Ancient homology underlies adaptive mimetic diversity across butterflies

Nature Communications

Volumn 5, Issue , 2014, Pages

  Gallant, Jason R ^a   Imhoff, Vance E ^b   Martin, Arnaud ^c   Savage, Wesley K ^b,f   Chamberlain, Nicola L ^b   Pote, Ben L ^b   Peterson, Chelsea ^b   Smith, Gabriella E ^b   Evans, Benjamin ^d   Reed, Robert D ^c   Kronforst, Marcus R ^e   Mullen, Sean P ^b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Boston University   (United States)

^c Department of Obstetrics Gynecology   (United States)

^d YALE UNIVERSITY   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

^f University of Massachusetts Lowell   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDE; WNT PROTEIN;

BUTTERFLY; CONVERGENT EVOLUTION; HOMOLOGY; IMMUNITY; MIMICRY; MOLECULAR ANALYSIS; PHENOTYPIC PLASTICITY; WING;

ARTICLE; BUTTERFLY; CLONING; CONTROLLED STUDY; EVOLUTIONARY HOMOLOGY; FORELIMB; GENE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; NONHUMAN; REGULATORY MECHANISM; WNTA GENE; ANIMAL; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR EVOLUTION; PHENOTYPE; PIGMENTATION; SEQUENCE HOMOLOGY;

PAPILIONOIDEA;

ANIMALS; BIOLOGICAL EVOLUTION; BUTTERFLIES; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; GENETIC VARIATION; GENOME; PHENOTYPE; PIGMENTATION; SEQUENCE HOMOLOGY, NUCLEIC ACID; WING; WNT PROTEINS;

EID: 84908122557     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5817     Document Type: Article

References (61)

1. Mayr, E. Animal Species and Evolution (Harvard University Press, 1963).
2. Steiner, C. C., Rompler, H., Boettger, L. M., Schoneberg, T. & Hoekstra, H. E. The genetic basis of phenotypic convergence in beach mice: similar pigment patterns but different genes. Mol. Biol. Evol. 26, 35-45 (2009).
3. Gross, J. B., Borowsky, R. & Tabin, C. J. A novel role for Mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax mexicanus. PLoS Genet. 5, e1000326 (2009).
4. Rosenblum, E. B., Rompler, H., Schoneberg, T. & Hoekstra, H. E. Molecular and functional basis of phenotypic convergence in white lizards at White Sands. Proc. Natl Acad. Sci. USA 107, 2113-2117 (2010).
5. Chan, Y. F. et al. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302-305 (2010).
6. Conte, G. L., Arnegard, M. E., Peichel, C. L. & Schluter, D. The probability of genetic parallelism and convergence in natural populations. Proc. Biol. Sci. 279, 5039-5047 (2012).
7. Tenaillon, O. et al. The molecular diversity of adaptive convergence. Science 335, 457-461 (2012).
8. Sobel, J. M. & Streisfeld, M. A. Flower color as a model system for studies of plant evo-devo. Front. Plant Sci. 4, 321 (2013).
9. Nijhout, F. H. The Development and Evolution of Butterfly Wing Patterns (Smithsonian Institution Scholarly Press, 1991).
10. Wittkopp, P. et al. Intraspecific polymorphism to interspecific divergence: genetics of pigmentation in Drosophila. Science 326, 540-544 (2009).
11. Hubbard, J. K., Uy, J. A. C., Hauber, M. E., Hoekstra, H. E. & Safran, R. J. Vertebrate pigmentation: from underlying genes to adaptive function. Trends Genet. 26, 231-239 (2010).
12. Hoekstra, H. E. Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity 97, 222-234 (2006).
13. Manceau,M., Domingues, V. S., Linnen, C. R., Rosenblum, E. B. & Hoekstra, H. E. Convergence in pigmentation at multiple levels: mutations, genes and function. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 2439-2450 (2010).
14. Kronforst, M. R. et al. Unraveling the thread of nature's tapestry: the genetics of diversity and convergence in animal pigmentation. Pigment. Cell Melanoma Res. 25, 411-433 (2012).
15. Brunetti, C. R. et al. The generation and diversification of butterfly eyespot color patterns. Curr. Biol. 11, 1578-1585 (2001).
16. Shirai, L. T. et al. Evolutionary history of the recruitment of conserved developmental genes in association to the formation and diversification of a novel trait. BMC Evol. Biol. 12, 21 (2012).
17. Oliver, J. C., Tong, X. L., Gall, L. F., Piel, W. H. & Monteiro, A. A single origin for nymphalid butterfly eyespots followed by widespread loss of associated gene expression. PLoS Genet. 8, e1002893 (2012).
18. Reed, R. D. et al. Optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333, 1137-1141 (2011).
19. Mullen, S. P., Dopman, E. B. & Harrison, R. G. Hybrid zone origins, species boundaries, and the evolution of wing-pattern diversity in a polytypic species complex of North American admiral butterflies (Nymphalidae: Limenitis). Evolution 62, 1400-1417 (2008).
20. Martin, A. et al. Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand. Proc. Natl Acad. Sci. USA 109, 12632-12637 (2012).
21. Murat, S., Hopfen, C. & McGregor, A. P. The function and evolution of Wnt genes in arthropods. Arthropod. Struct. Dev. 39, 446-452 (2010).
22. Gross, J. C. & Boutros, M. Secretion and extracellular space travel of Wnt proteins. Curr. Opin. Genet. Dev. 22, 385-390 (2013).
23. Werner, T., Koshikawa, S., Williams, T. M. & Carroll, S. B. Generation of a novel wing colour pattern by the Wingless morphogen. Nature 464, 1143-U1157 (2010).
24. Yamaguchi, J. et al. Periodic Wnt1 expression in response to ecdysteroid generates twin-spot markings on caterpillars. Nat. Commun. 4, 1857 (2013).
25. Heikkila, M., Kaila, L., Mutanen, M., Pena, C. & Wahlberg, N. Cretaceous origin and repeated tertiary diversification of the redefined butterflies. Proc. R. Soc. B 279, 1093-1099 (2012).
26. Yan, D. & Lin, X. Shaping morphogen gradients by proteoglycans. Cold Spring Harb. Perspect. Biol. 1, a002493 (2009).
27. Binari, R. et al. Genetic evidence that heparin-like glycosaminoglycans are involved in wingless signaling. Development 724, 2623-2632 (1997).
28. Greco, V., Hannus, M. & Eaton, S. Argosomes: a potential vehicle for the spread of morphogens through epithelia. Cell 106, 633-645 (2001).
29. Serfas, M. & Carroll, S. Pharmacologic approaches to butterfly wing patterning: sulfated polysaccharides mimic or antagonize cold shock and alter the interpretation of gradients of positional information. Dev. Biol. 287, 416-424 (2005).
30. Anders, S., Reyes, A. & Huber, W. Detecting differential usage of exons from RNA-seq data. Genome Res. 22, 2008-2017 (2012).
31. Dooner, H. K. & He, L. Maize genome structure variation: interplay between retrotransposon polymorphisms and genic recombination. Plant Cell 20, 249-258 (2008).
32. Huges, T. Regulation of gene expression by alternative untranslated regions. Trends Genet. 22, 119-122 (2006).
33. Consortium, H. G. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487, 94-98 (2012).
34. Chamberlain, N. L., Hill, R. I., Kapan, D. D., Gilbert, L. E. & Kronforst, M. R. Polymorphic butterfly reveals the missing link in ecological speciation. Science 326, 847-850 (2009).
35. Losos, J. Convergence, adaptation, and constraint. Evolution 65, 1827-1840 (2011).
36. Gompel, N. & Prud'homme, B. The causes of repeated genetic evolution. Dev. Biol. 332, 36-47 (2009).
37. Stern, D. L. & Orgogozo, V. Is genetic evolution predictable? Science 323, 746-751 (2009).
38. Martin, A. & Orgogozo, V. The loci of repeated evolution: a catalog of genetic hotspots of phenotypic variation. Evolution 67, 1235-1250 (2013).
39. Stern, D. The genetic causes of convergent evolution. Nat. Rev. Genet. 14, 751-764 (2013).
40. Janssen, R. et al. Conservation, loss, and redeployment of Wnt ligands in protostomes: implications for understanding the evolution of segment formation. BMC Evol. Biol. 10, 374 (2010).
41. Platt, A. P. A simple technique for hand-pairing Limenitis butterflies (Nymphalidae). J. Lepid. Soc. 23, 109-112 (1969).
42. Robinson, R. Lepidoptera Genetics (Pergamon, 1971).
43. Platt, A. P. & Brower, L. P. Mimetic versus disruptive coloration in intergrating populations of Limenitis arthemis and asytanax butterflies. Evolution 22, 699-718 (1968).
44. Vos, P. et al. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23, 4407-4414 (1995).
45. VanOojen, J. W. & Voorrips, R. E. JoinMap version 3.0: software for the calculation of genetic linkage maps. Plant Research International (2001).
46. Maeki, K. & Remington, C. L. Studies of the chromosomes of the North American Rhopalocera. 4. Nymphalinae, Charaxidinae, Libytheinae. J. Lepid. Soc. 14, 179-201 (1968).
47. Hanrahan, S. J. & Johnston, J. S. New genome size estimates of 134 species of arthropods. Chromosome Res. 19, 809-823 (2011).
48. Beldade, P., Saneko, S. V., Pul, N. & Long, A. D. A gene-based linkage map for Bicyclus anynana butterflies allows for a comprehensive analysis of synteny with the lepidopteran reference genome. PLoS Genet. 5, e10000366 (2009).
49. Pringle, E. G. et al. Synteny and chromosome evolution in the Lepidoptera: evidence from mapping in Heliconius melpomene. Genetics 177, 417-426 (2007).
50. Joron, M. et al. A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biol. 4, 1831-1840 (2006).
51. Trapnell, C. et al. Differential gene and transcript expression analysis of RNAseq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578 (2012).
52. Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066 (2002).
53. DePristo, M. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491-498 (2011).
54. McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010).
55. Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156-2158 (2011).
56. Rogers, A. R. & Huff, C. Linkage disequilibrium between loci with unknown phase. Genetics 182, 839-844 (2009).
57. Foll, M. & Gaggiotti, O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180, 977-993 (2008).
58. Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945-959 (2000).
59. Opler, P. A., Lotts, K. & Naberhaus, T. Butterflies and Moths of North America ohttp://www.butterfliesandmoths.org/.4 (2012).
60. Ries, L. & Mullen, S. P. A rare model limits the distribution of its more common mimic: A twist on frequency-dependent batesian mimicry. Evolution 62, 1798-1803 (2008).
61. Martin, A. & Reed, R. Wingless and aristaless2 define a developmental ground plan for moth and butterfly wing pattern evolution. Mol. Biol. Evol. 27, 2864-2878 (2010).