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Loss of male secondary sexual structures in allopatry in the Neotropical butterfly genus Arcas (Lycaenidae: Theclinae: Eumaeini)

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Male secondary sexual characters in Lepidoptera may be present or absent in species that otherwise appear to be closely related, an observation that has led to differences of opinion over the taxonomic usefulness of these structures above the species level. An evolutionary issue raised by this debate is whether male secondary sexual characters (1) can be regained after being lost evolutionarily, (2) are not lost after being evolved, or (3) are ‘switched on and off’ by genes that regulate development. A second evolutionary issue is the conditions under which male secondary sexual characters might be lost or gained evolutionarily. Because these structures are thought to promote species recognition, theory predicts evolutionary losses to be most likely in allopatry; evolutionary gains to be most likely during the process of secondarily establishing sympatry or during sympatric speciation. We updated the species-level taxonomy of the brilliant emerald-winged Neotropical lycaenid butterfly genus Arcas and performed an analysis of phylogenetic relations among species to assess these evolutionary issues. We morphologically detail a scent pouch on the ventral hindwing of Arcas and report that six species possess the pouch with androconia, one possesses the pouch without androconia, and the remaining two species have neither pouch nor androconia. In addition, eight Arcas species have a morphologically species-specific male forewing scent pad, and one lacks a scent pad. This variation appears to be the result of three evolutionary losses and no gains of male secondary sexual organs. The four Arcas species lacking a scent pouch or a scent pad are allopatric with their closest phylogenetic relatives while four of five with both of these structures are sympatric. Although Arcas is a small genus, these results are significantly more extreme than predicted by chance. For taxonomy, this study provides a rationale for the evolutionary loss of male secondary sexual structures and suggests that their absence, but itself, does not indicate a lack of relationship above the species level.

Affiliations: 1: aDepartment of Entomology, PO Box 37012, NHB Stop 105, Smithsonian Institution, Washington, DC 20013-7012, USA ; 2: bDepartamento de Biologia, Universidade Federal do Maranhão, Avenida dos Portugueses s/n, Bacanga 65085-580, São Luís, MA, Brazil ; 3: c7 Countryside Way, Andover, MA 01810-6041, USA; 4: dMuseu de Zoologia, Universidade de São Paulo, Avenida Nazaré 481, Ipiranga, 04263-000 São Paulo, SP, Brazil


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1. Ackery P.R. , Vane-Wright R.I. ( 1984) "Milkweed butterflies: their cladistics and biology". BMNH/Cornell University Press, London/New York, NY, ix + 425pp.
2. Alcock J. , O’Neill K.M. ( 1986) "Density-dependent mating tactics in the gray hairstreak, Strymon melinus(Lepidoptera, Lycaenidae)". Journal of Zoology Vol 209: 105113.
3. Alcock J. , O’Neill K.M. ( 1987) "Territory preferences and intensity of competition in the grey hairstreak Strymon melinus(Lepidoptera: Lycaenidae) and the tarantula hawk wasp Hemipepsis ustulata(Hymenoptera: Pompilidae)". American Midland Naturalist Vol 11: 120138.
4. Austin G.T. , Johnson K. ( 1995) "Theclinae of Rondônia, Brazil: Arcas, with descriptions of three new species (Lepidoptera: Lycaenidae)". Tropical Lepidoptera Vol 6: 3139.
5. Baker T.C. , Cardé R.T. ( 1979) "Courtship behavior of the oriental fruit moth ( Grapholitha molesta): Experimental analysis and consideration of the role of sexual selection in the evolution of courtship pheromones in the Lepidoptera". Annals of the Entomological Society of America Vol 72: 173188.
6. Bálint Z. ( 2002) "Miscellaneous notes on ArcasSwainson, 1832 (Lepidoptera: Lycaenidae, Eumaeini)". Annales Historico-Naturales Musei Nationalis Hungarici Vol 94: 141161.
7. Bálint Z. ( 2006) " ArcasSwainson, 1832 is revisited: review of some species-group names, identification of the sister group and a key for species (Lepidoptera, Lycaenidae: Eumaeini)". Annales Historico-Naturales Musei Nationalis Hungarici Vol 98: 147158.
8. Bálint Z. , Wojtusiak J. ( 2006) "Contribution to the knowledge of Neotropical Lycaenidae — reinstating names of three recently described species and description of a new one (Lepidoptera: Eumaeini)". Genus Vol 17: 273282.
9. Birch M.C. ( 1970) "Structure and function of the pheromone-producing brush organs in males of Phlogophora meticulosa(L.) (Lepidoptera: Noctuidae)". Transactions of the Royal Entomological Society of London Vol 122: 277292.
10. Birch M.C. ( 1972) "Male abdominal brush-organs in British noctuid moths and their value as a taxonomic character". Entomologist Vol 105: 185–205, 233244.
11. Birch M.C. , Poppy G.M. , Baker T.C. ( 1990) "Scents and eversible scent structures of male moths". Annual Review of Entomology Vol 1990: 2558.
12. Boppré M. , Vane-Wright R.I. ( 1989) "Androconial systems in Danainae (Lepidoptera): functional morphology of Amauris, Tirumala, Danausand Euploea ". Zoological Journal of the Linnean Society Vol 97: 101133.
13. Brown K.S. ( 1982) "Historical and ecological factors in the biogeography of aposematic neotropical butterflies". American Zoologist Vol 22: 453471.
14. Brown K.S. ,( 1993) "Selected Neotropical species", In: New T.R. (Ed.) Conservation biology of Lycaenidae (Butterflies) . IUCN, Gland, pp. 146149.
15. Brown K.S. , Freitas A.V.L. ( 2000) "Diversidade de Lepidoptera em Santa Teresa, Espírito Santo". Boletim do Museu de Biologia Mello Leitão (N.S.) Vol 11–12: 71116.
16. Burns J.M. ( 1964) "Evolution in skipper butterflies of the genus Erynnis ". University of California Publications in Entomology. Vol Vol. 37. University of California Press, Berkeley, CA, 214pp.
17. Casagrande M.M. , Mielke O.H. ( 1993) "Borboletas (Lepidoptera) ameaçadas de extinção no Paraná". Revista Brasileira de Zoologia Vol 9: 7592.
18. Comstock J.H. ( 1918) The wings of insects . Comstock, Ithaca, NY, 430pp.
19. Constantino L.M. ( 1997) "Conocimiento de los ciclos de vida y plantas hospederas de lepidópteros diurnos de Colombia como estrategia para el manejo, uso y conservación de poblaciones silvestres". Seminario. Aconteceres entomológicos (Medellín) , pp. 5789.
20. Cordero C. , Macías R. , Jiménez G. ( 2000) "The number of copulations of territorial males of the butterfly Callophrys xami(Lycaenidae)". Journal of Research on the Lepidoptera Vol 35: 7889.
21. de Jong R. ( 1982) "Secondary sexual characters in Celaenorrhinusand the delimitation of the genus (Lepidoptera, Hesperiidae)". Journal of Natural History Vol 16: 695705.
22. Dixey F.A. ( 1910) "The plume-scales of the Pierinae". Proceedings of the Entomological Society of London Vol 1909: xciiicxli.
23. Druce H.H. ( 1907) "On Neotropical Lycaenidae, with descriptions of new species". Proceedings of the Zoological Society of London Vol 1907: 566632.
24. Eberhard W.G. ( 1985) Sexual selection and animal genitalia. Harvard University Press, Cambridge, MA, 244pp.
25. Elias M. , Joron M. , Willmott K. , Silva-Brandão K.L. , Kaiser V. , Arias C.F. , Gomez Piñerez S. , Uribe L.M. , Brower A.V.Z. , Freitas A.V.L. , Jiggins C.D. ( 2009) "Out of the Andes: patterns of diversification in clearwing butterflies". Molecular Ecology Vol 18: 17161729.
26. Eliot J.N. ( 1973) "The higher classification of the Lycaenidae (Lepidoptera): a tentative arrangement". Bulletin of the British Museum (Natural History) Entomology Vol 28: 371505.
27. Faynel C. ( 2003) "Cinq années d’observation sur les Theclinae de Guyane française (Lepidoptera: Lycaenidae)". Bulletin des Lépidoptéristes Parisiens, hors-série: Lépidoptères de Guyane : 4962.
28. Godman F.D. , Salvin O. ( 1887–1901) "Biologia Centrali-Americana. Insecta. Lepidoptera-Rhopalocera". Fam. Lycaenidae. Vol 2: 1112.
29. Goloboff P.A. , Farris J.S. , Nixon K.C. ( 2008) "TNT, a free program for phylogenetic analysis". Cladistics Vol 24: 774786.
30. Gould S.J. ( 1970) "Dollo on Dollo’s Law: Irreversibility and the Status of Evolutionary Laws". Journal of the History of Biology Vol 3: 189212.
31. Grandtner M.M. ( 2005) Elsevier’s dictionary of trees: with names in Latin, English, French, Spanish and other languages . Elsevier, San Diego, CA, 1493pp.
32. Grant G.C. ( 1978) "Morphology of the presumed male pheromone glands on the forewing of tortricid and phycitid moths". Annals of the Entomological Society of America Vol 71: 423431.
33. Gries G. , Schaefer P.W. , Gries R. , Liška J. , Gotoh T. ( 2001) "Reproductive character displacement in Lymantria monachafrom northern Japan". Journal of Chemical Ecology Vol 27: 11631176.
34. Groot A.T. , Horovitz J. L. , Hamilton J. , Santangelo R.G. , Schal C. , Gould F. ( 2006) "Experimental evidence for interspecific directional selection on moth pheromone communication". Proceeding of the National Academy of Sciences of the United States of America Vol 103: 58585863.
35. Hall J.P.W. , Harvey D. J. . ( 2002) "A survey of the androconial organs in the Riodinidae (Lepidoptera)". Zoological Journal of the Linnean Society Vol 136: 171197.
36. Holdridge L.R. ( 1967) Life zone ecology . Tropical Science Center, San Jose, CA, 206pp.
37. Janzen D.H. , Hallwachs W. ( 2010) " Dynamic database for an inventory of the macrocaterpillar fauna, and its food plants and parasitoids, of Area de Conservacion Guanacaste (ACG), northwestern Costa Rica ". Available online at: (accessed May 2010).
38. Johnson K. , Salazar J.A. ( 2002) "A new species of ArcasSwainson from Colombia (Lycaenidae)". Boletín Científico. Museo de Historia Natural. Universidad de Caldas Vol 6: 147152.
39. Löfstedt C. , Herrebout W.M. , Menken S.B.J. ( 1991) "Sex pheromones and their potential role in the evolution of reproductive isolation in small ermine moths (Yponomeutidae)". Chemoecology Vol 2: 2028.
40. Longstaff G.B. ( 1908) "Bionomic notes on butterflies". Transactions of the Entomological Society of London Vol 1908: 607673.
41. Longstaff, G.B. (1912) Butterfly-hunting in many lands. Notes of a field naturalist.Longmans, Green, London, xx + 729 pp., 16 pls., 19 figs.
42. Lorch P.D. , Eadie J.McA. ( 1999) "The power of the concentrated-changes test for correlated evolution". Systematic Biology Vol 48: 170191.
43. Lundgren L. , Bergström G. ( 1975) "Wing scents and scent-released phases in the courtship behavior of Lycaeides argyrognomon(Lepidoptera: Lycaenidae)". Journal of Chemical Ecology Vol 1: 399412.
44. Maddison W. P. ( 1990) "A method for testing the correlated evolution of two binary characters: are gains or losses concentrated on certain branches of a phylogenetic tree?" Evolution Vol 44: 539557.
45. Maddison, W. P. & D.R. Maddison. (2011) Mesquite: a modular system for evolutionary analysis, Version 2.75. Available onlnine at:
46. McElfresh J.S. , Millar J.G. ( 2001) "Geographic variation in the pheromone system of the saturniid moth Hemileuca eglanterina ". Ecology Vol 82: 35053518.
47. Mielke O.H.H. , Casagrande M.M. ,( 2004) "Borboletas", In: Mikich S.B. , Bérnils R.S. (Eds) Livro vermelho da fauna ameaçada no Estado do Paraná . Instituto Ambiental do Paraná, Curitiba, pp. 713739.
48. Müller F. ( 1878) "Pflanzengattungen, an denen mir bekannte Tagfalter-Raupen leben". Stettiner Entomologische Zeitung Vol 39: 296.
49. Nicolay S.S. ( 1971) "A review of the genus Arcaswith descriptions of new species (Lycaenidae, Strymonini)". Journal of the Lepidopterists’ Society Vol 25: 87108.
50. Nixon K.C. ( 2002) WinClada version 1.00.08 . Published by the author, Ithaca, NY.
51. Otero L.S. , Brown K.S. Jr. , Mielke O.H.H. , Monteiro R.F. , Costa J.M. , Macedo M.V. , Maciel N.C. , Becker J. , Salgado N.G. , Santos S.B. , Moya G.E. , Almeida J.M. , Duarte M. ,( 2000) "Invertebrados terrestres". In: Bergallo H.G. , Rocha C.F.D. , Alves M.A.S. , Vansluys M. (Eds) A fauna ameaçada de extinção do estado do Rio de Janeiro. Editora da Universidade do Estado do Rio de Janeiro, Rio de Janeiro, pp. 5362.
52. Phelan P.L. , Baker T.C. ( 1987) "Evolution of male pheromones in moths: reproductive isolation through sexual selection?" Science Vol 235: 205207.
53. Pierce F.N. ( 1908) The genitalia of the group Noctuidae of the Lepidoptera of the British Islands. An account of the morphology of the male clasping organs . A.W. Duncan, Liverpool, 88pp.
54. Powell J. ( 1968) "A study of area occupation and mating behavior in Incisalia iroides(Lepidoptera: Lycaenidae)". Journal of the New York Entomological Society Vol 76: 4757.
55. Quental T.B. ( 2008) "Systematics, sexual selection and evolution of secondary sexual characters in Neotropical Eumaeini butterflies (Lepidoptera: Lycaenidae)". Dissertation, Harvard University, Cambridge, MA, 226pages.
56. Robbins R.K. ( 1980) "The lycaenid “false head” hypothesis: historical review and quantitative analysis". Journal of the Lepidopterists’ Society Vol 34: 194208.
57. Robbins R.K. ( 1991) "Evolution, comparative morphology, and identification of the eumaeine butterfly genus RekoaKaye (Lycaenidae: Theclinae)". Smithsonian Contribution to Zoology Vol 498: 164.
58. Robbins R.K. ,( 2004) "Lycaenidae. Theclinae. Tribe Eumaeini". In: Lamas G. ,(Ed.), Checklist: Part 4A. Hesperioidea — Papilionoidea. In: Heppner J.B. (Ed.) Atlas of Neotropical Lepidoptera . Volume Vol 5A. Association for Tropical Lepidoptera and Scientific Publishers, Gainesville, FL, pp. 118137.
59. Robbins R.K. , Duarte M. ,( 2004) "Descriptions of new butterfly genera. Lycaenidae, Eumaeini". In: Lamas G. ,(Ed.), Checklist: Part 4A. Hesperioidea - Papilionoidea. In: Heppner J.B. (Ed.), Atlas of Neotropical Lepidoptera . Vol Volume 5A. Association for Tropical Lepidoptera and Scientific Publishers, Gainesville, FL, pp. 275282.
60. Robbins R.K. , Duarte M. ( 2005) "Phylogenetic analysis of Cyanophrys Clench, a synopsis of its species, and the potentially threatened C. bertha (Jones) (Lycaenidae: Theclinae: Eumaeini)". Proceedings Entomological Society of Washington Vol 107: 398416.
61. Salazar J.A. ( 2004) " Arcas lecromiSalazar & Constantino, 1995 sinónimo de Arcas splendor Druce, 1907(Lepidoptera: Lycaenidae)". Boletín Científico. Museo de Historia Natural. Universidad de Caldas Vol 8: 354355.
62. Salazar J.A. ( 2008) "Mariposas Colombianas XII. Notes on the territoriality and perching sites of Arcas imperialis(Cramer) In Colombia (Lepidoptera: Lycaenidae). Boletín Científico. Museo de Historia Natural ". Universidad de Caldas Vol 13: 8391.
63. Salazar J. A. , Constantino L.M. ( 1995a) "Sobre algunas especies colombianas del género ArcasSwainson, 1832 y descripción de una nueva (Lepidoptera: Lycaenidae)". Shilap Vol 23: 123128.
64. Salazar J. A. , Constantino L.M. ( 1995b) "Descripción de un nuevo género y dos especies nuevas de lepidópteros de la Cordillera Central de Colombia (Lepidoptera: Lycaenidae)". Shilap Vol 23: 457464.
65. Scott J.A. , 1970) "Hilltopping as a mating mechanism to aid the survival of low density species". Journal of Research on the Lepidoptera Vol 7: 191204.
66. Scott J.A. ( 1974) "Population biology and adult behavior of Lycaena arota(Lycaenidae)". Journal of the Lepidopterists’ Society Vol 28: 6472.
67. Shields O. ( 1967) "Hilltopping, an ecological study of summit congregation behavior of butterflies on a southern California hill". Journal of Research on the Lepidoptera Vol 6: 69178.
68. Snodgrass R.E. ( 1935) Principles of insect morphology. McGraw-Hill, New York, NY, 667 pp.
69. Sokal R.R. , Rohlf F.J. ( 1968) Biometry. W.H. Freeman, San Francisco, CA, 776 pp.
70. Stempffer H. ( 1967) "The genera of the African Lycaenidae (Lepidoptera: Rhopalocera)". Bulletin of the British Museum (Natural History) Entomology , Supplement 10, 322pp.
71. Swinton A.H. ( 1908) "The family tree of moths and butterflies traced in their organs of sense". Societas Entomolica Vol 23: 99101, 114–116, 124–126, 131–132, 140–141, 156–158,162–165.
72. Symonds M.R.E. , Elgar M.A. ( 2004) "Species overlap, speciation and the evolution of aggregation pheromones in bark beetles". Ecological Letters Vol 7: 202212.
73. Symonds M.R.E. , Elgar M.A. ( 2008) "The evolution of pheromone diversity". Trends in Ecology & Evolution Vol 23: 220228.
74. Stobbe R. ( 1912) "Die abdominalen Duftorgane der mannlichen Sphingiden und Noctuiden". Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere Vol 32: 493532.
75. Thomas M.B. ( 1893) "The androconia of Lepidoptera". The American Naturalist Vol 27: 10181021.
76. Valencia C.A. , Gil Z.N. , Constantino L.M. ( 2005) Mariposas diurnas de la zona central cafetera colombiana . Guía de campo. Chinchiná, Cenicafé, 244 pp.
77. Weeks A. G. ( 1905) Illustrations of diurnal Lepidoptera with descriptions. The University Press, Boston, MA, [1]: [1]+ xii + 117 pp.
78. Willmott K.R. , Freitas A.V.L. ( 2006) "Higher-level phylogeny of the Ithomiinae (Lepidoptera: Nymphalidae): classification, patterns of larval hostplant colonisation and diversification". Cladistics Vol 22: 297368.
79. Wilson E.O. , Brown W.L. Jr ( 1953) "The subspecies concept". Systematic Zoology Vol 2: 97111.
80. Zikán J.F. ( 1956) "Beiträge zur Biologie von 12 Theclinen-Arten". Dusenia (Curitiba) Vol 7: 139148.

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