The subspecies concept in butterflies: Has its application in taxonomy and conservation biology outlived its usefulness?

Biological Journal of the Linnean Society

Volumn 106, Issue 4, 2012, Pages 699-716

  Braby, Michael F ^a,b   Eastwood, Rodney ^c   Murray, Neil ^d  

^a MUSEUM AND ART GALLERY OF THE NORTHERN TERRITORY   (Australia)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c HARVARD UNIVERSITY   (United States)

^d LA TROBE UNIVERSITY   (Australia)

Author keywords

Biological species concept; Conservation genetics; Geographical variation; Hybrid population; Introgression; Phylogenetic species concept

Indexed keywords

ADAPTIVE RADIATION; ALLOPATRY; BIODIVERSITY; BUTTERFLY; CONSERVATION GENETICS; DIVERGENCE; GENETIC DRIFT; GENETIC STRUCTURE; GENETIC VARIATION; GEOGRAPHICAL VARIATION; HYBRID; INTROGRESSION; MORPHOLOGY; NATURAL SELECTION; SPECIES CONCEPT; SUBSPECIES; TAXONOMY;

ANIMALIA; INVERTEBRATA; PAPILIONOIDEA;

EID: 84863735191     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2012.01909.x     Document Type: Review

References (123)

1. Abbott RJ, Ritchie MG, Hollingsworth PM. 2008. Introduction. Speciation in plants and animals: patterns and process. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 363: 2965-2969.
2. Amadon D. 1949. The seventy-five percent rule for subspecies. The Condor 51: 250-258.
3. Avise JC. 1989. A role for molecular genetics in the recognition and conservation of endangered species. Trends in Ecology and Evolution 4: 279-281.
4. Avise JC. 2000. Phylogeography. The history and formation of species. Cambridge, MA: Harvard University Press.
5. Avise JC, Ball RM. 1990. Principles of genealogical concordance in species concepts and biological taxonomy. Oxford Surveys in Evolutionary Biology 7: 45-67.
6. Balakrishnan R. 2005. Species concepts, species boundaries and species identification: a view from the tropics. Systematic Biology 54: 689-693.
7. Barton NH, Hewitt GM. 1985. Analysis of hybrid zones. Annual Review of Ecology and Systematics 16: 113-148.
8. Baum DA. 1992. Phylogenetic species concepts. Trends in Ecology and Evolution 7: 1-2.
9. Baum DA, Donohue MJ. 1995. Choosing among alternative 'phylogenetic' species concepts. Systematic Botany 20: 560-573.
10. Braby MF. 1993. Early stages, biology and taxonomic status of Tisiphone helena (Olliff) (Lepidoptera: Nymphalidae: Satyrinae). Journal of the Australian Entomological Society 32: 273-282.
11. Braby MF. 2000. Butterflies of Australia. Their identification, biology and distribution. Melbourne: CSIRO Publishing.
12. Braby MF. 2004. The complete field guide to butterflies of Australia. Melbourne: CSIRO Publishing.
13. Braby MF. 2008. Taxonomic review of Candalides absimilis (C. Felder, 1862) and C. margarita (Semper, 1879) (Lepidoptera: Lycaenidae), with descriptions of two new subspecies. The Beagle, records of the Museums and Art Galleries of the Northern Territory 24: 33-54.
14. Braby MF. 2010. The merging of taxonomy and conservation biology: a synthesis of Australian butterfly systematics (Lepidoptera: Hesperioidea and Papilionoidea) for the 21st century. Zootaxa 2707: 1-76.
15. Brooks TM, Helgen KM. 2010. A standard for species. Nature 467: 540-541.
16. Brower AVZ. 2006. Problems with DNA barcodes for species delimitation: 'ten species' of Astraptes fulgerator reassessed (Lepidoptera: Hesperiidae). Systematics and Biodiversity 4: 127-132.
17. Burbrink FT, Lawson R, Slowinski JB. 2000. Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): a critique of the subspecies concept. Evolution 54: 2107-2118.
18. Carstens BC, Knowles LL. 2007. Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: an example from Melanoplus grasshoppers. Systematic Biology 56: 400-411.
19. CITES. 2012. Convention on international trade in endangered species of wild flora and fauna. Available at:.
20. Collins MM. 1996. Charles Remington's contributions of the species concept. Journal of the Lepidopterists' Society 50: 268-270.
21. Common IFB, Waterhouse DF. 1981. Butterflies of Australia. Sydney: Angus and Robertson.
22. Conroy BA. 1971. Geographic variation and speciation in the sword grass brown butterfly, Tisiphone abeona Donovan. PhD Thesis, The University of Sydney.
23. Coyne JA, Orr HA. 2004. Speciation. Sunderland, MA: Sinauer Associates.
24. Cracraft J. 1983. Species concepts and speciation analysis. Current Ornithology 1: 159-187.
25. Cracraft J. 1989. Speciation and its ontology: the emperical consequences of alternative species concepts for understanding patterns and processes of differentiation. In: Otte D, Endler JA, eds. Speciation and its consequences. Sunderland, MA: Sinauer Associates, 28-59.
26. Cracraft J. 1997. Species concepts in systematics and conservation biology - an ornithological viewpoint. In: Claridge MF, Dawah HA, Wilson MR, eds. Species: the units of biodiversity. London: Chapman and Hall, 325-339.
27. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK. 2000. Considering evolutionary processes in conservation biology. Trends in Ecology and Evolution 15: 290-295.
28. Cranston PS. 2010. Insect biodiversity and conservation in Australasia. Annual Review of Entomology 55: 55-75.
29. Crozier RH. 1997. Preserving the information content of species: genetic diversity, phylogeny, and conservation value. Annual Review of Ecology and Systematics 28: 243-268.
30. Crusz H. 1986. The dilemma of subspecies. Trends in Ecology and Evolution 1: 104.
31. Darwin C. 1859. On the origin of species by means of natural selection. London: John Murray.
32. Davis JI. 1996. Phylogenetics, molecular variation, and species concepts. BioScience 46: 502-511.
33. Degner JF, Stout IJ, Roth JD, Parkinson CL. 2007. Population genetics and conservation of the threatened southeastern beach mouse (Peromyscus polionotus niveiventris): subspecies and evolutionary units. Conservation Genetics 8: 1441-1452.
34. Descimon H, Mallet J. 2009. Bad species. In: Settele J, Konvička M, Shreeve TG, Van Dyck H, eds. Ecology of butterflies in Europe. Cambridge: Cambridge University Press, 219-249.
35. Dunn KL, Kitching RL, Dexter EM. 1994. The conservation status of Australian butterflies. Canberra: Unpublished report to Australian National Parks and Wildlife Service. 381.
36. Eastwood RG. 2006. Ant association and speciation in Lycaenidae (Lepidoptera): consequences of novel adaptations and Pleistocene climate changes. PhD Thesis, Griffith University.
37. Eastwood RG, Braby MF, Schmidt DJ, Hughes JM. 2008. Taxonomy, ecology, genetics and conservation status of the pale imperial hairstreak (Jalmenus eubulus) (Lepidoptera: Lycaenidae): a threatened butterfly from the Brigalow Belt, Australia. Invertebrate Systematics 22: 407-423.
38. Eastwood RG, Hughes JM. 2003. Phylogeography of the rare myrmecophagous butterfly Acrodipsas cuprea (Lepidoptera: Lycaenidae) from pinned museum specimens. Australian Journal of Zoology 51: 331-340.
39. Eastwood RG, Pierce NE, Kitching RL, Hughes JM. 2006. Do ants enhance diversification in lycaenid butterflies? Phylogenetic evidence from a model myrmecophile, Jalmenus evagoras. Evolution 60: 315-327.
40. Edwards ED, Newland J, Regan L. 2001. Lepidoptera: hesperioidea, papilionoidea. Zoological catalogue of Australia, Vol. 31.6. Melbourne: CSIRO Publishing.
41. Endler JA. 1977. Geographic variation, speciation, and clines. Princeton, NJ: Princeton University Press.
42. Frankel OH. 1970. Genetic conservation in perspective. In: Frankel OH, Bennett E, eds. Genetic resources in plants - their exploration and conservation. Oxford: Blackwell Scientific Publications, 469-489.
43. Frankel OH, Soulé ME. 1981. Conservation and evolution. Cambridge: Cambridge University Press.
44. Frankham R. 2010. Challenges and opportunities of genetic approaches to biological conservation. Biological Conservation 143: 1919-1927.
45. Fraser DJ, Bernatchez L. 2001. Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology 10: 2741-2752.
46. Frost DR, Kluge AG, Hillis DM. 1992. Species in contemporary herpetology: comments on phylogenetic inference and taxonomy. Herpetological Review 23: 46-54.
47. Funk DJ, Omland KE. 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution and Systematics 34: 397-423.
48. Gillham NW. 1956. Geographic variation and the subspecies concept in butterflies. Systematic Zoology 5: 110-120.
49. Gippoliti S, Amori G. 2007. The problem of subspecies and biased taxonomy in conservation lists: the case of mammals. Folia Zoologica 56: 113-117.
50. Goldstein PZ, DeSalle R, Amato G, Vogler AP. 2000. Conservation genetics at the species boundary. Conservation Biology 14: 120-131.
51. Gompert Z, Nice CC, Fordyce JA, Forister ML, Shapiro AM. 2006. Identifying units for conservation using molecular systematics: the cautionary tale of the Karner blue butterfly. Molecular Ecology 15: 1759-1768.
52. Groves C. 2004. The what, why and how of primate taxonomy. International Journal of Primatology 25: 1105-1126.
53. Haig SM, Beever EA, Chambers SM, Draheim HM, Dugger BD, Dunham S, Elliott-Smith E, Fontaine JB, Kesler DC, Knaus BJ, Lopes LF, Loschl P, Mullins TD, Sheffield LM. 2006. Taxonomic considerations in listing subspecies under the U.S. Endangered Species Act. Conservation Biology 20: 1584-1594.
54. Hamilton CW, Reichard SH. 1992. Current practice in the use of subspecies, variety, and forma in the classification of wild plants. Taxon 41: 485-498.
55. Hebert PDN, Cywinska A, Ball SL, Dewaard JR. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Series B, Biological Sciences 270: 313-321.
56. Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W. 2004. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Acadamy of Sciences of the United States of America 101: 14812-14817.
57. Hennig W. 1966. Phylogenetic systematics. Urbana, IL: University of Illinois Press.
58. Hewitt GM. 1988. Hybrid zones - natural laboratories for evolutionary studies. Trends in Ecology and Evolution 3: 158-167.
59. Hey J. 2001. The mind of the species problem. Trends in Ecology and Evolution 16: 326-329.
60. Hey J. 2006. On the failure of modern species concepts. Trends in Ecology and Evolution 21: 447-450.
61. ICZN. 1999. International code of zoological nomenclature. London: International Trust for Zoological Nomenclature.
62. Isaac NJB, Mallet J, Mace GM. 2004. Taxonomic inflation: its influence on macroecolgy and conservation. Trends in Ecology and Evolution 19: 464-469.
63. IUCN Standards and Petitions Subcommittee. 2010. Guidelines for using the IUCN red list categories and criteria, Version 8.1. Gland: IUCN Species Survival Commission.
64. James FC. 2010. Avian subspecies. Ornithological Monographs 67: 1-5.
65. Joyce DA, Dennis RLH, Bryant SR, Shreeve TG, Ready JS, Pullin AS. 2009. Do taxonomic divisions reflect genetic differentiation? A comparison of morphological and genetic data in Coenonympha tullia (Müller), Satyrinae. Biological Journal of the Linnean Society 97: 314-327.
66. Kizirian D, Donnelly MA. 2004. The criterion of reciprocal monophyly and classification of nested diversity at the species level. Molecular Phylogenetics and Evolution 32: 1072-1076.
67. Kohn MH, Murphy WJ, Ostrander EA, Wayne RK. 2006. Genomics and conservation genetics. Trends in Ecology and Evolution 21: 630-637.
68. Kunte K, Shea C, Aardema ML, Scriber JM, Juenger TE, Gilbert LE, Kronforst MR. 2011. Sex chromosome mosaicism and hybrid speciation among tiger swallowtail butterflies. PLoS Genetics 7: e1002274.
69. Lucas AM. 1969. Clinal variation in pattern and colour in coastal populations of the butterfly Tisiphone abeona (Donovan) (Lepidoptera: Satyrinae). Australian Journal of Zoology 17: 37-48.
70. Mallet J. 1995. A species definition for the modern synthesis. Trends in Ecology and Evolution 10: 294-299.
71. Mallet J. 2001. Subspecies, semispecies, superspecies. In: Levin S, ed. Encyclopedia of biodiversity, Vol. 5. London: Academic Press, 523-526.
72. Mallet J. 2004. Poulton, Wallace and Jordan: how discoveries in Papilio butterflies led to a new species concept 100 years ago. Systematics and Biodiversity 1: 441-452.
73. Mallet J. 2005. Hybridization as an invasion of the genome. Trends in Ecology and Evolution 20: 229-237.
74. Mallet J. 2007. Hybrid speciation. Nature 446: 279-283.
75. Mallet J. 2008. Hybridization, ecological races and the nature of species: emperical evidence for the ease of speciation. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 363: 2971-2986.
76. Margules CR, Sarkar S. 2007. Systematic conservation planning. Cambridge: Cambridge University Press.
77. Mayr E. 1942. Systematics and the origin of species. New York, NY: Columbia University Press.
78. Mayr E. 1963. Animal species and evolution. Cambridge, MA: Harvard University Press.
79. Mayr E. 1982a. The growth of biological thought: diversity, evolution, and inheritance. Cambridge, MA: Harvard University Press.
80. Mayr E. 1982b. Of what use are subspecies? Auk 99: 593-595.
81. McDade LC. 1995. Species concepts and problems in practice: insight from botanical monographs. Systematic Botany 20: 606-622.
82. McQuillan PB, Ek CJ. 1997. A biogeographical analysis of the Tasmanian endemic Ptunarra brown butterfly, Oreixenica ptunarra Couchman, 1953 (Lepidoptera: Nymphalidae: Satyrinae). Australian Journal of Zoology 44: 21-37.
83. Mitter KT, Larsen TB, De Prins W, De Prins J, Collins SC, Vande Weghe G, Sáfián S, Zakharov EV, Hawthorne DJ, Kawahara AY, Regier JC. 2011. The butterfly subfamily Pseudopontiinae is not monobasic: marked genetic diversity and morphology reveal three new species of Pseudopontia (Lepidoptera: Pieridae). Systematic Entomology 36: 139-163.
84. Moritz C. 1994. Defining 'evolutionary significant units' for conservation. Trends in Ecology and Evolution 9: 373-375.
85. Moritz C. 2002. Strategies to protect biological diversity and the evolutionary processes that sustain it. Systematic Biology 51: 238-254.
86. Neigel JE, Avise JC. 1986. Phylogenetic relationships of mitochondrial DNA under various demographic models of speciation. In: Nevo E, Karlin S, eds. Evolutionary processes and theory. New York, NY: Academic Press.
87. New TR. 1984. Insect conservation - an Australian perspective. Dordrecht: Dr W. Junk Publishers.
88. New TR. 1999. The evolution and characteristics of the Australian butterfly fauna. In: Kitching RL, Jones RE, Scheermeyer E, Pierce NE, eds. Biology of Australian butterflies. Monographs of Australian lepidoptera, Vol. 6. Melbourne: CSIRO Publishing, 33-52.
89. New TR, Field RP, Sands DPA. 2007. Victoria's butterflies in a national conservation context. The Victorian Naturalist 124: 243-249.
90. Nixon KC, Wheeler QD. 1990. An amplification of the phylogenetic species concept. Cladistics 6: 211-223.
91. O'Brien SJ, Mayr E. 1991. Bureaucratic mischief: recognising endangered species and subspecies. Science 251: 1187-1188.
92. Paetkau D. 1999. Using genetics to identify intraspecific conservation units: a critque of current methods. Conservation Biology 13: 1507-1509.
93. Pearse FK. 1978. Geographic variation and natural selection in the Common Brown butterfly Heteronympha merope. PhD Thesis, La Trobe University.
94. Pearse FK, Murray ND. 1981. Clinal variation in the Common Brown butterfly Heteronympha merope merope (Lepidoptera: Satyrinae). Australian Journal of Zoology 29: 631-642.
95. Petit RJ, Excoffier L. 2009. Gene flow and species delimitation. Trends in Ecology and Evolution 24: 386-393.
96. de Queiroz K. 1998. The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In: Howard DJ, Berlocher SH, eds. Endless forms: species and speciation. Oxford: Oxford University Press, 57-75.
97. de Queiroz K. 2007. Species concepts and species delimitation. Systematic Biology 56: 879-886.
98. Ryder OA. 1986. Species conservation and systematics: the dilemma of subspecies. Trends in Ecology and Evolution 1: 9-10.
99. Sands DPA. 2009. Stretching the trinomials: what are limits for recognizing a subspecies? News Bulletin of the Entomological Society of Queensland 37: 65-66.
100. Sands DPA, New TR. 2002. The action plan for Australian butterflies. Canberra: Environment Australia.
101. Santos H, Burban C, Rousselet J, Rossi J-P, Branco M, Kerdelhué C. 2011. Incipient allochronic speciation in the pine processionary moth (Thaumetopoea pityocampa, Lepidoptera, Notodontidae). Journal of Evolutionary Biology 24: 146-158.
102. Sarkar S, Pressey RL, Faith DP, Margules CR, Fuller T, Stoms DM, Moffett A, Wilson KA, Williams KJ, Williams PH, Andelman S. 2006. Biodiversity conservation planning tools: present status and challenges for the future. Annual Review of Environment and Resources 31: 123-159.
103. Schmidt DJ, Hughes JM. 2006. Genetic affinities among subspecies of a widespread Australian lycaenid butterfly, Ogyris amaryllis (Hewitson). Australian Journal of Zoology 54: 429-446.
104. Sibatani A, Grund RB. 1978. A revision of the Theclinesthes onycha complex (Lepidoptera: Lycaenidae). Transactions of the Lepidopterological Society of Japan 29: 1-34.
105. Sites JW, Crandall KA. 1997. Testing species boundaries in biodiversity studies. Conservation Biology 11: 1289-1297.
106. Sites JW, Marshall JC. 2003. Delimiting species: a renaissance issue in systematic biology. Trends in Ecology and Evolution 18: 462-470.
107. Sperling FAH. 1993. Mitochondrial DNA variation and Haldane's rule in the Papilio glaucus and P. troilus species groups. Heredity 71: 227-233.
108. Sperling FAH. 2003. Butterfly molecular systematics: from species definitions to higher-level phylogenies. In: Boggs CL, Watt WB, Ehrlich PR, eds. Butterflies: ecology and evolution taking flight. Chicago, IL: University of Chicago Press, 431-458.
109. Stanford CB. 2001. The subspecies concept in primatology: the case of mountain gorillas. Primates 42: 309-318.
110. Tobias JA, Seddon N, Spottiswoode CN, Pilgrim JD, Fishpool LDC, Collar NJ. 2010. Quantitative criteria for species delimitation. Ibis 152: 724-746.
111. Vane-Wright RI. 1996. Systematics and the conservation of biological diversity. Annals of the Missouri Botanical Garden 83: 47-57.
112. Vane-Wright RI. 2003. Indifferent philosophy versus almighty authority: on consistency, consensus and unitary taxonomy. Systematics and Biodiversity 1: 3-11.
113. Vane-Wright RI, Tennent J. 2011. Colour and size in Junonia villida (Lepidoptera, Nymphalidae): subspecies or phenotypic plasticity? Systematics and Biodiversity 9: 289-305.
114. Vogler AP, DeSalle R. 1994. Diagnosing units of conservation managment. Conservation Biology 8: 354-363.
115. Waples RS. 1995. Evolutionary significant units and the conservation of biological diversity under the Endangered Species Act. In: Nielsen J, ed. Evolution and the aquatic ecosystem. Bethesda, MD: American Fisheries Society, 8-27.
116. Waterhouse GA. 1914. A monograph of the genus Tisiphone Hübner. Australian Zoologist 1: 15-19.
117. Waterhouse GA. 1928. A second monograph of the genus Tisiphone Hübner. Australian Zoologist 5: 217-240.
118. Waterhouse GA, Lyell G. 1914. The butterflies of Australia. A monograph of the Australian Rhopalocera. Sydney: Angus and Robertson.
119. Wiens JJ. 2007. Species delimitation: new approaches for discovering diversity. Systematic Biology 56: 875-878.
120. Wilson EO, Brown WL. 1953. The subspecies concept and its taxonomic application. Systematic Zoology 2: 97-111.
121. Wüster W, Bush B, Keogh JS, O'Shea M, Shine R. 2001. Taxonomic contributions in the 'amateur' literature: comments on recent descriptions of new genera and species by Raymond Hoser. Litteratura Serpentium 21: 67-79, 86-91.
122. Yeates DK, Seago A, Nelson L, Cameron SL, Joseph L, Trueman JWH. 2011. Integrative taxonomy, or iterative taxonomy? Systematic Entomology 36: 209-217.
123. Zink RM. 2004. The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proceedings of the Royal Society of London Series B, Biological Sciences 271: 561-564.