Multilocus analyses of admixture and introgression among hybridizing Heliconius butterflies

Evolution

Volumn 60, Issue 6, 2006, Pages 1254-1268

  Kronforst, Marcus R ^a,b   Young, Laura G ^a   Blume, Lauren M ^a   Gilbert, Lawrence E ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b RICE UNIVERSITY   (United States)

Author keywords

Admixture; Gene flow; Heliconius; Hybridization; Introgression; Isolation with migration; Lepidoptera

Indexed keywords

BUTTERFLY; DNA; GENE FLOW; GENETIC VARIATION; GENOTYPE; HYBRIDIZATION; INTROGRESSION; MIMICRY; NATURAL SELECTION;

HELICONIUS; HELICONIUS CYDNO; HELICONIUS ERATO; HELICONIUS HIMERA; HELICONIUS MELPOMENE; HELICONIUS PACHINUS; LEPIDOPTERA; PAPILIONOIDEA;

DNA;

ANIMAL; ARTICLE; BUTTERFLY; CHEMISTRY; COSTA RICA; DEMOGRAPHY; EVOLUTION; FEMALE; GENE FLOW; GENETICS; HAPLOTYPE; HYBRIDIZATION; MALE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

ANIMALS; BASE SEQUENCE; BUTTERFLIES; COSTA RICA; DEMOGRAPHY; DNA; EVOLUTION; FEMALE; GENE FLOW; HAPLOTYPES; HYBRIDIZATION, GENETIC; MALE;

EID: 33748571508     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1554/06-005.1     Document Type: Article

References (71)

1. Barton, N. H. 2001. The role of hybridization in evolution. Mol. Ecol. 10:551-568.
2. Barton, N. H., and G. M. Hewitt. 1985. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16:113-148.
3. Beltrán, M., C. D. Jiggins, V. Bull, M. Linares, J. Mallet, W. O. McMillan, and E. Bermingham. 2002. Phylogenetic discordance at the species boundary: comparative gene genealogies among Heliconius butterflies. Mol. Biol. Evol. 19:2176-2190.
4. Benson, W. W. 1972. Natural selection for Müllerian mimicry in Heliconius erato in Costa Rica. Science 176:936-939.
5. Brower, A. V. Z. 1994a. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc. Natl. Acad. Sci. USA 91:6491-6495.
6. _. 1994b. Phylogeny of Heliconius butterflies inferred from mitochondrial DNA sequences (Lepidoptera: Nymphalidae). Mol. Phylogenet. Evol. 3:159-174.
7. _. 1996. Parallel race formation and the evolution of mimicry in Heliconius butterflies: a phylogenetic hypothesis from mitochondrial DNA sequences. Evolution 50:195-221.
8. Brower, A. V. Z., and R. DeSalle. 1998. Patterns of mitochondrial versus nuclear DNA sequence divergence among nymphalid butterflies: the utility of wingless as a source of characters for phylogenetic inference. Insect Mol. Biol. 7:73-82.
9. Brower, A. V. Z., and M. G. Egan. 1997. Cladistic analysis of Heliconius butterflies and relatives (Nymphalidae: Heliconiiti): a revised phylogenetic position for Eueides based on sequences from mtDNA and a nuclear gene. Proc. R. Soc. Lond. B 264:969-977.
10. Brown, Jr., K. S., P. M. Sheppard, and J. R. G. Turner. 1974. Quaternary refugia in South America: evidence from race formation in Heliconius butterflies. Proc. R. Soc. Lond. B 187:369-378.
11. Brunetti, C. R., J. E. Selegue, A. Monteiro, V. French, P. M. Brakefield, and S. B. Carroll. 2001. The generation and diversification of butterfly eyespot color patterns. Curr. Biol. 11:1578-1585.
12. Burke, J. M., and M. L. Arnold. 2001. Genetics and the fitness of hybrids. Annu. Rev. Genetics 35:31-52.
13. Bush, G. L. 1994. Sympatric speciation in animals: new wine in old bottles. Trends Ecol. Evol. 9:285-288.
14. Butlin, R. 1987. Speciation by reinforcement. Trends Ecol. Evol. 2:8-12.
15. Carroll, S. B., J. Gates, D. N. Keyes, S. W. Paddock, G. E. F. Panganiban, J. E. Seleque, and J. A. Williams. 1994. Pattern formation and eyespot determination in butterfly wings. Science 265:109-114.
16. Cho, S., A. Mitchell, J. C. Regier, C. Mitter, R. W. Poole, T. P. Friedlander, and S. Zhao. 1995. A highly conserved nuclear gene for low-level phylogenetics: elongation factor-1α recovers morphology-based tree for heliothine moths. Mol. Biol. Evol. 12:650-656.
17. Davison, A., W. O. McMillan, A. S. Griffin, C. D. Jiggins, and J. L. B. Mallet. 1999. Behavioural and physiological adaptation between two parapatric Heliconius species (Lepidoptera: Nymphalidae). Biotropica 31:661-668.
18. Emelianov, I., F. Marec, and J. Mallet. 2004. Genomic evidence for divergence with gene flow in host races of the larch budmoth. Proc. R. Soc. Lond. B 271:97-105.
19. Estrada, C., and C. D. Jiggins. 2002. Patterns of pollen feeding and habitat preference among Heliconius species. Ecol. Entomol. 27:448-456.
20. Falush, D., M. Stephens, and J. K. Pritchard. 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567-1587.
21. Feder, J. L., S. B. Opp, B. Wlazlo, K. Reynolds, W. Go, and S. Spisak. 1994. Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly. Proc. Natl. Acad. Sci. USA 91:7990-7994.
22. Flanagan, N. S., A. Tobler, A. Davison, O. G. Pybus, D. D. Kapan, S. Planas, M. Linares, D. Heckle, and W. O. McMillan. 2004. Historical demography of Müllerian mimicry in the neotropical Heliconius butterflies. Proc. Natl. Acad. Sci. USA 101:9704-9709.
23. Gilbert, L. E. 2003. Adaptive novelty through introgression in Heliconius wing patterns: evidence for shared genetic "tool box" from synthetic hybrid zones and a theory of diversification. Pp. 281-318 in C. L. Boggs, W. B. Watt, and P. R. Ehrlich, eds. Ecology and evolution taking flight: butterflies as model systems. Univ. of Chicago Press, Chicago, IL.
24. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41:95-98.
25. Hey, J., and R. Nielsen. 2004. Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747-760.
26. Higgins, D. G., and P. M. Sharp. 1988. CLUSTAL: a package for performing multiple sequence alignments on a microcomputer. Gene 73:237-244.
27. Hudson, R. R. 1985. The sampling distribution of linkage disequilibrium under an infinite allele model without selection. Genetics 109:611-631.
28. Hudson, R. R., and N. L. Kaplan. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147-164.
29. Huelsenbeck, J. P., and F. Ronquist. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755.
30. Jiggins, C. D., and W. O. McMillan. 1997. The genetic basis of an adaptive radiation: warning colour in two Heliconius species. Proc. R. Soc. Lond. B 246:1167-1175.
31. Jiggins, C. D., W. O. McMillan, W. Neukirchen, and J. Mallet. 1996. What can hybrid zones tell us about speciation? The case of Heliconius erato and H. himera (Lepidoptera: Nymphalidae). Biol. J. Linn. Soc. 59:221-242.
32. Jiggins, C. D., W. O. McMillan, P. King, and J. Mallet. 1997. The maintenance of species differences across a Heliconius hybrid zone. Heredity 79:495-505.
33. Jiggins, C. D., R. E. Naisbit, R. L. Coe, and J. Mallet. 2001. Reproductive isolation caused by colour pattern mimicry. Nature 411:302-305.
34. Jiggins, C. D., C. Estrada, and A. Rodrigues. 2004. Mimicry and the evolution of premating isolation in Heliconius melpomene Linnaeus. J. Evol. Biol. 17:680-691.
35. Kapan, D. D. 2001. Three-butterfly system provides a field test of Müllerian mimicry. Nature 409:338-340.
36. Keys, D. N., D. L. Lewis, J. E. Selegue, B. J. Pearson, L. V. Goodrich, R. L. Johnson, J. Gates, M. P. Scott, and S. B. Carroll. 1999. Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283:532-534.
37. Kobayashi, N., K. Tamura, and T. Aotsuka. 1999. PCR error and molecular population genetics. Biochem. Genet. 37:317-321.
38. Kronforst, M. R. 2004. The role of hybridization in the evolution of Heliconius butterflies: species diversification, the evolution of reproductive isolation, and interspecific gene flow. Ph.D. diss., University of Texas, Austin, TX.
39. _. 2005. Primers for the amplification of nuclear introns in Heliconius butterflies. Mol. Ecol. Notes 5:158-162.
40. Kronforst, M. R., and T. H. Fleming. 2001. Lack of genetic differentiation among widely spaced subpopulations of a butterfly with home range behaviour. Heredity 86:243-250.
41. Kronforst, M. R., L. G. Young, D. D. Kapan, C. McNeely, R. J. O'Neill, and L. E. Gilbert. 2006. Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proc. Natl. Acad. Sci. USA 103:6575-6580.
42. Kumar, S., K. Tamura, I. B. Jakobsen, and M. Nei. 2001. MEGA2: molecular evolutionary genetics analysis software. School of Life Sciences, Arizona State University, Tempe, AZ.
43. Mallet, J. 1993. Speciation, raciation, and color pattern evolution in Heliconius butterflies: evidence from hybrid zones. Pp. 226-260 in R. G. Harrison, ed. Hybrid zones and the evolutionary process. Oxford Univ. Press, New York.
44. _. 2005. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20:229-237.
45. Mallet, J., and N. H. Barton. 1989. Strong natural selection in a warning color hybrid zone. Evolution 43:421-431.
46. Mallet, J., W. O. McMillan, and C. D. Jiggins. 1998. Mimicry and warning color at the boundary between races and species. Pp. 390-403 in D. J. Howard and S. H. Berlocher, eds. Endless forms: species and speciation. Oxford Univ. Press, New York.
47. Mallet, J., W. Neukirchen, and M. Linares. 2003. Wild-caught hybrids among Heliconius and Eueides species: a database. Available at: http://www.ucl.ac.uk/taxome/hyb/hybtab.html.
48. McMillan, W. O., C. D. Jiggins, and J. Mallet. 1997. What initiates speciation in passion-vine butterflies? Proc. Natl. Acad. Sci. USA 94:8628-8633.
49. Mueller, U. G., and L. L. Wolfenbarger. 1999. AFLP genotyping and fingerprinting. Trends Ecol. Evol. 14:389-394.
50. Naisbit, R. E., C. D. Jiggins, and J. Mallet. 2001. Disruptive sexual selection against hybrids contributes to speciation between Heliconius cydno and Heliconius melpomene. Proc. R. Soc. Lond. B 268:1-6.
51. Naisbit, R., C. D. Jiggins, M. Linares, C. Salazar, and J. Mallet. 2002. Hybrid sterility, Haldane's rule and speciation in Heliconius cydno and H. melpomene. Genetics 161:1517-1526.
52. Naisbit, R., C. D. Jiggins, and J. Mallet. 2003. Mimicry: developmental genes that contribute to speciation. Evol. Develop. 5:269-280.
53. Nei, M. 1987. Molecular evolutionary genetics. Columbia Univ. Press, New York.
54. Nielsen, R., and J. Wakeley. 2001. Distinguishing migration from isolation. A Markov chain Monte Carlo approach. Genetics 158:885-896.
55. Nijhout, H. F., G. A. Wray, and L. E. Gilbert. 1990. An analysis of the phenotypic effects of certain colour pattern genes in Heliconius. Biol. J. Linn. Soc. 40:357-372.
56. Ortíz-Barrientos, D., J. Reiland, J. Hey, and M. A. F. Noor. 2002. Recombination and the divergence of hybridizing species. Genetica 116:167-178.
57. Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
58. Reed, R. D., and L. E. Gilbert. 2004. Wing venation and distal-less expression in Heliconius butterfly wing pattern development. Dev. Genes Evol. 214:628-634.
59. Reed, R. D. and L. M. Nagy. 2005. Evolutionary redeployment of a biosynthetic module: expression of eye pigment genes vermilion, cinnabar, and white in butterfly wing development. Evol. Dev. 7:301-311.
60. Reed, R. D., and M. S. Serfas. 2004. Butterfly wing pattern evolution is associated with changes in a notch/distal-less temporal pattern formation process. Curr. Biol. 14:1159-1166.
61. Rozas, J., and R. Rozas. 1999. DnaSP version 3: An integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174-175.
62. Schluter, D. 1998. Ecological causes of speciation. Pp. 114-129 in D. J. Howard and S. H. Berlocher, eds. Endless forms: species and speciation. Oxford Univ. Press, New York.
63. Seehausen, O. 2004. Hybridization and adaptive radiation. Trends Ecol. Evol. 19:198-207.
64. Servedio, M. R., and M. A. F. Noor. 2003. The role of reinforcement in speciation: theory and data. Annu. Rev. Ecol. Evol. Syst. 34:339-364.
65. Sheppard, P. M., J. R. G. Turner, K. S. Brown, W. W. Benson, and M. C. Singer. 1985. Genetics and evolution of Müllerian mimicry in Heliconius butterflies. Philos. Trans. R. Soc. Lond. B 308:433-613.
66. Simon, C., F. Frati, A. Beckenbach, B. Crespi, H. Liu, and P. Flook. 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann. Entomol. Soc. Am. 87:651-702.
67. Smiley, J. 1978. Plant chemistry and the evolution of host specificity: new evidence for Heliconius and Passiflora. Science 201:745-747.
68. Turner, J. R. G., and J. L. B. Mallet. 1996. Did forest islands drive the diversity of warningly coloured butterflies? Biotic drift and the shifting balance. Philos. Trans. Roy. Soc. London B 351:835-845.
69. Turner, T. L., M. W. Hahn, and S. V. Nuzhdin. 2005. Genomic islands of speciation in Anopheles gambiae. PLoS Biol. 3:e285.
70. Vos, P., R. Hogers, M. Bleeker, M. Reijans, T. Van De Lee, M. Hornes, A. Frijters, J. Pot, J. Peleman, M. Kuiper, and M. Zabeau. 1995. AFLP: a new technique for DNA fingerprinting. Nucleic. Acids Res. 23:4407-4414.
71. Won, Y. J., and J. Hey. 2005. Divergence population genetics of chimpanzees. Mol. Biol. Evol. 22:297-307.