Hybrid incompatibility is consistent with a hybrid origin of Heliconius heurippa Hewitson from its close relatives, Heliconius cydno Doubleday and Heliconius melpomene Linnaeus

Journal of Evolutionary Biology

Volumn 18, Issue 2, 2005, Pages 247-256

  Salazar, C A ^a   Jiggins, C D ^b,c   Arias, C F ^a   Tobler, A ^d   Bermingham, E ^b   Linares, M ^a  

^a UNIVERSIDAD DE LOS ANDES   (Colombia)

^b SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d DUKE UNIVERSITY   (United States)

Author keywords

Dominance Theory; Haldane's rule; Heliconius; Hybrid speciation; Lepidoptera

Indexed keywords

PRIMER DNA;

HYBRID; INCOMPATIBILITY; PHYLOGENETICS; SPECIATION (BIOLOGY);

AGAR GEL ELECTROPHORESIS; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BUTTERFLY; COLOMBIA; COMPARATIVE STUDY; FEMALE; FORELIMB; GENETIC MARKER; GENETICS; GENOME; GEOGRAPHY; HYBRIDIZATION; MALE; PHYSIOLOGY; PIGMENTATION; POLYMERASE CHAIN REACTION; POPULATION GENETICS; REPRODUCTION; SPECIES DIFFERENCE;

ANIMALS; BUTTERFLIES; COLOMBIA; DNA PRIMERS; ELECTROPHORESIS, AGAR GEL; FEMALE; GENETIC MARKERS; GENETICS, POPULATION; GENOME; GEOGRAPHY; HYBRIDIZATION, GENETIC; MALE; MODELS, GENETIC; PIGMENTATION; POLYMERASE CHAIN REACTION; REPRODUCTION; SPECIES SPECIFICITY; WING;

HELICONIUS; HELICONIUS CYDNO; HELICONIUS HEURIPPA; HELICONIUS MELPOMENE; LEPIDOPTERA;

EID: 14844353469     PISSN: 1010061X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2004.00839.x     Document Type: Article

References (50)

1. Arnold, M.L. 1997. Natural Hybridization and Evolution. Oxford series in Ecology and Evolution. Oxford University Press, New York.
2. Barbash, D.A., Siino, D.F., Tarone, A.M. & Roote, J.A. 2003. A rapidly evolving Myb-related protein causes species isolation in Drosophila. Proc. Natl Acad Sci. USA. 100: 5302-5307.
3. Barbash, D.A., Awadalla, P. & Tarone, A.M. 2004. Functional divergence caused by ancient positive selection of a drosophila hybrid incompatibility locus. PLoS Biol. 2: 0839-0848.
4. Beltrán, M., Jiggins, C.D., Bull, V., McMillan, W.O., Bermingham, E. & Mallet, J. 2002. Phylogenetic discordance at the species boundary: gene genealogies in Heliconius butterflies. Mol. Biol. Evol. 19: 2176-2190.
5. Brower, A.V.Z. 1994. Phylogeny of Heliconius butterflies inferred from mitochondrial DNA sequences (Lepidoptera: Nymphalidae). Mol. Phylogenet. Evol. 3: 159-174.
6. Bullini, L. 1994. Origin and evolution of animal hybrid species. Trends Ecol. Evol. 9: 422-426.
7. Coyne, J.A. & Orr, H.A. 1989. Patterns of speciation in Drosophila. Evolution 43: 362-381.
8. Coyne, J.A. & Orr, H.A. 1997. Patterns of speciation in Drosophila revisited. Evolution 51: 295-303.
9. Dowling, T.E. & Secor, C.L. 1997. The role of hybridization and introgression in the diversification of animals. Annu. Rev. Ecol. Sys. 28: 593-619.
10. Emsley, M.G. 1965. Speciation in Heliconius (Lep., Nymphalidae): morphology and geographic distribution. Zoologica, New York 50: 191-254.
11. 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. In: Ecology and Evolution Taking Flight: Butterflies as Model Systems (C. L. Boggs, W. B. Watt & P. R. Ehrlich, eds), Univ. of Chicago Press, Chicago.
12. Hudson, R. & Coyne, J. 2002. Mathematical consequences of the genealogical species concept. Evolution 56: 1557-1565.
13. Hutter, P. 2002. X-linked small GTPase and OXPHOS genes are candidates for the genetic basis of hybrid inviability in Drosophila. Dev. Genes Evol. 212: 504-512.
14. Jiggins, C.D., McMillan, W.O., Neukirchen, W. & Mallet, J. 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.
15. Jiggins, C.D., Linares, M., Nasbit, R.E., Salazar, C., Yang, Z.H. & Mallet, J. 2001a. Sex-linked hybrid sterility in a butterfly. Evolution 55: 1631-1638.
16. Jiggins, C.D., Nasbit, R.E., Coe, R.L. & Mallet, J. 2001b. Reproductive isolation caused by colour pattern mimicry. Nature 411: 302-305.
17. Johnson, N.A. 2000. Speciation: Dobzhansky-Muller incompatibilities, dominance and gene interactions. Trends. Ecol. Evol. 15: 480-481.
18. Laurie, C. 1997. The weaker sex is heterogametic: 75 years of Haldane's rule. Genetics 147: 937-951.
19. Lewontin, R.C. & Felsenstein, J. 1965. The robustness of homogeneity test in 2 x N tables. Biometrics 21: 19-33.
20. Linares, M. 1997. Origin of Neotropical mimetic biodiversity from a three-way hybrid zone of Heliconius butterflies. In: Proceedings of the International Symposium on Biodiversity and Systematics in Tropical Ecosystems, Bonn 1994 (H. Ulrich, ed.), Zoologishunginstitut und Museum Alexander Koenig, Bonn.
21. Machado, C.A., Kliman, R.M., Markert, J.A. & Hey, J. 2002. Inferring the history of speciation from multilocus DNA sequence data: the case of Drosophila pseudoobscura and close relatives. Mol. Biol. Evol. 19: 472-488.
22. Mallet, J., McMillan, W.O. & Jiggins, C.D. 1998. Mimicry and warning colour at the boundary between races and species. In: Endless Forms: Species and Speciation (D. J. Howard & S. H. Berlocher, eds), pp. 390-403. Oxford University Press, New York.
23. Mayr, E. 1963 Animal Species and Evolution. Harvard University Press, Cambridge, Mass.
24. McMillan, W.O., Jiggins, C.D. & Mallet, J. 1997. What initiates speciation in passion vine butterflies? Proc. Natl Acad. Sci. U. S. A. 94: 8628-8633.
25. Naisbit, R., Jiggins, C.D., Linares, M., Salazar, C. & Mallet, J. 2002a. Hybrid sterility, Haldane's rule and speciation in Heliconius cydno and H. melpomene. Genetics 161: 1517-1526.
26. Naisbit, R., Jiggins, C.D. & Mallet, J. 2002b. Disruptive sexual selection against hybrids contributes to speciation between Heliconius cydno and Heliconius melpomene. Proc. R. Soc. Lond. B Biol. Sci. 268: 1-6.
27. Naisbit, R., Jiggins, C.D. & Mallet, J. 2003. Mimicry: developmental genes that contribute to speciation. Evol. Dev. 5: 269-280.
28. Nichols, R.A. 2001. Gene trees and species trees are not the same. Trends Ecol. Evol. 16: 358-364.
29. Orr, H.A. 1995. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139: 1805-1813.
30. Orr, H.A. 1997. Haldane's rule. Annu. Rev. Ecol. Sys. 28: 195-218.
31. Orr, H.A. & Turelli, M. 2001. The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution 55: 1085-1094.
32. Pääbo, S. 2003. The mosaic that is our genome. Nature 421: 409-412.
33. Perez, D.E., Wu, C.I., Johnson, N.A. & Wu, M.L. 1993. Genetics of reproductive isolation in the Drosophila simulans clade: DNA marker-assisted mapping and characterization of a hybrid-male sterility gene, Odysseus (Ods). Genetics 134: 261-275.
34. Presgraves, D.C. 2002. Patterns of postzygotic isolation in Lepidoptera. Evolution 56: 1168-1183.
35. Presgraves, D.C., Balagopalan, L., Abmayr, S.M. & Orr, H.A. 2003. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423: 715-719.
36. 1 postzygotic incompatibilities in birds. Evolution 45: 1707-1709.
37. Read, A. & Nee, S. 1991. Is Haldane's rule significant? Evolution 45: 1707-1709.
38. Rieseberg, L.H. 1997. Hybrid origins of plant species. Annu. Rev. Ecol. Sys. 28: 359-389.
39. Rieseberg, L.H., Raymond, O., Rosenthal, D.M., Lai, Z., Livingstone, K., Nakazato, T., Durphy, J.L., Schwarzbach, A.E., Donovan, L.A. & Lexer, C. 2003. Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization. Science 301: 1211-1216.
40. Sasa, M.M., Chippendale, P.T. & Johnson, N.A. 1998. Patterns of postzygotic isolation in frogs. Evolution 52: 1811-1820.
41. Seehausen, O. 2004. Hybridization and adaptive radiation. Trends Ecol. Evol. 19: 198-207.
42. Sheppard, P.M., Turner, J.R.G., Brown, K.S., Benson, W.W. & Singer, M.C. 1985. Genetics and the evolution of muellerian mimicry in Heliconius butterflies. Philos. Trans. R. Soc. Lond. B Biol. Sci. 308: 433-613.
43. Takahata, N. & Slatkin, M. 1984. Mitochondrial gene flow. Proc. Natl Acad. Sci. U. S. A. 81: 1764-1767.
44. Tao, Y. & Hartl, D.L. 2003. Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. III. Heterogeneous accumulation of hybrid incompatibilities, degree of dominance, and implications for Haldane's rule. Evolution 57: 2580-2598.
45. Tao, Y., Zeng, Z., Li, J., Hartl, D.L. & Laurie, C. 2003. Genetic Dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. II. Mapping hybrid male sterility loci on the third chromosome. Genetics 164: 1399-1418.
46. Ting, C.T., Tsaur, S.C. & Wu, C.I. 2000. The phylogeny of closely related species as revealed by the genealogy of a speciation gene, Odysseus. Proc. Natl Acad. Sci. U. S. A. 97: 5313-5316.
47. Turelli, M. 1998. The causes of Haldane's rule. Science 282: 889-891.
48. Turelli, M. & Orr, H.A. 1995. The Dominance Theory of Haldane's rule. Genetics 140: 389-402.
49. Turelli, M. & Orr, H.A. 2000. Dominance, epistasis and the genetics of postzygotic isolation. Genetics 154: 1663-1679.
50. Wittbrodt, J., Adam, D., Malitschek, B., Maueler, W., Raulf, F., Telling, A., Robertson, S.M. & Schartl, M. 1989. Novel putative receptor tyrosine kinase encoded by the melanome inducing Tu locus in Xiphophorus. Nature 341: 415-421.