Stable Heliconius butterfly hybrid zones are correlated with a local rainfall peak at the edge of the Amazon basin

Evolution

Volumn 68, Issue 12, 2014, Pages 3470-3484

  Rosser, Neil ^a,b   Dasmahapatra, Kanchon K ^b   Mallet, James ^a,c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

^c HARVARD UNIVERSITY   (United States)

Author keywords

Frequency dependent selection; Heliconius butterflies; Mimicry; Moving hybrid zones; Pleistocene refugia

Indexed keywords

HELICONIUS; PAPILIONOIDEA;

RAIN;

ANIMAL; BUTTERFLY; GENE LINKAGE DISEQUILIBRIUM; GENETIC SELECTION; GENETICS; HYBRIDIZATION; SEASON; SPECIES DIFFERENTIATION;

ANIMALS; BUTTERFLIES; GENETIC SPECIATION; HYBRIDIZATION, GENETIC; LINKAGE DISEQUILIBRIUM; RAIN; SEASONS; SELECTION, GENETIC;

EID: 84914164284     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12539     Document Type: Article

References (75)

1. Arias, C. F., A. G. Muñoz, C. D. Jiggins, J. Mavárez, E. Bermingham, and M. Linares . 2008. A hybrid zone provides evidence for incipient ecological speciation in Heliconius butterflies. Mol. Ecol. 17:4699-4712.
2. Arntzen, J. W., and G. P. Wallis . 1991. Restricted gene flow in a moving hybrid zone of the newts Triturus cristatus and T. marmoratus in western France. Evolution 45:805-826.
3. Barton, N. H. 1979. The dynamics of hybrid zones. Heredity 43:341-359.
4. Barton, N. H. 1982. The structure of the hybrid zone in Uroderma bilobatum (Chiroptera: Phyllostomatidae). Evolution 36:863-866.
5. Barton, N. H., and K. S. Gale . 1993. Genetic analysis of hybrid zones. Pp. 226-260 in R. G. Harrison, ed. Hybrid zones and the evolutionary process. Oxford Univ. Press, New York.
6. Barton, N. H., and G. M. Hewitt . 1985. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16:113-148.
7. Barton, N. H., and G. M. Hewitt . 1989. Adaptation, speciation and hybrid zones. Nature 341:497-503.
8. Barton, N. H., and M. Turelli . 2011. Spatial waves of advance with bistable dynamics: cytoplasmic and genetic analogues of Allee effects. Am. Nat. 178:E48-E75.
9. Baxter, S. W., N. J. Nadeau, L. S. Maroja, P. Wilkinson, B. A. Counterman, A. Dawson, M. Beltran, S. Perez-Espona, N. Chamberlain, L. Ferguson, et al. 2010. Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene Clade. PLoS Genet. 6:e1000794.
10. Bazykin, A. D. 1969. Hypothetical mechanism of speciation. Evolution 23:685-687.
11. Beven, S., E. F. Connor, and K. Beven . 1984. Avian biogeography in the Amazon basin and the biological model of diversification. J. Biogeogr. 11:383-399.
12. Blum, M. J. 2002. Rapid movement of a Heliconius hybrid zone: evidence for phase III of Wright's shifting balance theory? Evolution 56:1992-1998.
13. Blum M.J. 2008. Ecological and genetic associations across a Heliconius hybrid zone. J. Evolution. Biol. 21:330-341.
14. Britch, S. C., M. L. Cain, and D. J. Howard . 2001. Spatio-temporal dynamics of the Allonemobius fasciatus-A. socius mosaic hybrid zone: a 14-year perspective. Mol. Ecol. 10:627-638.
15. Bronson, C. L., T. C. Grubb, G. D. Sattler, and M. J. Braun . 2003. Mate preference: a possible causal mechanism for a moving hybrid zone. Anim. Behav. 65:489-500.
16. Brown, K. S. 1979. Ecologia Geográfica e Evolução nas Florestas Neotropicais. Universidade Estadual de Campinas, Campinas, Brazil.
17. Brown, K. S. 1981. The biology of Heliconius and related genera. Annu. Rev. Entomol. 26:427-456.
18. Buggs, R. J. A. 2007. Empirical study of hybrid zone movement. Heredity 99:301-312.
19. Bush, M. B. 1994. Amazonian speciation: a necessarily complex model. J. Biogeogr. 21:5-17.
20. Carling, M. D., and B. Zuckerberg . 2011. Spatio-temporal changes in the genetic structure of the Passerina bunting hybrid zone. Mol. Ecol. 20:1166-1175.
21. Chai, P. 1986. Field observations and feeding experiments on the responses of rufous-tailed jacamars (Galbula ruficauda) to free-flying butterflies in a tropical rainforest. Biol. J. Linn. Soc. 29:161-189.
22. Chai, P. 1996. Butterfly visual characteristics and ontogeny of responses to butterflies by a specialized tropical bird. Biol. J. Linn. Soc. 59:37-67.
23. Counterman, B. A., F. Araujo-Perez, H. M. Hines, S. W. Baxter, C. M. Morrison, D. P. Lindstrom, R. Papa, L. Ferguson, M. Joron, R. H. ffrench-Constant, et al. 2010. Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in Heliconius erato. PLoS Genet. 6:e1000796.
24. Dasmahapatra, K. K., M. J. Blum, A. Aiello, S. Hackwell, N. Davies, E. Bermingham, and J. Mallet . 2002. Inferences from a rapidly moving hybrid zone. Evolution 56:741-753.
25. Dasmahapatra, K. K., G. Lamas, F. Simpson, and J. Mallet . 2010. The anatomy of a "suture zone" in Amazonian butterflies: a coalescent-based test for vicariant geographic divergence and speciation. Mol. Ecol. 19:4283-4301.
26. Endler, J. A. 1977. Geographic variation, speciation, and clines. Princeton Univ. Press, Princeton, NJ.
27. Feder, J. L., S. P. Egan, and P. Nosil . 2012. The genomics of speciation-with-gene-flow. Trends Genet. 28:342-350.
28. Haas, F., and A. Brodin . 2005. The crow Corvus corone hybrid zone in southern Denmark and northern Germany. Ibis 147:649-656.
29. Haffer, J. 1969. Speciation in Amazonian forest birds. Science 165:131-137.
30. Haffer J. 2008. Hypotheses to explain the origin of species in Amazonia. Braz. J. Biol. 68:917-947.
31. Heliconius Genome Consortium. 2012. Genomic evidence for promiscuous exchange of adaptations among Heliconius butterfly species. Nature 487:94-98.
32. Hewitt, G. M. 1988. Hybrid zones-natural laboratories for evolutionary studies. Trends Ecol. Evol. 3:158-167.
33. Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones, and A. Jarvis . 2005. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25:1965-1978.
34. Hill, W. G. 1974. Estimation of linkage disequilibrium in randomly mating populations. Heredity 33:229-239.
35. Hines, H. M., B. A. Counterman, R. Papa, P. Albuquerque de Moura, M. Z. Cardoso, M. Linares, J. Mallet, R. D. Reed, C. D. Jiggins, M. R. Kronforst, et al. 2011. Wing patterning gene redefines the mimetic history of Heliconius butterflies. Proc. Natl. Acad. Sci. USA 108:19666-19671.
36. Jiggins, C. D., 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.
37. Joron, M., I. R. Wynne, G. Lamas, and J. Mallet . 2001. Variable selection and the coexistence of multiple mimetic forms of the butterfly Heliconius numata. Evol. Ecol. 13:721-754.
38. Joron, M., R. Papa, M. Beltrán, N. Chamberlain, J. Mavárez, S. Baxter, M. Abanto, E. Bermingham, S. J. Humphray, J. Rogers, et al. 2006. A conserved supergene locus controls colour pattern diversity in Heliconius Butterflies. PLoS Biol. 4:e303.
39. Joron, M., L. Frezal, R. T. Jones, N. L. Chamberlain, S. F. Lee, C. R. Haag, A. Whibley, M. Becuwe, S. W. Baxter, L. Ferguson, et al. 2011. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477:203-206.
40. Kawaguchi, I., and A. Sasaki . 2006. The wave speed of intergradation zone in two-species lattice Müllerian mimicry model. J. Theor. Biol. 243:594-603.
41. Key, K. H. L. 1968. The concept of stasipatric speciation. Syst. Zool. 17:14-22.
42. Krosby, M., and S. Rohwer . 2010. Ongoing movement of the hermit warbler x townsend's warbler hybrid zone. PLoS ONE 5:e14164.
43. Lamas, G. 2004. Atlas of Neotropical Lepidoptera. Checklist: Part 4A. Hesperioidea-Papilionoidea. Association for Tropical Lepidoptera/Scientific Publishers, Gainesville, FL.
44. Langham, G. M. 2004. Specialized avian predators repeatedly attack novel color morphs of Heliconius butterflies. Evolution 58:2783-2787.
45. Mallet, J. 1986. Hybrid zones of Heliconius butterflies in Panama and the stability and movement of warning colour clines. Heredity 56:191-202.
46. Mallet J. 1989. The genetics of warning colour in Peruvian hybrid zones of Heliconius erato and H. melpomene. Proc. R. Soc. B 236:163-185.
47. Mallet, J. 1993. Speciation, raciation, and colour pattern evolution in Heliconius butterflies: the evidence from hybrid zones. Pp. 226-260 in R. G. Harrison, ed. Hybrid zones and the evolutionary process. Oxford Univ. Press, New York.
48. Mallet, J. 2010. Shift happens! Shifting balance and the evolution of diversity in warning colour and mimicry. Ecol. Entomol. 35:90-104.
49. Mallet, J., and N. Barton . 1989a, b. Inference from clines stabilized by frequency-dependent selection. Genetics 122:967-976.
50. Mallet, J., and N. H. Barton . 1989b. Strong natural selection in a warning-color hybrid zone. Evolution 43:421-431.
51. Mallet, J., N. H. Barton, G. Lamas, J. Santisteban, M. Muedas, and H. Eeley . 1990. Estimates of selection and gene flow from measures of cline width and linkage disequilibrium in Heliconius hybrid zones. Genetics 124:921-936.
52. Mallet, J., 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.
53. Mallet, J., and J. R. G. Turner . 1998. Biotic drift or the shifting balance: did forest islands drive the diversity of warningly coloured butterflies? Pp. 262-280 in P. R. Grant, ed. Evolution on Islands. Oxford Univ. Press, Oxford, U.K.
54. Martin, S. H., K. K. Dasmahapatra, N. J. Nadeau, C. Salazar, J. R. Walters, F. Simpson, M. Blaxter, A. Manica, J. Mallet, and C. D. Jiggins . 2013. Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Res. 23:1817-1828.
55. Mayr, E. 1963. Animal species and evolution. Harvard Univ. Press, Cambridge, MA.
56. Mérot, C, J. Mavárez, A. Evin, K. K. Dasmahapatra, J. Mallet, G. Lamas, and M. Joron . 2013. Genetic differentiation without mimicry shift in a pair of hybridizing Heliconius species (Lepidoptera: Nymphalidae). Biol. J. Linn. Soc. 109:830-847.
57. Merrill, R. M., R. W. R. Wallbank, V. Bull, P. C. A. Salazar, J. Mallet, M. Stevens, and C. D. Jiggins . 2012. Disruptive ecological selection on a mating cue. Proc. R. Soc. B 279:4907-4913.
58. Mettler, R. D., and G. M. Spellman . 2009. A hybrid zone revisited: molecular and morphological analysis of the maintenance, movement, and evolution of a Great Plains avian (Cardinalidae: Pheucticus) hybrid zone. Mol. Ecol. 18:3256-3267.
59. Moore, W. S., and D. B. Buchanan . 1985. Stability of the northern flicker hybrid zone in historical times: implications for adaptive speciation theory. Evolution 39:135-151.
60. Moritz, C., J. L. Patton, C. J. Schneider, and T. B. Smith . 2000. Diversification of rainforest faunas: an integrated molecular approach. Annu. Rev. Ecol. Syst. 31:533-563.
61. Nadeau, N. J., A. Whibley, R. T. Jones, J. W. Davey, K. K. Dasmahapatra, S. W. Baxter, M. A. Quail, M. Joron, R. H. ffrench-Constant, M. L. Blaxter, et al. 2012. Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing. Phil. Trans. R. Soc. B 367:343-353.
62. Nelson, B. W., C. A. C. Ferreira, M. F. da Silva, and M. L. Kawasaki . 1990. Endemism centres, refugia and botanical collection density in Brazilian Amazonia. Nature 345:714-716.
63. Pinheiro, C. E. G. 1997. Unpalatability, mimicry and escaping ability in neotropical butterflies: experiments with wild predators. Doctoral dissertation, University of Oxford, U.K.
64. R Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
65. Reed, R. D., R. Papa, A. Martin, H. M. Hines, B. A. Counterman, C. Pardo-Diaz, C. D. Jiggins, N. L. Chamberlain, M. R. Kronforst, R. Chen, et al. 2011. optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333:1137-1141.
66. Rising, J. D. 1996. The stability of the oriole hybrid zone in western Kansas. Condor 98:658-663.
67. Rosser, N., A. B. Phillimore, B. Huertas, K. R. Willmott, and J. Mallet . 2012. Testing historical explanations for gradients in species richness in heliconiine butterflies of tropical America. Biol. J. Linn. Soc. 105:479-497.
68. Sasaki, A., I. Kawaguchi, and A. Yoshimori . 2002. Spatial mosaic and interfacial dynamics in a Müllerian mimicry system. Theor. Popul. Biol. 61:49-71.
69. Secondi, J., V. Bretagnolle, C. Compagnon, and B. Faivre . 2003. Species-specific song convergence in a moving hybrid zone between two passerines. Biol. J. Linn. Soc. 80:507-517.
70. Sheppard, P. M., J. R. G. Turner, K. S. Brown, W. W. Benson, and M. C. Singer . 1985. Genetics and the evolution of Müllerian mimicry in Heliconius butterflies. Phil. Trans. R. Soc. B 308:433-610.
71. Supple, M. A., H. M. Hines, K. K. Dasmahapatra, J. J. Lewis, D. M. Nielsen, C. Lavoie, D. A. Ray, C. Salazar, W. O. McMillan, and B. A. Counterman . 2013. Genomic architecture of adaptive color pattern divergence and convergence in Heliconius butterflies. Genome Res. 23:1248-1257.
72. Szymura, J. M., and N. H. Barton . 1991. The genetic structure of the hybrid zone between the fire-bellied toads Bombina bombina and B. variegata: comparisons between transects and between loci. Evolution 45:237-261.
73. Taylor, S. A., T. A. White, W. M. Hochachka, V. Ferretti, R. L. Curry, and I. Lovette . 2014. Climate-mediated movement of an avian hybrid zone. Curr. Biol. 24:671-676.
74. Whinnett, A., M. Zimmermann, K. R. Willmott, N. Herrera, R. Mallarino, F. Simpson, M. Joron, G. Lamas, and J. Mallet . 2005. Strikingly variable divergence times inferred across an Amazonian butterfly "suture zone." Proc. R. Soc. B 272:2525-2533.
75. Wilf, P., N. R. Cúneo, K. R. Johnson, J. F. Hicks, S. L. Wing, and J. D. Obradovich . 2003. High plant diversity in Eocene South America: evidence from Patagonia. Science 300:122-125.