A trans-amazonian screening of mtDNA reveals deep intraspecific divergence in forest birds and suggests a vast underestimation of species diversity

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Milá, Borja ^a,b   Tavares, Erika S ^c   Muñoz Saldaña, Alberto ^a   Karubian, Jordan ^d   Smith, Thomas B ^b   Baker, Allan J ^c  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DEPARTMENT OF NATURAL HISTORY   (Canada)

^d Tulane University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

ARTICLE; BIRD; COLOR; ECUADOR; FOREST; FOREST BIRD; FRENCH GUIANA; GENETIC DISTANCE; GENETIC SCREENING; GENETIC VARIABILITY; NONHUMAN; PHYLOGEOGRAPHY; PLUMAGE COLOR; SAMPLING; SPECIES DIVERSITY; TAXONOMY;

ANIMALS; BIRDS; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX IV; FEATHERS; GENETIC VARIATION; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SOUTH AMERICA; TREES;

AVES;

EID: 84863993913     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040541     Document Type: Article

References (102)

1. Vieites DR, Wollenberg KC, Andreone F, Köhler J, Glaw F, et al. (2009) Vast underestimation of Madagascar's biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences 106: 8267-8272.
2. Bradley RD, Baker RJ, (2001) A test of the genetic species concept: cytochrome-b sequences and mammals Journal of Mammalogy 82: 960-973.
3. Monaghan MT, Balke M, Gregory TR, Vogler AP, (2005) DNA-based species delineation in tropical beetles using mitochondrial and nuclear markers. Philosophical Transactions of the Royal Society B: Biological Sciences 360: 1925-1933.
4. Isler ML, Isler PR, Whitney BM, (2007) Species limits in antbirds (Thamnophilidae): the warbling antbird (Hypocnemis cantator) complex. Auk 124: 11-28.
5. Dincǎ V, Zakharov EV, Hebert PDN, Vila R, (2011) Complete DNA barcode reference library for a country's butterfly fauna reveals high performance for temperate Europe. Proceedings of the Royal Society B: Biological Sciences 278: 347-355.
6. Clare EL, Kim BK, Fenton MB, Hebert PDN, (2011) Neotropical bats: estimating species diversity with DNA barcodes. PLOS One 6: e22648.
7. Moritz C, Cicero C, (2004) DNA barcoding: promise and pitfalls. PLoS Biol 2: e354.
8. Hajibabaei M, Singer GAC, Hebert PDN, Hickey DA, (2007) DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends in Genetics 23: 167-172.
9. Janzen DH, Hajibabaei M, Burns JM, Hallwachs W, Remigio E, et al. (2005) Wedding biodiversity inventory of a large and complex Lepidoptera fauna with DNA barcoding. Philosophical Transactions of the Royal Society B: Biological Sciences 360: 1835-1845.
10. Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM, (2004) Identification of birds through DNA barcodes. PLoS Biology 2: 1657-1663.
11. Kerr KCR, Stoeckle MY, Dove CJ, Weigt LA, Francis CM, et al. (2007) Comprehensive DNA barcode coverage of North American birds. Molecular Ecology Notes 7: 535-543.
12. Kerr K, Birks S, Kalyakin M, Red'kin Y, Koblik E, et al. (2009) Filling the gap- COI barcode resolution in eastern Palearctic birds. Frontiers in Zoology 6: 29.
13. Lijtmaer DA, Kerr KCR, Barreira AS, Hebert PDN, Tubaro PL, (2011) DNA barcode libraries provide insight into continental patterns of avian diversification. PLoS One 6: e20744.
14. Kerr KCR, Lijtmaer DA, Barreira AS, Hebert PDN, Tubaro PL, (2009) Probing evolutionary patterns in Neotropical birds through DNA barcodes. PLoS One 4: e4379.
15. Tavares ES, Gonçalves P, Miyaki CY, Baker AJ, (2011) DNA barcode detects high genetic structure within Neotropical bird species. PLoS One 6: e28543.
16. Yoo HS, Eah J-Y, Kim JS, Kim Y-J, Min M-S, et al. (2006) DNA barcoding Korean birds. Molecules and Cells 22: 323-327.
17. Aleixo A, (2004) Historical diversification of a terra-firme forest bird superspecies: a phylogeographic perspective on the role of different hypotheses of Amazonian diversification. Evolution 58: 1303-1317.
18. Cheviron ZA, Hackett SJ, Capparella AP, (2005) Complex evolutionary history of a Neotropical lowland forest bird (Lepidothrix coronata) and its implications for historical hypotheses of the origin of Neotropical avian diversity. Molecular Phylogenetics and Evolution 36: 338-357.
19. Marks BD, Hackett SJ, Capparella AP, (2002) Historical relationships among Neotropical lowland forest areas of endemism as determined by mitochondrial DNA sequence variation within the Wedge-billed Woodcreeper (Aves: Dendrocolaptidae: Glyphorynchus spirurus). Molecular Phylogenetics and Evolution 24: 153-167.
20. Nyári AS, (2007) Phylogeographic patterns, molecular and vocal differentiation, and species limits in Schiffornis turdina (Aves). Molecular Phylogenetics and Evolution 44: 154-164.
21. Ribas CC, Joseph L, Miyaki CY, Johnson KP, (2006) Molecular systematics and patterns of diversification in Pyrrhura (Psittacidae), with special reference to the picta-leucotis complex. The Auk 123: 660-680.
22. Miller MJ, Bermingham E, Klicka J, Escalante P, Raposo do Amaral FS, et al. (2008) Out of Amazonia again and again: episodic crossing of the Andes promotes diversification in a lowland forest flycatcher. Proceedings of the Royal Society B: Biological Sciences 275: 1133-1142.
23. Weir JT, Price M, (2011) Andean uplift promotes lowland speciation through vicariance and dispersal in Dendrocincla woodcreepers. Molecular Ecology 20: 4550-4563.
24. Bates JM, Hackett SJ, Goerck JM, (1999) High levels of mitochondrial DNA differentiation in two lineages of antbirds (Drymophila and Hypocnemis). Auk 116: 1093-1106.
25. Navarro-Sigüenza A, Peterson AT, (2004) An alternative species taxonomy of the birds of Mexico. Biota Neotropica 4: 1-32.
26. Cracraft J, (1985) Historical biogeography and patterns of differentiation within the South American areas of endemism. Ornithological Monographs 36: 49-84.
27. Restall R, Rodner C, Lentino M, (2006) Birds of Northern South America: An Identification Guide. New Haven: Yale University Press.
28. Ivanova NV, DeWaard JR, Hebert PDN, (2006) An inexpensive, automation friendly protocol for recovering high quality DNA. Molecular Ecology Notes 6: 998-1002.
29. Tavares ES, Baker AJ, (2008) Single mitochondrial gene barcodes reliably indentify sister-species in diverse clades of birds. BMC Evolutionary Biology 8: 81.
30. Dean AD, Greenwald JE, (1995) Use of filtered pipet tips to elute DNA from agarose gels. Biotechniques 18: 980.
31. Excoffier L, Laval G, Schneider S, (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47-50.
32. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739.
33. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R, (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497.
34. Fu YX, (1997) Statistical neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915-925.
35. Bleiweiss R, (2004) Ultraviolet plumage reflectance distinguishes sibling bird species. Proceedings of the National Academy of Sciences 101: 16561-16564.
36. Eaton MD, (2005) Human vision fails to distinguish widespread sexual dichromatism among sexually "monochromatic" birds. Proceedings of the National Academy of Sciences 102: 10942-10946.
37. Lovette IJ, (2004) Molecular phylogeny and plumage signal evolution in a trans Andean and circum Amazonian avian species complex. Molecular Phylogenetics and Evolution 32: 512-523.
38. Merilä J, Bjorklund M, Baker A, (1997) Historical demography and present day population structure of the greenfinch, Carduelis chloris- an analysis of mtDNA control-region sequences. Evolution 51: 946-956.
39. Milá B, McCormack JE, Castañeda G, Wayne RK, Smith TB, (2007) Recent postglacial range expansion drives the rapid diversification of a songbird lineage in the genus Junco. Proceedings of the Royal Society B 274: 2653-2660.
40. Pérez-Tris J, Bensch S, Carbonell R, Helbig AJ, Tellería JL, (2004) Historical diversification of migration patterns in a passerine bird. Evolution 58: 1819-1832.
41. Seutin G, Ratcliffe LM, Boag PT, (1995) Mitochondrial DNA homogeneity in the phenotypically diverse redpoll finch complex (Aves: Carduelinae: Carduelis flammea-hornemanni). Evolution 49: 962-973.
42. Zink RM, (1997) Phylogeographic studies of North American birds. Avian Molecular Evolution and Systematics: Academic Press pp. 301-324.
43. Zink RM, Dittman DL, (1993) Gene flow, refugia, and evolution of geographic variation in the song sparrow (Melospiza melodia). Evolution 47: 717-729.
44. Pavlova A, Zink RM, Drovetski SV, Red'kin Y, Rohwer S, (2003) Phylogeographic patterns in Motacilla flava and Motacilla citreola: species limits and population history. Auk 123: 744-758.
45. Buerkle CA, (1999) The historical pattern of gene flow among migratory and nonmigratory populations of prairie warblers (Aves: Parulinae). Evolution 53: 1915-1924.
46. Kimura M, Clegg SM, Lovette IJ, R HK, Girman DJ, et al. (2002) Phylogeographical approaches to assessing demographic connectivity between breeding and overwintering regions in a Nearctic-Neotropical warbler (Wilsonia pusilla). Molecular Ecology 11: 1605-1616.
47. Milá B, Girman DJ, Kimura M, Smith TB, (2000) Genetic evidence for the effect of a postglacial population expansion on the phylogeography of a North American songbird. Proceedings of the Royal Society Biological Sciences Series B 267: 1033-1040.
48. Milá B, Smith TB, Wayne RK, (2006) Postglacial population expansion drives the evolution of long-distance migration in a songbird. Evolution 60: 2403-2409.
49. Martin PR, Montgomerie R, Loughheed SC, (2009) Rapid sympatry explains greater color pattern divergence in high latitude birds. Evolution 64: 336-347.
50. Weir JT, Wheatcroft D, (2011) A latitudinal gradient in rates of evolution of avian syllable diversity and song length. Proceedings of the Royal Society B 278: 1713-1720.
51. Weir JT, Price T, (2011) Limits to speciation inferred from times to secondary sympatry and ages of hybridizing species along a latitudinal gradient. American Naturalist 177: 462-469.
52. Weir JT, Schluter D, (2007) The latitudinal gradient in recent speciation and extinction rates of birds and mammals. Science 315: 1574-1576.
53. Tobias JA, Bates JM, Hackett SJ, Seddon N, (2008) Comment on "The latitudinal gradient in recent speciation and extinction rates of birds and mammals" Science 319: 901c.
54. Cardillo M, Orme CD, Owens IPF, (2005) Testing for latitudinal bias in diversification rates: an example using New World birds. Ecology 86: 2278-2287.
55. Ricklefs RE, (2006) Global variation in the diversification rate of passerine birds. Ecology 87: 2468-2478.
56. Johns GC, Avise JC, (1998) A comparative summary of genetic distances in the vertebrates from the Mitochondrial cytochrome b gene. Mol Biol Evol 15: 1481-1490.
57. Braun MJ, Isler ML, Isler PR, Bates JM, Robbins MB, (2005) Avian speciation in the Pantepui: the case of the Roraiman antbird (Percnostola [Schistocichla] "leucostigma" saturata). Condor 107: 327-341.
58. Armenta JK, Weckstein JD, Lane DF, (2005) Geographic variation in mitochondrial DNA sequences of an Amazonian nonpasserine: the black-spotted barbet complex. Condor 107: 527-536.
59. Zink RM, (1996) Comparative phylogeography in North American birds. Evolution 50: 308-317.
60. Brumfield RT, (2005) Mitochondrial variation in Bolivian populations of the Variable Antshrike (Thamnophilus caerulescens). Auk 122: 414-432.
61. Cabanne GS, D'Horta FM, Meyer D, SIlva JMC, Miyaki CY, (2011) Evolution of Dendrocolaptes platyrostris (Aves: Furnariidae) between the South American open vegetation corridor and the Atlantic forest. Biological Journal of the Linnean Society 103: 801-820.
62. Cracraft J, Prum RO, (1988) Patterns and processes of diversification: speciation and historical congruence in some neotropical birds. Evolution 42: 603-620.
63. Burney CW, Brumfield RT, (2009) Ecology predicts levels of genetic differentiation in Neotropical birds. American Naturalist 174: 358-368.
64. Aleixo A, (2006) Historical diversification of floodplain forest specialist species in the Amazon: a case study with two species of the avian genus Xiphorhynchus (Aves:Dendrocolaptidae). Biological Journal of the Linnean Society 89: 383-395.
65. Cadena CD, Gutiérrez-Pinto N, Dávila N, Terry Chesser R, (2011) No population genetic structure in a widespread aquatic songbird from the Neotropics. Molecular Phylogenetics and Evolution 58: 540-545.
66. Puebla-Olivares F, Bonaccorso E, Espinosa de los Monteros A, Omland KE, Llorente-Bousquets JE, et al. (2008) Speciation in the Emerald Toucanet (Aulachorhynchus prasinus) complex. Auk 125: 39-50.
67. Milá B, Toews DPL, Smith TB, Wayne RK, (2011) A cryptic contact zone between divergent mitochondrial DNA lineages in southwestern North America supports past introgressive hybridization in the yellow-rumped warbler complex (Aves: Dendroica coronata). Biol J Linn Soc 103: 696-706.
68. Irwin DE, Rubstov AS, Panov EN, (2009) Mitochondrial introgression and replacement between yellowhammers (Emberiza citrinella) and pine buntings (Emberiza leucocephalos) (Aves: Passeriformes). Biological Journal of the Linnean Society 98: 422-438.
69. Zink RM, Barrowclough GF, (2008) Mitochondrial DNA under siege in avian phylogeography. Molecular Ecology 17: 2107-2121.
70. Hebert PDN, Gregory TR, (2005) The promise of DNA barcoding for taxonomy. Systematic Biology 54: 852-859.
71. Burns KJ, Naoki K, (2004) Molecular phylogenetics and biogeography of Neotropical tanagers in the genus Tangara. Molecular Phylogenetics and Evolution 32: 838-854.
72. Cadena CD, Klicka J, Ricklefs RE, (2007) Evolutionary differentiation in the Neotropical montane region: molecular phylogenetics and phylogeography of Buarremon brush-finches (Aves, Emberizidae). Molecular Phylogenetics and Evolution 44: 993-1016.
73. Hackett SJ, Rosenberg KV, (1990) Comparison of phenotypic and genetic differentiation in South American antwtrens (Formicaridae). Auk 107: 473-489.
74. Lovette IJ, Pérez-Emán JL, Sullivan JP, Banks RC, Fiorentino I, et al. (2010) A comprehensive multilocus phylogeny for the wood-warblers and a revised classification of the Parulidae (Aves). Molecular Phylogenetics and Evolution 57: 753-770.
75. McGuire JA, Witt CC, Altshuler DL, Remsen JVJ, (2007) Phylogenetic systematics and biogeography of hummingbirds: Bayesian and maximum likelihood analyses of partitioned data and selection of an appropriate partitioning strategy. Systematic Biology 56: 837-856.
76. Voelker G, Rohwer S, Bowie RCK, Outlaw DC, (2007) Molecular systematics of a speciose, cosmopolitan songbird genus: defining the limits of, and relationships among, the Turdus thrushes. Molecular Phylogenetics and Evolution 42: 422-434.
77. Hackett SJ, (1996) Molecular phylogenetics and biogeography of tanagers in the genus Ramphocelus (Aves). Molecular Phylogenetics and Evolution 5: 368-382.
78. Eberhard JR, Bermingham E, (2004) Phylogeny and biogeography of the Amazona ochrocephala (Aves; Psittacidae) complex. Auk 121: 318-332.
79. Eberhard JR, Bermingham E, (2005) Phylogeny and comparative biogeography of Pionopsitta parrots and Pteroglossus toucans. Molecular Phylogenetics and Evolution 36: 288-304.
80. Russello MA, Amato G, (2004) A molecular phylogeny of Amazona: implications for Neotropical parrot biogeography, taxonomy, and conservation. Molecular Phylogenetics and Evolution 30: 421-437.
81. Campagna L, Geale K, Handford P, Lijtmaer DA, Tubaro PL, et al. (2011) A molecular phylogeny of the Sierra-Finches (Phrygilus, Passeriformes): Extreme polyphyly in a group of Andean specialists. Molecular Phylogenetics and Evolution 61: 521-533.
82. McCormack JE, Peterson AT, Bonaccorso E, Smith TB, (2008) Speciation in the highlands of Mexico: genetic and phenotypic divergence in the Mexican jay (Aphelocoma ultramarina). Molecular Ecology 17: 2505-2521.
83. Aleixo A, (2002) Molecular systematics and the role of the "varzea"-"terra firme" ecotone in the diversification of Xiphorhynchus woodcreepers (Aves: Dendrocolaptidae). Auk 119: 621-640.
84. Ribas CC, Gaban-Lima R, Miyaki CY, Cracraft J, (2005) Historical biogeography and diversification within the Neotropical parrot genus Pionopsitta (Aves: Psittacidae). Journal of Biogeography 32: 1409-1427.
85. Omland KE, Lanyon SM, (2000) Reconstructing plumage evolution in orioles (Icterus): repeated convergence and reversal in patterns. Evolution 54: 2119-2133.
86. Moore WS, Weibel AC, Agius A, (2006) Mitochondrial DNA phylogeny of the woodpecker genus Veniliornis (Picidae, Picinae) and related genera implies convergent evolution of plumage patterns. Biological Journal of the Linnean Society 87: 611-624.
87. Beheregaray LB, Caccone A, (2007) Cryptic biodiversity in a changing world. Journal of Biology 6: 9.
88. Toews DPL, Irwin DE, (2008) Cryptic speciation in a Holarctic passerine revealed by genetic and bioacoustic analyses. Molecular Ecology 17: 2691-2705.
89. Dacosta JM, Klicka J, (2008) The Great American Interchange in birds: a phylogenetic perspective with the genus Trogon. Molecular Ecology 17: 1328-1343.
90. Padial JM, de la Riva I, (2010) A response to recent proposals for integrative taxonomy. Biological Journal of the Linnean Society 101: 747-756.
91. Sites JWJ, Marshall JC, (2004) Operational criteria for delimiting species. Annu Rev Ecol Evol Syst 35: 199-227.
92. Sangster G, (2009) Increasing numbers of bird species result from taxonomic progress, not taxonomic inflation. Proceedings of the Royal Society B 276: 3185-3191.
93. Blackburn TM, Gaston KJ, (1996) Spatial patterns in the geographic range sizes of bird species in the New World. Phil Trans R Soc Lond B 351: 897-912.
94. Brumfield RT, Capparella AP, (1996) Historical diversification of birds in northwestern south America: A molecular perspective on the role of vicariant events. Evolution 50: 1607-1624.
95. Brumfield RT, Edwards SV, (2007) Evolution into and out of the Andes: a Bayesian analysis of historical diversification in Thamnophilus antshrikes. Evolution pp. 346-367.
96. Beven S, Connor EF, Beven K, (1984) Avian biogeography in the Amazon basin and the biological model of diversification. Journal of Biogeography 11: 383-399.
97. Moritz C, Patton JL, Schneider CJ, Smith TB, (2000) Diversification of rainforest faunas: an integrated molecular approach. Annual Review of Ecology and Systematics 31: 533-563.
98. Avise JC, Walker D, Johns GC, (1998) Speciation durations and Pleistocene effects on vertebrate phylogeography. Proc R Soc Lond B 265: 1707-1712.
99. Buermann W, Saatchi S, Smith TB, Zutta BR, Chaves JA, et al. (2008) Predicting species distrubutions across the Amazonian and Andean regions using remote sensing data. Journal of Biogeography 35: 1160-1176.
100. Faith D, (1994) Genetic diversity and taxonomic priorities for conservation. Biological Conservation 68: 69-74.
101. Faith DP, Reid CAM, Hunter J, (2004) Integrating phylogenetic diversity, complementarity, and endemism for conservation assessment. Conservation Biology 18: 255-261.
102. Thomassen HA, Buermann W, Milá B, Graham CH, Cameron SE, et al. (2009) Modeling environmentally associated morphological and genetic variation in a rainforest bird, and its application to conservation prioritization. Evolutionary Applications 3: 1-16.