DNA barcoding applied to ex situ tropical amphibian conservation programme reveals cryptic diversity in captive populations

Molecular Ecology Resources

Volumn 13, Issue 6, 2013, Pages 1005-1018

  Crawford, Andrew J ^a,b,c   Cruz, Catalina ^c   Griffith, Edgardo ^d   Ross, Heidi ^d   Ibáñez, Roberto ^a,b   Lips, Karen R ^a,e   Driskell, Amy C ^f   Bermingham, Eldredge ^a   Crump, Paul ^b  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^b Círculo Herpetológico de Panamá ^*  (United States)

^c UNIVERSIDAD DE LOS ANDES   (Colombia)

^d El Valle Amphibian Conservation Center   (Panama)

^e Bldg 142   (United States)

^f SMITHSONIAN INSTITUTION   (United States)

Author keywords

Amphibian decline; Cryptic species diversity; DNA barcode of life; ex situ conservation; Species delimitation

Indexed keywords

AMPHIBIA; VERTEBRATA;

MITOCHONDRIAL DNA;

AMPHIBIA; AMPHIBIAN DECLINE; ANIMAL; ARTICLE; CHEMISTRY; CLASSIFICATION; CRYPTIC SPECIES DIVERSITY; DNA BARCODE OF LIFE; DNA BARCODING; ENDANGERED SPECIES; ENVIRONMENTAL PROTECTION; EX SITU CONSERVATION; GENETIC VARIABILITY; GENETICS; PANAMA; PHYLOGENY; SPECIES DELIMITATION; SPECIES DIFFERENCE; STATISTICAL MODEL;

AMPHIBIAN DECLINE; CRYPTIC SPECIES DIVERSITY; DNA BARCODE OF LIFE; EX SITU CONSERVATION; SPECIES DELIMITATION;

AMPHIBIANS; ANIMALS; CONSERVATION OF NATURAL RESOURCES; DNA BARCODING, TAXONOMIC; DNA, MITOCHONDRIAL; ENDANGERED SPECIES; GENETIC VARIATION; LIKELIHOOD FUNCTIONS; PANAMA; PHYLOGENY; SPECIES SPECIFICITY;

EID: 84873999670     PISSN: 1755098X     EISSN: 17550998     Source Type: Journal    
DOI: 10.1111/1755-0998.12054     Document Type: Article

References (119)

1. Allendorf FW, Luikart G (2007) Conservation and the Genetics of Populations. Blackwell, Malden, MA.
2. Angulo A, Icochea J (2010) Cryptic species complexes, widespread species and conservation: lessons from Amazonian frogs of the Leptodactylus marmoratus group (Anura: Leptodactylidae). Systematics and Biodiversity, 8, 357-370.
3. Angulo A, Reichle S (2008) Acoustic signals, species diagnosis, and species concepts: the case of a new cryptic species of Leptodactylus (Amphibia, Anura, Leptodactylidae) from the Chapare region, Bolivia. Zoological Journal of the Linnean Society, 152, 59-77.
4. April J, Mayden RL, Hanner RH, Bernatchez L (2011) Genetic calibration of species diversity among North America's freshwater fishes. Proceedings of the National Academy of Sciences of the United States of America, 108, 10602-10607.
5. Avise JC (2004) Molecular Markers, Natural History, and Evolution, 2nd edn. Sinauer Associates, Inc., Sunderland, Massachusetts.
6. Bergmann T, Hadrys H, Breves G, Schierwater B (2009) Character-based DNA barcoding: a superior tool for species classification. Berliner und Münchener Tierärztliche Wochenschrift, 122, 446-450.
7. Berven KA (1982) The genetic basis of altitudinal variation in the wood frog Rana sylvatica. I. An experimental analysis of life history traits. Evolution, 36, 962-983.
8. Bickford D, Lohman DJ, Sodhi NS et al. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22, 148-155.
9. Borisenko AV, Sones JE, Hebert PDN (2009) The front-end logistics of DNA barcoding: challenges and prospects. Molecular Ecology Resources, 9, 27-34.
10. Boulenger GA (1896) Descriptions of new reptiles and batrachians from Colombia. Annals and Magazine of Natural History Series, 6, 16-21.
11. Boulenger GA (1898) An account of the reptiles and batrachians collected by Mr. W. F. H. Rosenberg in Western Ecuador. Proceedings of the Zoological Society of London, 1898, 107-126.
12. Brower AVZ (2006) Problems with DNA barcodes for species delimitation: 'Ten species' of Astraptes fulgerator reassessed (Lepidoptera: Hesperiidae). Systematics and Biodiversity, 4, 127-132.
13. Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociological Methods and Research, 33, 261-304.
14. Campbell JA, Savage JM (2000) Taxonomic reconsideration of middle American frogs of the Eleutherodactylus rugulosus group (Anura: Leptodactylidae): a reconnaissance of subtle nuances among frogs. Herpetological Monographs, 14, 186-292.
15. Charlesworth B (1998) Measures of divergence between populations and the effect of forces that reduce variability. Molecular Biology and Evolution, 15, 538-543.
16. Collins R, Boykin L, Cruickshank R, Armstrong K (2011) Barcoding's next top model: an evaluation of nucleotide substitution models for specimen identification. Methods in Ecology and Evolution, 3, 457-465.
17. Cope ED (1864) Contributions to the herpetology of tropical America. Proceedings of the Academy of Natural Sciences of Philadelphia, 16, 166-181.
18. Cope ED (1886) Thirteenth contribution to the herpetology of tropical America. Proceedings of the American Philosophical Society, 23, 271-287.
19. Crawford AJ, Smith EN (2005) Cenozoic biogeography and evolution in direct-developing frogs of Central America (Leptodactylidae: Eleutherodactylus) as inferred from a phylogenetic analysis of nuclear and mitochondrial genes. Molecular Phylogenetics and Evolution, 35, 536-555.
20. Crawford AJ, Bermingham E, Polanía C (2007) The role of tropical dry forest as a long-term barrier to dispersal: a comparative phylogeographical analysis of dry forest tolerant and intolerant frogs. Molecular Ecology, 16, 4789-4807.
21. Crawford AJ, Lips KR, Bermingham E (2010a) Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proceedings of the National Academy of Sciences of the United States of America, 107, 13777-13782.
22. Crawford AJ, Ryan MJ, Jaramillo CA (2010b) A new species of Pristimantis (Anura: Strabomantidae) from the Pacific coast of the Darien Province, Panama, with a molecular analysis of its phylogenetic position. Herpetologica, 66, 192-206.
23. Daugherty CH, Cree A, Hay JM, Thompson MB (1990) Neglected taxonomy and continuing extinctions of tuatara (Sphenodon). Nature, 347, 177-179.
24. Dayrat B (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society, 85, 407-415.
25. De Queiroz K (2007) Species concepts and species delineation. Systematic Biology, 56, 879-886.
26. Dubois A (2003) The relationships between taxonomy and conservation biology in the century of extinctions. Comptes Rendus Biologies, 326, 9-21.
27. Dunn ER (1933) Amphibians and reptiles from El Valle de Anton, Panama. Occasional Papers of the Boston Society of Natural History, 8, 65-79.
28. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution, 17, 368-376.
29. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783-791.
30. Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) Version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle.
31. Felsenstein J, Churchill GA (1996) A Hidden Markov Model approach to variation among sites in rate of evolution. Molecular Biology and Evolution, 13, 93-104.
32. Floyd R, Abebe E, Papert A, Blaxter M (2002) Molecular barcodes for soil nematode identification. Molecular Ecology, 11, 839-850.
33. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294-299.
34. Fouquet A, Gilles A, Vences M et al. (2007) Underestimation of species richness in Neotropical frogs revealed by mtDNA analyses. PLoS ONE, 2, e1109.
35. Fujita MK, Leaché AD, Burbrink FT, McGuire JA, Moritz C (2012) Coalescent-based species delimitation in an integrative taxonomy. Trends in Ecology & Evolution, 27, 480-488.
36. Funk WC, Caminer M, Ron SR (2011) High levels of cryptic species diversity uncovered in Amazonian frogs. Proceedings of the Royal Society B: Biological Sciences, 279, 1806-1814.
37. Gagliardo R, Crump P, Griffith E et al. (2008) The principles of rapid response for amphibian conservation, using the programmes in Panama as an example. International Zoo Yearbook, 42, 125-135.
38. Glaw F, Köhler J (1998) Amphibian species diversity exceeds that of mammals. Herpetological Review, 29, 11-12.
39. Goldstein PZ, DeSalle R (2011) Integrating DNA barcode data and taxonomic practice: determination, discovery, and description. BioEssays, 33, 135-147.
40. Hailer F, Kutschera VE, Hallström BM et al. (2012) Nuclear genomic sequences reveal that polar bears are an old and distinct bear lineage. Science, 336, 344-347.
41. Hanken J (1999) Why are there so many new amphibian species when amphibians are declining? Trends in Ecology & Evolution, 14, 7-8.
42. Hasegawa M, Kishino H, Yano T-A (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22, 160-174.
43. Hebert PDN, Ratnasingham S, de Waard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270, S96-S99.
44. Hof C, Araújo MB, Jetz W, Rahbek C (2011) Additive threats from pathogens, climate and land-use change for global amphibian diversity. Nature, 480, 516-519.
45. Hoffmann M, Hilton-Taylor C, Angulo A et al. (2010) The impact of conservation on the status of the World's vertebrates. Science, 330, 1503-1509.
46. Howard JG, Raphael BL, Brown JL et al. (1989) Male sterility associated with karyotypic hybridization in Kirk's dik-dik (Madoqua kirkii). Proceedings American Association of Zoo Veterinarians Annual Meeting, pp. 58-60.
47. Hudson RR (1990) Gene genealogies and the coalescent process. In: Oxford Surveys in Evolutionary Biology (eds. Futuyma D, Antonovics J), vol. 7, pp. 1-44. Oxford University Press, New York.
48. Ibáñez R, Jaramillo CA, Arosemena F (1994) A new species of Eleutherodactylus (Anura: Leptodactylidae) from Panamá. Amphibia-Reptilia, 15, 337-341.
49. Ibáñez R, Jaramillo CA, Solís FA (1995) Una especies nueva de Atelopus (Amphibia: Bufonidae) de Panamá. Caribbean Journal of Science, 31, 57-64.
50. Jansen M, Bloch R, Schulze A, Pfenninger M (2011) Integrative inventory of Bolivia's lowland anurans reveals hidden diversity. Zoologica Scripta, 40, 567-583.
51. Jiménez de la Espada M (1872) Nuevos batrácios Americanos. Anales de la Sociedad Española de Historia Natural. Madrid, 1, 84-88.
52. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Mammalian Protein Metabolism (ed. Munro HN), pp. 21-132. Academic Press, New York.
53. Kessing B, Croom H, Martin A et al. (2004) The Simple Fool's Guide to PCR, version 1.0. In: Special Publication, Dept. of Zoology, University of Hawaii, Honolulu, USA.
54. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111-120.
55. Kocher TD, Thomas WK, Meyer A et al. (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences of the United States of America, 86, 6196-6200.
56. Köhler J, Vieites DR, Bonett RM et al. (2005) New amphibians and global conservation: A boost in species discoveries in a highly endangered vertebrate group. BioScience, 55, 693-696.
57. Lind MI, Ingvarsson PK, Johansson H, Hall D, Johansson F (2011) Gene flow and selection on phenotypic plasticity in an island system of Rana temporaria. Evolution, 65, 684-697.
58. Lips KR (1999) Mass mortality and population declines of anurans at an upland site in western Panama. Conservation Biology, 13, 117-125.
59. Lips KR, Brem F, Brenes R et al. (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences of the United States of America, 103, 3165-3170.
60. Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia, 91, 219-227.
61. Mace GM (2004) The role of taxonomy in species conservation. Philosophical Transactions of the Royal Society B: Biological Sciences, 359, 711-719.
62. Maddison DR, Maddison WP (2005) MacClade 4. Sinauer Associates, Inc., Sunderland, Massachusetts.
63. May RM (1990) Taxonomy as destiny. Nature, 347, 129-130.
64. Meegaskumbura M, Bossuyt F, Pethiyagoda R et al. (2002) Sri Lanka: an amphibian hot spot. Science, 298, 379.
65. Mendelson JR, III, Lips KR, Gagliardo RW et al. (2006) Confronting amphibian declines and extinctions. Science, 313, 48.
66. Mendelson JR, Savage JM, Griffith E et al. (2008) Spectacular new gliding species of Ecnomiohyla (Anura: Hylidae) from Central Panama. Journal of Herpetology, 42, 750-759.
67. Mendoza ÁM, García-Ramirez JC, Cárdenas-Henao H (2012) Epithelial mucosa as an alternative tissue for DNA extraction in amphibians. Conservation Genetics Resources, 4, 1097-1099.
68. Meyer CP, Geller JB, Paulay G (2005) Fine scale endemism on coral reefs: Archipelagic differentiation in turbinid gastropods. Evolution, 59, 113-125.
69. Miyamoto MM (1983) Frogs of the Eleutherodactylus rugulosus group: a cladistic study of allozymes, morphological, and karyological data. Systematic Zoology, 32, 109-124.
70. Miyamoto MM (1984) Central American frogs allied to Eleutherodactylus cruentus: allozyme and morphological data. Journal of Herpetology, 18, 256-263.
71. Moritz C (1994) Applications of mitochondrial DNA analysis in conservation: a critical review. Molecular Ecology, 3, 401-411.
72. Nabholz B, Mauffrey J-F, Bazin E, Galtier N, Glemin S (2008) Determination of mitochondrial genetic diversity in mammals. Genetics, 178, 351-361.
73. Padial JM, de la Riva I (2007) Integrative taxonomists should use and produce DNA barcodes. Zootaxa, 1586, 67-68.
74. Padial JM, Castroviejo-Fisher S, Köhler J et al. (2009) Deciphering the products of evolution at the species level: the need for an integrative taxonomy. Zoologica Scripta, 38, 431-447.
75. Padial J, Miralles A, de la Riva I, Vences M (2010) The integrative future of taxonomy. Frontiers in Zoology, 7, 16.
76. Paz A, Crawford AJ (2012) Molecular-based rapid inventories of sympatric diversity: a comparison of DNA barcode clustering methods applied to geography-based vs. clade-based sampling of amphibians. Journal of Biosciences, 37, 887-896.
77. Peters WCH (1862) Über die batrachier-gattung Hemiphractus. Monatsberichte der Königlichen Preussische Akademie des Wissenschaften zu Berlin, 1862, 144-152.
78. Peters WCH (1863) Fernere mittheilungen über neue batrachier. Monatsberichte der Königlichen Preussische Akademie des Wissenschaften zu Berlin, 1863, 445-470.
79. Peters WCH (1873) Über eine neue schildrötenart, Cinosternon Effeldtii und einige andere neue oder weniger bekannte amphibien. Monatsberichte der Königlichen Preussische Akademie des Wissenschaften zu Berlin, 1873, 603-618.
80. Phillimore AB, Hadfield JD, Jones OR, Smithers RJ (2010) Differences in spawning date between populations of common frog reveal local adaptation. Proceedings of the National Academy of Sciences of the United States of America, 107, 8292-8297.
81. Piganeau G, Eyre-Walker A (2009) Evidence for variation in the effective population size of animal mitochondrial DNA. PLoS ONE, 4, e4396.
82. Posada D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253-1256.
83. Prunier J, Kaufmann B, Grolet O et al. (2012) Skin swabbing as a new efficient DNA sampling technique in amphibians, and 14 new microsatellite markers in the alpine newt (Ichthyosaura alpestris). Molecular Ecology Resources, 12, 524-531.
84. Puillandre N, Lambert A, Brouillet S, Achaz G (2011) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21, 1864-1877.
85. Ratnasingham S, Hebert PDN (2007) BoLD: the barcode of life data system. Molecular Ecology Notes, 7, 355-364. Available from http://www.barcodinglife.org.
86. Rissler LJ, Apodaca JJ (2007) Adding more ecology into species delimitation: ecological niche models and phylogeography help define cryptic species in the Black Salamander (Aneides flavipunctatus). Systematic Biology, 56, 924-942.
87. Rocha L, Craig M, Bowen B (2007) Phylogeography and the conservation of coral reef fishes. Coral Reefs, 26, 501-512.
88. Ryan MJ, Savage JM, Lips KR, Giermakowski JT (2010) A new species of the Craugastor rugulosus series (Anura: Craugastoridae) from West-Central Panama. Copeia, 2010, 405-409.
89. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406-425.
90. Samadi S, Barberousse A (2006) The tree, the network, and the species. Biological Journal of the Linnean Society, 89, 509-521.
91. Sarkar IN, Planet PJ, DeSalle R (2008) CAOS software for use in character-based DNA barcoding. Molecular Ecology Resources, 8, 1256-1259.
92. Savage JM (1981) The systematic status of Central American frogs confused with Eleutherodactylus cruentus. Proceedings of the Biological Society of Washington, 94, 413-420.
93. Savage JM, Hollingsworth BD, Lips KR, Jaslow AP (2004) A new species of rainfrog (genus Eleutherodactylus) from the Serranía de Tabasará, west-central Panama and reanalysis of the fitzingeri species group. Herpetologica, 60, 519-529.
94. Sites JW, Marshall JC (2003) Delimiting species: a Renaissance issue in systematic biology. Trends in Ecology & Evolution, 18, 462-470.
95. Slatkin M (1991) Inbreeding coefficients and coalescence times. Genetical Research, 58, 167-175.
96. Srivathsan A, Meier R (2012) On the inappropriate use of Kimura-2-parameter (K2P) divergences in the DNA-barcoding literature. Cladistics, 28, 190-194.
97. Stuart SN, Chanson JS, Cox NA et al. (2004) Status and trends of amphibian declines and extinctions worldwide. Science, 306, 1783-1786.
98. Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Molecular Biology and Evolution, 9, 678-687.
99. Tamura K, Peterson D, Peterson N et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731-2739.
100. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876-4882.
101. Turmelle AS, Kunz TH, Sorenson MD (2011) A tale of two genomes: contrasting patterns of phylogeographic structure in a widely distributed bat. Molecular Ecology, 20, 357-375.
102. Vences M, Thomas M, Bonett RM, Vieites DR (2005a) Deciphering amphibian diversity through DNA barcoding: Chances and challenges. Philosophical Transactions of the Royal Society B: Biological Sciences, 360, 1859-1868.
103. Vences M, Thomas M, Van der Meijden A, Chiari Y, Vieites DR (2005b) Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Frontiers in Zoology, 2, 5.
104. Vieites DR, Wollenberg KC, Andreone F et al. (2009) Vast underestimation of Madagascar's biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences of the United States of America, 106, 8267-8272.
105. Voyles J, Young S, Berger L et al. (2009) Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science, 326, 582-585.
106. Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the National Academy of Sciences of the United States of America, 105, 11466-11473.
107. Wang IJ, Crawford AJ, Bermingham E (2008) Phylogeography of the Pygmy Rain Frog (Pristimantis ridens) across the lowland wet forests of isthmian Central America. Molecular Phylogenetics and Evolution, 47, 992-1004.
108. Weigt LA, Crawford AJ, Rand AS, Ryan MJ (2005) Biogeography of the túngara frog, Physalaemus pustulosus: a molecular perspective. Molecular Ecology, 14, 3857-3876.
109. Werle E, Schneider C, Renner M, Volker M, Fiehn W (1994) Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Research, 22, 4354-4355.
110. Wiens JJ, Penkrot TA (2002) Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Systematic Biology, 51, 69-91.
111. Will KW, Mishler BD, Wheeler QD (2005) The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology, 54, 844-851.
112. Woodhams D, Kilburn V, Reinert L et al. (2008) Chytridiomycosis and amphibian population declines continue to spread eastward in Panama. EcoHealth, 5, 268-274.
113. Wynn A, Heyer WR (2001) Do geographically widespread species of tropical amphibians exist? An estimate of genetic relatedness within the neotropical frog Leptodactylus fuscus (Schneider 1799) (Anura Leptodactylidae). Tropical Zoology, 14, 255-285.
114. Xia YUN, Gu H-F, Peng RUI et al. (2012) COI is better than 16S rRNA for DNA barcoding Asiatic salamanders (Amphibia: Caudata: Hynobiidae). Molecular Ecology Resources, 12, 48-56.
115. Yang Z (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. Journal of Molecular Evolution, 39, 306-324.
116. Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Molecular Ecology, 17, 2107-2121.
117. Zippel KC, Ibáñez R, Lindquist ED et al. (2006) Implicaciones en la conservación de las ranas doradas de Panamá, asociadas con su revision taxonómica. Herpetotropicos, 3, 29-39.
118. Zippel K, Johnson K, Gagliardo R et al. (2011) The Amphibian Ark: a global community for ex situ conservation of amphibians. Herpetological Conservation and Biology, 6, 340-352.
119. Zwickl DJ (2006) Genetic Algorithm Approaches for the Phylogenetic Analysis of Large Biological Sequence Datasets Under the Maximum Likelihood Criterion. The University of Texas, Austin.