Natural hybridization in heliconiine butterflies: The species boundary as a continuum

BMC Evolutionary Biology

Volumn 7, Issue , 2007, Pages

  Mallet, James ^a,b,c   Beltrán, Margarita ^a,c   Neukirchen, Walter ^d   Linares, Mauricio ^e  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^c SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^d Universidad de Los Andes ^*  (Germany)

^e UNIVERSIDAD DE LOS ANDES   (Colombia)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPATRY; ARTICLE; BEHAVIOR; BUTTERFLY; ECOLOGY; FEMALE; GENE FLOW; GENE LOCUS; GENETIC DISTANCE; GENETIC TRAIT; GEOGRAPHY; HABITAT; HYBRID; HYBRIDIZATION; LEPIDOPTERA; MALE; MOLECULAR CLOCK; MORPHOLOGY; NONHUMAN; PHENOTYPE; PHYLOGENY; POPULATION; PROKARYOTE; RACE; SPECIES; SPECIES DIFFERENTIATION; ANIMAL; CLASSIFICATION; GENETIC MARKER; GENETICS; POPULATION GENETICS; SPECIES DIFFERENCE;

EUEIDES; HELICONIUS; HELICONIUS ERATO; HELICONIUS HEURIPPA; HELICONIUS HIMERA; LEPIDOPTERA; NYMPHALIDAE; PAPILIONOIDEA; PROKARYOTA;

GENETIC MARKER; MITOCHONDRIAL DNA;

ANIMALS; BUTTERFLIES; DNA, MITOCHONDRIAL; GENETIC MARKERS; GENETIC SPECIATION; GENETICS, POPULATION; HYBRIDIZATION, GENETIC; PHYLOGENY; SPECIES SPECIFICITY;

EID: 33947277824     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-7-28     Document Type: Article

References (102)

1. Sympatric speciation in phytophagous insects: moving beyond controversy? SH Berlocher JL Feder, Ann Rev Entomol 2002 47 773 815 10.1146/annurev.ento.47. 091201.145312
2. Host races in plant-feeding insects and their importance in sympatric speciation. M Drès J Mallet, Phil Trans Roy Soc Lond B 2002 357 471 492 10.1098/rstb.2002.1059
3. Genetic evidence for female host-specific races of the common cuckoo. HL Gibbs MD Sorenson K Marchetti LB de NB Davies H Nakamura, Nature 2000 407 183 186 10.1038/35025058 11001055
4. Genetic structure and epidemiology of Ascaris populations: patterns of host affiliation in Guatemala. TJC Anderson ME Romero-Abal J Jaenike, Parasitol 1993 107 319 334
5. Mitochondrial DNA and Ascaris epidemiology: the composition of parasite populations from individual hosts, families and villages. TJC Anderson ME Romero-Abal J Jaenike, Parasitol 1995 110 221 229
6. Biochemical-genetic and ecological evidence that red/brown individuals of the anemone Actinia equina comprise two morphs in Britain. DLJ Quicke AM Donoghue RC Brace, Marine Biol 1983 77 29 37 10.1007/BF00393207
7. Genetic evidence for assortative mating between 13-year cicadas and sympatric "17-year cicadas with 13-year life cycles" provides support for allochronic speciation. C Simon J Tang S Dalwadi G Staley J Deniega TR Unnasch, Evolution 2000 54 1326 1336 10.1554/0014-3820(2000)054[1326:GEFAMB]2.0. CO;2 11005299
8. Parallel speciation by natural selection. D Schluter LM Nagel, Amer Nat 1995 146 292 301 10.1086/285799
9. Cichlid fish diversity threatened by eutrophication that curbs sexual selection. O Seehausen JJM van Alphen F Witte, Science 1997 277 1808 1811 10.1126/science.277.5333.1808
10. Correlated trophic specialization and genetic divergence in sympatric lake whitefish ecotypes (Coregonus clupeaformis): support for the ecological speciation hypothesis. G Lu L Bernatchez, Evolution 1999 53 1491 1505 10.2307/2640895
11. Mitochondrial DNA analysis of sympatric morphotypes of bottlenose dolphins (genus: Tursiops) in Chinese waters. JY Wang LS Chou BN White, Molec Ecol 1999 8 1603 1612 10.1046/j.1365-294x.1999.00741.x
12. Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters. JKB Ford GM Ellis LG Barrett-Lennard AB Morton RS Palm KC Balcomb, Canad J Zool 1998 76 1456 1471 10.1139/cjz-76-8-1456
13. Taxonomic inflation: its influence on macroecology and conservation. NJB Isaac J Mallet GM Mace, Trends Ecol Evol 2004 19 464 469 10.1016/j.tree.2004.06. 004 16701308
14. ML Arnold, Natural Hybridization and Evolution Oxford: Oxford University Press 1997
15. Hybridization of bird species. PR Grant BR Grant, Science 1992 256 193 197 10.1126/science.256.5054.193
16. The problems with hybrids: setting conservation guidelines. FW Allendorf RF Leary P Spruell JK Wenburg, Trends Ecol Evol 2001 16 613 622 10.1016/S0169-5347(01)02290-X
17. Hybridization and adaptive radiation. O Seehausen, Trends Ecol Evol 2003 19 198 207 10.1016/j.tree.2004.01.003
18. Hybridization as an invasion of the genome. J Mallet, Trends Ecol Evol 2005 20 229 237 10.1016/j.tree.2005.02.010 16701374
19. E Mayr, Animal Species and Evolution Cambridge, Mass.: Harvard University Press 1963
20. E Mayr, The Growth of Biological Thought. Diversity, Evolution, and Inheritance Cambridge, Mass.: Belknap 1982
21. E Mayr, Systematics and Origin of Species New York: Columbia Univ. Press 1942
22. JA Endler, Geographic Variation, Speciation, and Clines Princeton, N.J.: Princeton University Press 1977
23. Adaptation, speciation and hybrid zones. NH Barton GM Hewitt, Nature 1989 341 497 503 10.1038/341497a0 2677747
24. JA Coyne HA Orr, Speciation Sunderland, Mass.: Sinauer Associates 2004
25. Species concepts. J Mallet, Evolutionary Genetics. Concepts and Case Studies Oxford: Oxford University Press, Fox CW, 2006 367 373
26. RG Harrison, Hybrid Zones and the Evolutionary Process New York: Oxford University Press 1993
27. What do hybrid zones in general, and the Chorthippus parallelus zone in particular, tell us about speciation. R Butlin, Endless Forms: Species and Speciation New York: Oxford University Press, Howard DJ, 1998 367 389
28. Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. S Via, Evolution 1999 53 1446 1457 10.2307/2640891
29. The biology of Heliconius and related genera. KS Brown, Ann Rev Entomol 1981 26 427 456 10.1146/annurev.en.26.010181.002235
30. Do pollen feeding and pupal-mating have a single origin in Heliconius? Inferences from multilocus sequence data. M Beltrán CD Jiggins AVZ Brower E Bermingham J Mallet, Biol J Linn Soc 2007
31. Cladistic analysis of Heliconius butterflies and relatives (Nymphalidae: Heliconiiti): a revised phylogenetic position for Eueides based on sequences from mtDNA and a nuclear gene. AVZ Brower MG Egan, Proc Roy Soc Lond B 1997 264 969 977 10.1098/rspb.1997.0134
32. Higher level phylogeny for the passion vine butterflies (Nymphalidae, Heliconiinae) based on early stage and adult morphology. CM Penz, Zool J Linn Soc 1999 127 277 344 10.1006/zjls.1998.0187
33. Adaptive radiation and convergence in subdivisions of the butterfly genus Heliconius (Lepidoptera: Nymphalidae). JRG Turner, Zool J Linn Soc 1976 58 297 308
34. Diversity in mimicry: paradox or paradigm? M Joron J Mallet, Trends Ecol Evol 1998 13 461 466 10.1016/S0169-5347(98)01483-9
35. Adaptation and evolution in Heliconius: a defense of neo-Darwinism. JRG Turner, Ann Rev Ecol Syst 1981 12 99 121 10.1146/annurev.es.12.110181.000531
36. Speciation, raciation, and color pattern evolution in Heliconius butterflies: evidence from hybrid zones. J Mallet, Hybrid Zones and the Evolutionary Process New York: Oxford University Press, Harrison RG, 1993 226 260
37. Mimicry and warning color at the boundary between races and species. J Mallet WO McMillan CD Jiggins, Endless Forms: Species and Speciation New York: Oxford Univ. Press, Howard DJ, 1998 390 403
38. Reproductive isolation caused by colour pattern mimicry. CD Jiggins RE Naisbit RL Coe J Mallet, Nature 2001 411 302 305 10.1038/35077075 11357131
39. Assortative mating and speciation as pleiotropic effects of ecological adaptation: examples in moths and butterflies. CD Jiggins I Emelianov J Mallet, Insect Evolutionary Ecology London: Royal Entomological Society, Fellowes M, 2005 451 473
40. An illustrated list of the type-specimens of the Heliconiinae (Lepidoptera: Nymphalidae) in the British Museum (Natural History). PR Ackery RL Smiles, Bull Brit Mus (Nat Hist), Entomol 1976 32 171 214
41. An illustrated key to the silvaniform Heliconius (Lepidoptera: Nymphalidae) with descriptions of new subspecies. KS Brown, Trans Amer Entomol Soc 1976 102 373 484
42. Semispecies relationships between Heliconius erato cyrbia Godt. and H. himera Hew. in southwestern Ecuador. H Descimon J Mast de Maeght, J Res Lepid 1984 22 229 239
43. Los Heliconiini (Lepidoptera, Nymphalidae) de Venezuela. KS Brown F Fernandez Yepez, Bol Entomol Venez 1985 N.S.3 29 76
44. H Holzinger R Holzinger, Heliconius and Related Genera. Lepidoptera: Nymphalidae. The Genera Eueides, Neruda and Heliconius Venette, France: Sciences Nat 1994
45. What can hybrid zones tell us about speciation? The case of Heliconius erato and H. himera (Lepidoptera: Nymphalidae). CD Jiggins WO McMillan W Neukirchen J Mallet, Biol J Linn Soc 1996 59 221 242 10.1006/bijl.1996.0063
46. Estimating the mating behavior of a pair of hybridizing Heliconius species in the wild. J Mallet WO McMillan CD Jiggins, Evolution 1998 52 503 510 10.2307/2411085
47. Adaptive novelty through introgression in Heliconius wing patterns: evidence for a shared genetic "toolbox" from synthetic hybrid zones and a theory of diversification. LE Gilbert, Ecology and Evolution Taking Flight: Butterflies as Model Systems Chicago: University of Chicago Press, Boggs CL, 2003 281 318
48. P Smart, The Illustrated Encyclopaedia of the Butterfly World London: Hamlyn 1976
49. B D'Abrera, Butterflies of the Neotropical region, Part II. Danaidae, Ithomiidae, Heliconidae & Morphidae edn Ferny Creek, Victoria, Australia: Hill House 1984
50. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. AVZ Brower, Proc Natl Acad Sci, USA 1994 91 6491 6495 10.1073/pnas.91.14.6491
51. The maintenance of species differences across a Heliconius hybrid zone. CD Jiggins WO McMillan P King J Mallet, Heredity 1997 79 495 505 10.1038/sj.hdy.6882230
52. Genetic evidence for a sibling species of Heliconius charithonia (Lepidoptera: Nymphalidae). CD Jiggins N Davies, Biol J Linn Soc 1998 64 57 67 10.1006/bijl.1997.0211
53. Bimodal hybrid zones and speciation. CD Jiggins J Mallet, Trends Ecol Evol 2000 15 250 255 10.1016/S0169-5347(00)01873-5 10802556
54. Polyphyly and gene flow between non-sibling Heliconius species. V Bull M Beltrán CD Jiggins WO McMillan E Bermingham J Mallet, BMC Biol 2006 4 11 16630334 10.1186/1741-7007-4-11
55. Multilocus analysis of admixture and introgression among hybridizing Heliconius butterflies. MR Kronforst LG Young LM Blume LE Gilbert, Evolution 2006 60 1254 1268 10.1554/06-005.1 16892975
56. Heliconiinae. G Lamas, Hesperioidea - Papilionoidea Gainesville, Florida: Association for Tropical Lepidoptera. Scientific Publishers, Lamas G, 2004 261 274
57. Natural hybrids of Papilio (Insecta: Lepidoptera): poor taxonomy or interesting evolutionary problem? FAH Sperling, Canad J Zool 1990 68 1790 1799
58. Slow evolutionary loss of the potential for interspecific hybridization in birds: a manifestation of slow regulatory evolution. EM Prager AC Wilson, Proc Natl Acad Sci, USA 1975 72 200 204 10.1073/pnas.72.1.200
59. E Mayr, Toward a New Philosophy of Biology Cambridge, Mass.: Harvard University Press 1988
60. Extinction by hybridization and introgression. JM Rhymer D Simberloff, Ann Rev Ecol Syst 1996 27 83 109 10.1146/annurev.ecolsys.27.1.83
61. Hybrids consummate species invasion. W Roush, Science 1997 277 316 317 10.1126/science.277.5324.316
62. Plant chemistry and the evolution of host specificity: new evidence from Heliconius and Passiflora. JT Smiley, Science 1978 201 745 747 10.1126/science.201.4357.745
63. Patterns of pollen feeding and habitat preference among Heliconius species. C Estrada CD Jiggins, Ecol Entomol 2002 27 448 456 10.1046/j.1365-2311. 2002.00434.x
64. The effect of DNA sequence divergence on sexual isolation in Bacillus. MS Roberts FM Cohan, Genetics 1993 134 401 408 8325477
65. Hybrid sterility, Haldane's rule, and speciation in Heliconius cydno and H. melpomene. RE Naisbit CD Jiggins M Linares J Mallet, Genetics 2002 161 1517 1526 12196397
66. Speciation by hybridization in Heliconius butterflies. J Mavárez C Salazar E Bermingham C Salcedo CD Jiggins M Linares, Nature 2006 441 868 871 10.1038/nature04738 16778888
67. Patterns of postzygotic isolation in Lepidoptera. DC Presgraves, Evolution 2002 56 1168 1183 10.1554/0014-3820(2002)056[1168:POPIIL]2.0.CO;2 12144018
68. What initiates speciation in passion-vine butterflies? WO McMillan CD Jiggins J Mallet, Proc Natl Acad Sci, USA 1997 94 8628 8633 10.1073/pnas.94.16. 8628
69. Hybrid incompatibility is consistent with a hybrid origin of Heliconius heurippa Hewitson from its close relatives, Heliconius cydno Doubleday and Heliconius melpomene Linnaeus. CA Salazar CD Jiggins CF Arias A Tobler E Bermingham M Linares, J Evol Biol 2005 18 247 256 10.1111/j.1420-9101.2004. 00839.x 15715831
70. Sex-linked hybrid sterility in a butterfly. CD Jiggins M Linares RE Naisbit C Salazar Z Yang J Mallet, Evolution 2001 55 1631 1638 10.1554/0014-3820(2001)055[1631:SLHSIA]2.0.CO;2 11580022
71. C Darwin, On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life London: John Murray 1859
72. Mimicry: developmental genes that contribute to speciation. RE Naisbit CD Jiggins J Mallet, Evol Devel 2003 5 269 280 10.1046/j.1525-142X.2003.03034.x
73. M Linares, Adaptive microevolution through hybridization and biotic destruction in the neotropics University of Texas at Austin Ph.D. 1989
74. The ghost of mimicry past: laboratory reconstitution of an extinct butterfly 'race'. M Linares, Heredity 1997 78 628 635 10.1038/sj.hdy.6881520
75. Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. MR Kronforst LG Young DD Kapan C McNeely RJ O'Neill LE Gilbert, Proc Natl Acad Sci, USA 2006 103 6575 6580 10.1073/pnas.0509685103
76. Hybrid speciation. J Mallet, Nature 2007
77. Genealogical perspectives on the species problem. DA Baum KL Shaw, Experimental and Molecular Approaches to Plant Biosystematics St. Louis, Missouri: Missouri Botanical Garden, Hoch PC, 1995 289 303
78. Gene trees in species trees. WP Maddison, Syst Biol 1997 46 523 536 10.2307/2413694
79. Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. RL Wang J Wakeley J Hey, Genetics 1997 147 1091 1106 9383055
80. Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. CS Wilding RK Butlin J Grahame, J Evol Biol 2001 14 611 619 10.1046/j.1420-9101.2001.00304.x
81. Genomic evidence for divergence with gene flow in host races of the larch budmoth. I Emelianov F Marec J Mallet, Proc Roy Soc Lond B 2004 271 97 105 10.1098/rspb.2003.2574
82. Genomic islands of speciation in Anopheles gambiae. TL Turner MW Hahn SV Nuzhdin, Public Library of Science - Biology 2005 3 e285, 1572 e285, 1578
83. A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. M Joron R Papa M Beltrán N Chamberlain J Mavárez S Baxter, Public Library of Science - Biology 2006 4 e303
84. Phylogenetic classification and the universal tree. WF Doolittle, Science 1999 284 2124 2129 10.1126/science.284.5423.2124 10381871
85. A species definition for the Modern Synthesis. J Mallet, Trends Ecol Evol 1995 10 294 299 10.1016/0169-5347(95)90031-4
86. Speciation in Heliconius (Lep., Nymphalidae): morphology and geographic distribution. MG Emsley, Zoologica, N Y 1965 50 191 254
87. Why are there so many mimicry rings? Correlations between habitat, behaviour and mimicry in Heliconius butterflies. J Mallet LE Gilbert, Biol J Linn Soc 1995 55 159 180 10.1006/bijl.1995.0034
88. Genetics and the evolution of muellerian mimicry in Heliconius butterflies. PM Sheppard JRG Turner KS Brown WW Benson MC Singer, Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 1985 308 433 613 10.1098/rstb.1985.0066
89. The genetics of warning colour in Peruvian hybrid zones of Heliconius erato and H. melpomene. J Mallet, Proc Roy Soc Lond B 1989 236 163 185
90. The genetic basis of an adaptive radiation: warning colour in two Heliconius species. CD Jiggins WO McMillan, Proc Roy Soc Lond B 1997 264 1167 1175 10.1098/rspb.1997.0161
91. The genetics of the mimetic coloration in the butterfly Heliconius cydno weymeri. M Linares, J Hered 1996 87 142 149
92. Localization of Müllerian mimicry genes on a dense linkage map of Heliconius erato. DD Kapan NS Flanagan A Tobler R Papa RD Reed J cevedo Gonzalez, Genetics 2006 173 735 757 16489214 10.1534/genetics.106.057166
93. A genetic linkage map of the mimetic butterfly, Heliconius melpomene. CD Jiggins J Mavárez M Beltrán WO McMillan JS Johnston E Bermingham, Genetics 2005 171 557 570 15489522 10.1534/genetics.104.034686
94. Adaptive polymorphism associated with multiple Müllerian mimicry in Heliconius numata (Lepid.: Nymph.). KS Brown WW Benson, Biotropica 1974 6 205 228 10.2307/2989666
95. Variable selection and the coexistence of multiple mimetic forms of the butterfly Heliconius numata. M Joron IR Wynne G Lamas J Mallet, Evol Ecol 2001 13 721 754 10.1023/A:1010875213123
96. Three-butterfly system provides a field test of Müllerian mimicry. DD Kapan, Nature 2001 409 338 340 10.1038/35053066 11201741
97. Causes and consequences of a lack of coevolution in Müllerian mimicry. J Mallet, Evol Ecol 2001 13 777 806 10.1023/A:1011060330515
98. Parallel genetic architecture of parallel adaptive radiations in mimetic Heliconius butterflies. MR Kronforst DD Kapan LE Gilbert, Genetics 2006 174 535 539 16783007 10.1534/genetics.106.059527
99. The biology of butterfly communities. LE Gilbert, The Biology of Butterflies London: Academic Press, Vane-Wright RI, 1984 41 54
100. Phylogeny of Heliconius butterflies inferred from mitochondrial DNA sequences (Lepidoptera: Nymphalinae). AVZ Brower, Molec Phylog Evol 1994 3 159 174 10.1006/mpev.1994.1018
101. A heuristic rate smoothing procedure for maximum likelihood estimation of species divergence times. Z Yang, Acta Zoo Sin 2004 50 645 656
102. Hybrids between species of Heliconius and Eueides butterflies: a database. J Mallet W Neukirchen M Linares, 2006 http://www.ucl.ac.uk/taxome/hyb/