene effect sizes fixed during adaptation. Heredity 102: 57-65.
4. Broman K, Sen S (2009). A Guide to QTL Mapping with R/qtl. Springer: New York.
5. Broman KW, Wu H, Sen S, Churchill GA (2003). R/qtl: QTL mapping in experimental crosses. Bioinforma Oxf Engl 19: 889-890.
6. Brown KS (1981). The biology of Heliconius and related genera. Annu Rev Entomol 26: 427-457.
7. Brown Jr KS, Benson WW (1974). Adaptive polymorphism associated with multiple Müllerian mimicry in Heliconius numata (Lepid. Nymph.). Biotropica 6: 205-228.
8. Browning BL, Browning SR (2009). A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. Am J Hum Genet 84: 210-223.
9. Carter AJR, Hermisson J, Hansen TF (2005). The role of epistatic gene interactions in the response to selection and the evolution of evolvability. Theor Popul Biol 68: 179-196.
10. Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013). Stacks: an analysis tool set for population genomics. Mol Ecol 22: 3124-3140.
11. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C et al. (2011). A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491-498.
12. De Visser JA, Hoekstra RF, van den Ende H (1997). An experimental test for synergistic epistasis and its application in Chlamydomonas. Genetics 145: 815-819.
13. Elmer KR, Meyer A (2011). Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends Ecol Evol 26: 298-306.
14. Ferguson L, Lee SF, Chamberlain N, Nadeau N, Joron M, Baxter S et al. (2010). Characterization of a hotspot for mimicry: assembly of a butterfly wing transcriptome to genomic sequence at the HmYb/Sb locus. Mol Ecol 19: 240-254.
15. Gilbert LE (2003). Adaptive novelty through introgression in Heliconius wing patterns: evidence for shared genetic 'tool box' from synthetic hybrid zones and a theory of diversification. In: Boggs CL, Watt WB, Ehrlich PR (eds). Butterflies: Ecology and Evolution Taking Flight. University of Chicago Press: Chicago.
16. Hansen TF (2006). The evolution of genetic architecture. Annu Rev Ecol Evol Syst 37: 123-157.
17. Heliconius Genome Consortium (2012). Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487: 94-98.
18. Holzinger H, Holzinger R (1994). Heliconius and Related Genera. Lepidoptera: Nymphalidae. The Genera Eueides, Neruda and Heliconius. Sciences Nat.: Vennette, France. 328 pages.
19. Jiggins CD, Mavarez J, Beltrán M, McMillan WO, Johnston JS, Bermingham E (2005). A genetic linkage map of the mimetic butterfly Heliconius melpomene. Genetics 171: 557-570.
20. Jiggins CD, Naisbit RE, Coe RL, Mallet J (2001). Reproductive isolation caused by colour pattern mimicry. Nature 411: 302-305.
21. Jiggins CD, McMillan WO (1997). The genetic basis of an adaptive radiation: warning colour in two Heliconius species. Proc R Soc B Biol Sci 264: 1167-1175.
22. Jones RT, Salazar PA, ffrench-Constant RH, Jiggins CD, Joron M (2011). Evolution of a mimicry supergene from a multilocus architecture. Proc Biol Sci 279: 316-325.
23. Joron M, Frezal L, Jones RT, Chamberlain NL, Lee SF, Haag CR et al. (2011). Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477: 203-206.
24. Joron M, Papa R, Beltrán M, Chamberlain N, Mavárez J, Baxter S et al. (2006). A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biol 4: e303.
25. Joron M, Wynne IR, Lamas G, Mallet J (1999). Variable selection and the coexistence of multiple mimetic forms of the butterfly Heliconius numata. Evol Ecol 13: 721-754.
26. Kapan DD (2001). Three-butterfly system provides a field test of müllerian mimicry. Nature 409: 338-340.
27. Kronforst MR, Kapan DD, Gilbert LE (2006a). Parallel genetic architecture of parallel adaptive radiations in mimetic Heliconius butterflies. Genetics 174: 535-539.
28. Kronforst MR, Young LG, Kapan DD, McNeely C, O'Neill RJ, Gilbert LE (2006b). Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proc Natl Acad Sci USA 103: 6575-6580.
29. Lair KP, Bradshaw WE, Holzapfel CM (1997). Evolutionary divergence of the genetic architecture underlying photoperiodism in the pitcher-plant mosquito, Wyeomyia Smithii. Genetics 147: 1873.
30. Lande R (1980). The genetic covariance between characters maintained by pleiotropic mutations. Genetics 94: 203-215.
31. Le Poul Y, Whibley A, Chouteau M, Prunier F, Llaurens V, Joron M (2014). Evolution of dominance mechanisms at a butterfly mimicry supergene. Nat Commun 5: 5644.
32. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N et al. (2009). The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079.
33. Linares M (1996). The genetics of the mimetic coloration in the butterfly Heliconius cydno weymeri. J Hered 87: 142-149.
34. Lunter G, Goodson M (2011). Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res 21: 936-939.
35. Mallet J (1989). The genetics of warning colour in peruvian hybrid zones of Heliconius erato and H. melpomene. Proc R Soc Lond B Biol Sci 236: 163-185.
36. Manceau M, Domingues VS, Linnen CR, Rosenblum EB, Hoekstra HE (2010). Convergence in pigmentation at multiple levels: mutations, genes and function. Philos Trans R Soc B Biol Sci 365: 2439-2450.
37. Martin A, McCulloch KJ, Patel NH, Briscoe AD, Gilbert LE, Reed RD (2014). Multiple recent co-options of Optix associated with novel traits in adaptive butterfly wing radiations. EvoDevo 5: 7.
38. Martin A, Orgogozo V (2013). The loci of repeated evolution: a catalog of genetic hotspots of phenotypic variation. Evolution 67: 1235-1250.
39. Martin A, Papa R, Nadeau NJ, Hill RI, Counterman BA, Halder G et al. (2012). Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand. Proc Natl Acad Sci USA 109: 12632-12637.
40. Nadeau NJ, Ruiz M, Salazar P, Counterman B, Medina JA, Ortiz-Zuazaga H et al. (2014). Population genomics of parallel hybrid zones in the mimetic butterflies, H. melpomene and H. erato. Genome Res 24: 1316-1333.
41. Nadeau NJ, Whibley A, Jones RT, Davey JW, Dasmahapatra KK, Baxter SW et al. (2012). Genomic islands of divergence in hybridizing Heliconius butterflies identified by slarge-scale targeted sequencing. Philos Trans R Soc Lond B Biol Sci 367: 343-353.
42. Naisbit RE, Jiggins CD, Mallet J (2003). Mimicry: developmental genes that contribute to speciation. Evol Dev 5: 269-280.
43. Nijhout HF, Wray GA, Gilbert LE (1990). An analysis of the phenotypic effects of certain colour pattern genes in Heliconius (Lepidoptera: Nymphalidae). Biol J Linn Soc 40: 357-372.
44. Orr HA (1998). The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52: 935-949.
45. Papa R, Kapan DD, Counterman BA, Maldonado K, Lindstrom DP, Reed RD et al. (2013). Multi-allelic major effect genes interact with minor effect QTLs to control adaptive color pattern variation in Heliconius erato. PLoS ONE 8: e57033.
46. Papa R, Martin A, Reed RD (2008). Genomic hotspots of adaptation in butterfly wing pattern evolution. Curr Opin Genet Dev 18: 559-564.
47. Pardo-Diaz C, Salazar C, Baxter SW, Merot C, Figueiredo-Ready W, Joron M et al. (2012). Adaptive introgression across species boundaries in Heliconius Butterflies. PLoS Genet 8: e1002752.
48. Reed RD, Papa R, Martin A, Hines HM, Counterman BA, Pardo-Diaz C et al. (2011). optix drives the repeated convergent evolution of butterfly wing patternmimicry. Science 333: 1137-1141.
49. Sheppard PM, Turner JRG, Brown KS, Benson WW, Singer MC (1985). Genetics and the evolution of muellerian mimicry in Heliconius Butterflies. Philos Trans R Soc Lond B Biol Sci 308: 433-610.
50. Stern DL (2013). The genetic causes of convergent evolution. Nat Rev Genet 14: 751-764.
51. Stinchcombe JR, Hoekstra HE (2007). Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100: 158-170.
52. Supple MA, Hines HM, Dasmahapatra KK, Lewis JJ, Nielsen DM, Lavoie C et al. (2013). Genomic architecture of adaptive color pattern divergence and convergence in Heliconius butterflies. Genome Res 23: 1248-1257.
53. Thompson MJ, Jiggins CD (2014). Supergenes and their role in evolution. Heredity 113: 1-8.
54. Turner JR (1977). Butterfly mimicry: the genetical evolution of an adaptation. Evol Biol 10: 163-206.
55. Turner JRG, Sheppard PM (1975). Absence of crossing-over in female butterflies (Heliconius). Heredity 34: 265-269.
56. Van Oijen JW, Voorrips RE (2001). Joinmap Version 3.0, software for the calculation of genetic linkage maps. Plant Res Int; Wageningen, the Netherlands.
57. Wu GC, Joron M, Jiggins CD (2010). Signatures of selection in loci governing major colour patterns in Heliconius butterflies and related species. BMC Evol Biol 10: 368.