Do pollen feeding, pupal-mating and larval gregariousness have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data

Biological Journal of the Linnean Society

Volumn 92, Issue 2, 2007, Pages 221-239

  Beltrán, Margarita ^a,b,c   Jiggins, Chris D ^c   Brower, Andrew V Z ^d   Bermingham, Eldredge ^a   Mallet, James ^b  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d MIDDLE TENNESSEE STATE UNIVERSITY   (United States)

Author keywords

Bayesian analysis; Ef1 ; Mimicry; mtDNA; Parsimony; Phylogeny

Indexed keywords

ADAPTATION; BAYESIAN ANALYSIS; BUTTERFLY; DNA; GENE EXPRESSION; LARVA; LIFE HISTORY TRAIT; MATING BEHAVIOR; MIMICRY; PARSIMONY ANALYSIS; PHYLOGENETICS; POLLEN; PUPA;

HELICONIUS; HELICONIUS DORIS; NERUDA; PAPILIONOIDEA;

EID: 34548740770     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2007.00830.x     Document Type: Article

References (78)

1. Barraclough TG, Harvey PH, Nee S. 1995. Sexual selection and taxonomic diversity in Passerine birds. Proceedings of the Royal Society of London Series B, Biological Sciences 259 : 211 215.
2. Barraclough TG, Hogan JE, Vogler AP. 1999. Testing whether ecological factors promote cladogenesis in a group of tiger beetles (Coleoptera: Cicindelidae). Proceedings of the Royal Society of London Series B, Biological Sciences 266 : 1061 1067.
3. Barraclough TG, Nee S. 2001. Phylogenetics and speciation. Trends in Ecology and Evolution 16 : 391 399.
4. Beltrán M. 1999. Genetic evidence to evaluate the possible hybrid origin of Heliconius heurippa (Lepidoptera: Nymphalidae). Master's Thesis, Andes University.
5. Beltrán M, Jiggins CD, Bull V, Linares M, Mallet J, McMillan WO, Bermingham E. 2002. Phylogenetic discordance at the species boundary: comparative gene genealogies among rapidly radiating Heliconius butterflies. Molecular Biology and Evolution 19 : 2176 2190.
6. Bischoff C, Kahns S, Lund A, Jorgensen HF, Praestegaard M, Clark BF, Leffers H. 2002. The human elongation factor 1 A-2 gene (EF1A2): complete sequence and characterization of gene structure and promoter activity. Genomics 68 : 63 70.
7. Boggs CL, Smiley JT, Gilbert LE. 1981. Patterns of pollen exploitation by Heliconius butterflies. Oecologia 48 : 284 289.
8. Brower AVZ. 1994a. Phylogeny of Heliconius butterflies inferred from mitochondrial DNA sequences (Lepidoptera: Nymphalidae). Molecular Phylogenetics and Evolution 3 : 159 174.
9. Brower AVZ. 1994b. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA Evolution. Proceedings of the National Academy of Sciences of the United States of America 91 : 6491 6495.
10. Brower AVZ. 1995. Locomotor mimicry in butterflies? A critical review of the evidence. Philosophical Transactions of the Royal Society of London B 347 : 413 425.
11. Brower AVZ. 1996a. A new mimetic species of Heliconius (Lepidoptera: Nymphalidae), from southeastern Colombia, revealed by cladistic analysis of mitochondrial DNA sequences. Zoological Journal of the Linnean Society 116 : 317 332.
12. Brower AVZ. 1996b. Parallel race formation and the Evolution of mimicry in Heliconius butterflies: a phylogenetic hypothesis from mitochondrial DNA sequences. Evolution 50 : 195 221.
13. Brower AVZ. 1997. The evolution of ecologically important characters in Heliconius butterflies (Lepidoptera: Nymphalidae): a cladistic review. Zoological Journal of the Linnean Society 119 : 457 472.
14. Brower AVZ, DeSalle R. 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 Molecular Biology 7 : 73 82.
15. Brower AVZ, DeSalle R, Vogler A. 1996. Gene trees, species trees, and systematics: a cladistic perspective. Annual Review of Ecology and Systematics 27 : 423 450.
16. Brower AVZ, Egan MG. 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. Proceedings of the Royal Society of London Series B, Biological Sciences 264 : 969 977.
17. Brown KS. 1981. The biology of Heliconius and related genera. Annual Review of Entomology 26 : 427 456.
18. Brown KS, Benson WW. 1977. Evolution in modern amazonian non-forest islands: Heliconius hermathena. Biotropica 9 : 95 117.
19. Bull V, Beltrán M, Jiggins CD, McMillan WO, Bermingham E, Mallet J. 2006. Polyphyly and gene flow between non-sibling Heliconius species. BMC Biology 4 : 11.
20. Cardoso NZ. 2001. Patterns of pollen collection and flower visitation by Heliconius butterflies in southeastern Mexico. Journal of Tropical Ecology 17 : 763 768.
21. Caterino MS, Sperling FAH. 1999. Papilio phylogeny based on mitochondrial cytochrome oxidase I and II genes. Molecular Phylogenetics and Evolution 11 : 122 137.
22. Cho SW, Mitchell A, Regier JC, Mitter C, Poole RW, Friedlander TP, Zhao SW. 1995. A highly conserved nuclear gene for low-level Phylogenetics - elongation factor-1-alpha recovers morphology-based tree for Heliothine moths. Molecular Biology and Evolution 12 : 650 656.
23. Deinert EI, Longino JT, Gilbert LE. 1994. Mate competition in butterflies. Nature 370 : 23 24.
24. DeSalle R. 1992. The phylogenetic relationships of flies in the family Drosophilidae deduced from mtDNA sequences. Molecular Phylogenetics and Evolution 1 : 31 40.
25. Emsley MG. 1963. A morphological study of imagine Heliconiinae (Lep. Nymphalidae) with a consideration of the evolutionary relationships within the group. Zoologica 48 : 85 130.
26. Emsley MG. 1965. Speciation in Heliconius (Lep., Nymphalidae): morphology and geographic distribution. Zoologica (New York) 50 : 191 254.
27. Farris JS, Kallersjo M, Kluge AG, Bult C. 1994. Testing significance of incongruence. Cladistics 10 : 315 319.
28. Felsenstein J. 1981. Evolutionary trees from DNA sequences a Maximum-likelihood approach. Journal of Molecular Evolution 17 : 368 376.
29. Flanagan N, Tobler A, Davison A, Pybus OG, Kapan DD, Planas S, Linares M, Heckel DG, McMillan W. 2004. Historical demography of Mullerian mimicry in the Neotropical Heliconius butterflies. Proceedings of the National Academy of Science United States of America. 101 : 9704 9709.
30. Gilbert LE. 1972. Pollen feeding and reproductive biology of Heliconius butterflies. Proceedings of the National Academy of Sciences of the United States of America 69 : 1403 1407.
31. Gilbert LE. 1976. Postmating female odor in Heliconius butterflies: a male-contributed antiaphrodisiac? Science 193 : 419 420.
32. Gilbert LE. 1991. Biodiversity of a Central American Heliconius community: pattern, process, and problems. In : Price PW, Lewinsohn TM, Fernandes TW, Benson WW, eds. Plant-animal interactions: evolutionary ecology in tropical and temperate regions. New York, NY : John Wiley and Sons, 403 427.
33. Goldman N, Anderson JP, Rodrigo AG. 2000. Likelihood-based tests of topologies in phylogenetics. Systematic Biology 49 : 652 670.
34. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17 : 754 755.
35. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. 2001. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294 : 2310 2314.
36. Jiggins CD, Davies N. 1998. Genetic evidence for a sibling species of Heliconius charithonia (Lepidoptera; Nymphalidae). Biological Journal of the Linnean Society 64 : 57 67.
37. Jiggins CD, Mavárez J, Beltrán M, McMillan WO, Johnston JS, Bermingham E. 2005. A genetic linkage map of the mimetic butterfly, Heliconius melpomene. Genetics 171 : 557 570.
38. Jiggins CD, McMillan WO, Neukirchen W, Mallet J. 1996. What can hybrid zones tell us about speciation? The case of Heliconius erato and H. himera (Lepidoptera: Nymphalidae). Biological Journal of the Linnean Society 59 : 221 242.
39. Kimura Y. 1980. A simpler method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16 : 111 120.
40. Krenn HW, Penz CM. 1998. Mouthparts of Heliconius butterflies (Lepidoptera: Nymphalidae): a search for anatomical adaptations to pollen-feeding behavior. International Journal of Insect Morphology and Embryology 27 : 301 309.
41. Krenn HW, Zulka KP, Gatschnegg T. 2001. Proboscis morphology and food preferences in nymphalid butterflies (Lepidoptera: Nymphalidae). Journal of Zoology 254 : 17 26.
42. Kronforst MR, Young LG, Blume LM, Gilbert LE. 2006. Multilocus analyses of admixture and introgression among hybridizing Heliconius butterflies. Evolution 60 : 1254 1268.
43. Lamas G. 1998. Comentarios taxonómicos y nomenclaturales sobre. Heliconiini neotropicales, con designación de lectotipos y descripción de cuatro subespecies nuevas (Lepidoptera: Nymphalidae: Heliconiinae). Revista Peruana de Entomologia 40 : 111 125.
44. Lamas G, Callaghan C, Casagrande MM, Mielke O, Pyrcz T, Robbins R, Viloria A. 2004. Hesperioidea and Papilionoidea. Gainesville, FL : Association for Tropical Lepidoptera.
45. Maddison WP, Maddison DR. 1997. MacClade. Analysis of phylogeny and character evolution, Version 3.07. Sunderland, MA : Sinauer Associates.
46. Mallet J. 2005. Hybridization as an invasion of the genome. Trends in Ecology and Evolution 20 : 229 237.
47. Mallet J, McMillan WO, Jiggins CD. 1998. Mimicry and warning colour at the boundary between races and species. In : Howard DJ, Berlocher SH, eds. Endless forms: species and speciation. New York, NY : Oxford University Press, 390 403.
48. Mallet J, Neukirchen W, Linares M. 2006. Hybrids between species of Heliconius and Eueides butterflies: a database. Available at: http://www.ucl.ac.uk/taxome/hyb/helichyb.htlm.
49. Mavárez J, Salazar C, Bermingham E, Salcedo C, Jiggins CD, Linares M. 2006. Speciation by hybridization in Heliconius butterflies. Nature. 441 : 868 871.
50. McMillan WO, Jiggins CD, Mallet J. 1997. What initiates speciation in passion-vine butterflies? Proceedings of the National Academy of Sciences of the United States of America 94 : 8628 8633.
51. Michener CD. 1942. A generic version of the Heliconiinae (Lepidoptera, Nymphalidae). American Museum Novitates 1197 : 1 8.
52. Miller JS, Brower AVZ, DeSalle R. 1997. Phylogeny of the neotropical moth tribe Josiini (Notodontidae: Dioptinae): comparing and combining evidence from DNA sequences and morphology. Biological Journal of the Linnean Society 60 : 297 316.
53. Miller JS, Wenzel JW. 1995. Ecological characters and phylogeny. Annual Review of Entomology 40 : 389 415.
54. Mitchell A, Cho S, Regier JC, Mitter C, Poole RW, Matthews M. 1997. Phylogenetic utility of elongation factor-1 alpha in Noctuoidea (Insecta: Lepidoptera): The limits of synonymous substitution. Molecular Biology and Evolution 14 : 381 390.
55. Mitter C, Brooks DR. 1983. Phylogenetic aspects of coevolution. In : Coevolution. In : Futuyma DJ Slatkin M, eds. Sunderland, MA : Sinauer Associates, 65 98.
56. Mitter C, Farrell B, Wiegmann BM. 1988. The phylogenetic study of adaptative zone: has phytophagy promoted insect diversification? American Naturalist 132 : 107 128.
57. Nahrstedt A, Davis RH. 1981. The occurrence of the cyanoglucosides, Linamarin and Lotaustralin, in Acraea and Heliconius butterflies. Comparative Biochemistry and Physiology B, Biochemistry and Molecular Biology 68 : 575 577.
58. Naisbit RE, Jiggins CD, Linares M, Salazar C, Mallet J. 2002. Hybrid sterility, Haldane's rule and speciation in Heliconius cydno and H. melpomene. Genetics 161 : 1517 1526.
59. Nijhout HF. 1991. The development and evolution of butterfly wing patterns. Washington, DC : Smithsonian Institution Press.
60. Palumbi SR. 1996. Nucleic acids II: the polymerase chain reaction. In : Hillis DM, Moritz C, Mable B, eds. Molecular systematics. Sunderland, MA : Sinauer Associates, 655.
61. Penz CM. 1999. Higher level phylogeny for the passion-vine butterflies (Nymphalidae, Heliconiinae) based on early stage and adult morphology. Zoological Journal of the Linnean Society 127 : 277 344.
62. Penz CM, Krenn HW. 2000. Behavioral adaptations to pollen-feeding in Heliconius butterflies (Nymphalidae, Heliconiinae): an experiment using Lantana flowers. Journal of Insect Behavior 13 : 865 880.
63. Penz CM, Peggie D. 2003. Phylogenetic relationships among Heliconiinae genera based on morphology (Lepidoptera: Nymphalidae). Systematic Entomology 28 : 451 479.
64. Posada D, Crandall KA. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14 : 817 818.
65. Reed RD, Sperling FAH. 1999. Interaction of process partitions in phylogenetic analysis: an example from the swallowtail butterfly genus Papilio. Molecular Biology and Evolution 16 : 286 297.
66. Salazar C, Jiggins CD, Arias CF, Tobler A, Bermingham E, Linares M. 2005. 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 18 : 247 256.
67. Shimodaira H, Hasegawa M. 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16 : 1114 1116.
68. Sillén-Tullberg B. 1988. Evolution of gregariousness in aposematic butterfly larvae: a phylogenetic analysis. Evolution 42 : 293 305.
69. Smith P, Kambhampati S, Armstrong K. 2002. Phylogenetic relationships among Bactrocera species (Diptera: Tephritidae) inferred from mitochrondrial DNA sequences. Molecular Phylogenetics and Evolution 26 : 8 17.
70. Swofford DL. 2000. PAUP*. Phylogenetic analysis using parsimony (*and other methods), 4th edn. Sunderland, MA : Sinauer Associates.
71. Tamura K, Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10 : 512 526.
72. Thornhill R, Alcock J. 1993. The evolution of insect mating systems. Cambridge, MA : Harvard University Press.
73. Tobler A, Flanagan N, Jiggins CD, Heckel D, Kapan D, McMillan WO. 2005. A genetic map of microsatellite, AFLP, allozyme and colour pattern genes in Heliconius erato. Heredity 94 : 408 417.
74. Turner JRG. 1976. Adaptive radiation and convergence in subdivisions of butterfly genus Heliconius (Lepidoptera-Nymphalidae). Zoological Journal of the Linnean Society 58 : 297 308.
75. Walldorf U, Hovemann BT. 1990. Apis mellifera cytoplasmic Elongation-factor 1-alpha (Ef-1-alpha) is closely related to Drosophila melanogaster Ef-1-alpha. FEBS Letters 267 : 245 249.
76. Wanntorp H-E, Brooks DR, Nilsson T, Nylin S, Ronquist F, Stearns SC, Wedell N. 1990. Phylogenetic approaches in ecology. Oikos 57 : 119 132.
77. Wiens J. 1998. The accuracy of methods for coding and sampling higher-level taxa for phylogenetic analysis: a simulation study. Systematic Biology 47 : 397 413.
78. Yang Z. 1994. Estimating the pattern of nucleotide substitution. Journal of Molecular Evolution 39 : 105 111.