Evolutionary Biology

, Volume 40, Issue 2, pp 228–245 | Cite as

The Early Stages of Speciation in Amazonian Forest Frogs: Phenotypic Conservatism Despite Strong Genetic Structure

  • Igor L. Kaefer
  • Bruno M. Tsuji-Nishikido
  • Edvaldo P. Mota
  • Izeni P. Farias
  • Albertina P. Lima
Research Article

Abstract

Phylogeographic perspectives incorporating multiple classes of characters, especially those relating to sexual signals, are promising for the elucidation of recent evolutionary mechanisms driving speciation. Here, forest frogs were used as a model system to access distinct stages in the process of evolutionary differentiation. We studied 280 individuals assigned to three species: Allobates paleovarzensis, A. nidicola and A. masniger. Samples were collected at 20 localities arranged in two study systems, along the middle Amazon and the lower Madeira Rivers, in Central Amazonia. Mantel tests, analyses of molecular variance, and the spatial distribution of haplogroups indicated that the distribution of genetic variability, as inferred from a mitochondrial DNA marker, was determined by a combination of isolation-by-distance effects and the transposition of large Amazonian rivers. These two factors had contrasting relative influences in each of the study systems, which also differed regarding the estimated time of the major cladogenetic events. Pronounced population genetic structure was observed. However, multivariate discriminant function analyses revealed that the phenotypic (morphological and acoustic) divergence was loosely related with genetic differentiation and did not successfully predict assignment of individuals to genetic groups. The observed distribution of genetic variability showed the important role of genetic drift in the diversification of the mitochondrial marker studied. The phenotypic conservatism among populations was surprising in view of the high genetic structuring observed, and indicates a prevailing role of stabilizing selective forces in the process of sexual signal and morphological differentiation.

Keywords

Genetic drift Integrative phylogeography Isolation by distance Mitochondrial DNA River barrier Sexual signals 

Supplementary material

11692_2012_9205_MOESM1_ESM.pdf (23 kb)
Online Resource 1 Advertisement call measurements of individuals of Allobates paleovarzensis in each study locality in Brazilian Amazonia. Values are presented as mean (above) and standard deviation (below). Call traits are: Note rate (NR, in notes/s); Note duration (ND, in s); Internote interval, as the silent interval between two consecutive notes of a call (InI, in s); Call rate (CR, in calls/s); Call duration (CD, in s); Intercall interval, as the silent interval between two consecutive calls (IcI, in s); Maximum (peak) frequency, as the frequency of higher intensity calculated for the entire note by a power spectrum function of Raven Pro 1.3 (MF, in Hz); Lowest frequency (LF, in Hz); Highest frequency (HF, in Hz); Note modulation, as the difference between the highest and the lowest frequencies of the call (NM, in Hz). Sampling locality codes, sample sizes and respective geographic coordinates are given on Table 1. (PDF 23 kb)
11692_2012_9205_MOESM2_ESM.pdf (19 kb)
Online Resource 2 Advertisement call measurements of individuals of Allobates nidicola and A. masniger in each study locality in Brazilian Amazonia. Values are presented as mean (above) and standard deviation (below). Call traits are: Note duration (ND, in s); Interval between notes (IN, in s); Lowest frequency (LF, in Hz); Highest frequency (HF, in Hz); Note modulation, calculated as the difference between the maximum and minimum frequencies (NM, in Hz); and Peak frequency (PF, in Hz). Sampling locality codes, sample sizes and respective geographic coordinates are given on Table 1. (PDF 18 kb)
11692_2012_9205_MOESM3_ESM.pdf (37 kb)
Online Resource 3 Morphometric measurements (in mm) of individuals of Allobates paleovarzensis in each study locality in Brazilian Amazonia. Values are presented as mean (above) and standard deviation (below). Morphometric traits are: Snout-vent length (SVL); Head length from angle of jaws to tip of snout (HL); Head width at level of angle of jaws (HW); Snout length from anterior corner of eye to tip of snout (SL); Eye to nostril distance from anterior corner of eye to centre of nostril (EN); Inter-nostril distance (IN); Eye length from anterior to posterior corner (EL); Inter-orbital distance (IO); Diameter of tympanum (TYM); Forearm length from proximal edge of palmar tubercle to outer edge of flexed elbow (FAL); Upper arm length from trunk insertion to outer edge of flexed elbow (UAL); Hand length from proximal edge of palmar tubercle to tip of fingers I, II, III and IV (HAND1, HAND2, HAND3 and HAND4); Width of disc on finger III (WFD); Tibia length from outer edge of flexed knee to heel (TL); Foot length from proximal edge of outer metatarsal tubercle to tip of toe IV (FL); Femur length (LL); Diameter of palmar tubercle (DPT); Width of tenar tubercle (WTT); Width of disc on toe IV (WTD); Width of finger III (WPF). Sampling locality codes, sample sizes and respective geographic coordinates are given on Table 1. (PDF 37 kb)
11692_2012_9205_MOESM4_ESM.pdf (37 kb)
Online Resource 4 Morphometric measurements (in mm) of individuals of Allobates nidicola and A. masniger in each study locality in Brazilian Amazonia. Values are presented as mean (above) and standard deviation (below). Morphometric traits are described in Online Resource 3. Sampling locality codes, sample sizes and respective geographic coordinates are given on Table 1. (PDF 37 kb)
11692_2012_9205_MOESM5_ESM.pdf (24 kb)
Online Resource 5 Distribution of 16S rDNA haplotypes of Allobates among 20 sampled localities in Brazilian Amazonia. Collection numbers of vouchers (INPA-H) and GenBank accession numbers are provided. Sampled localities are numbered according to Table 1. (PDF 24 kb)
11692_2012_9205_MOESM6_ESM.pdf (335 kb)
Online Resource 6 Mismatch distributions obtained from pairwise nucleotide site differences among 16S rDNA sequences composing the clusters of the (A) paleovarzensis and the (B) nidicolamasniger systems. Clusters were determined via Bayesian Analysis of Population Differentiation. Pairwise differences were not calculated for Cluster 4 of Allobates paleovarzensis due to the small number of samples that compose it. (PDF 334 kb)
11692_2012_9205_MOESM7_ESM.pdf (18 kb)
Online Resource 7 Classification matrix based on the discriminant function analysis, using phenotypic data from males of Allobates paleovazensis pertaining to four genetic clusters. Clusters are coded from C1 to C4, according to Table 4. Body-shape traits were used to discriminate individuals based on morphology. Acoustic measurements were adjusted for temperature and for both temperature and body size through linear regressions. The number and percentage of individuals correctly assigned to each genetic cluster are indicated. (PDF 18 kb)
11692_2012_9205_MOESM8_ESM.pdf (24 kb)
Online Resource 8 Classification matrix based on the discriminant function analysis, using phenotypic data from males of Allobates nidicola and A. masniger pertaining to seven genetic clusters. Clusters are coded from C1 to C7, according to Table 4. Body-shape traits were used to discriminate individuals based on morphology. Acoustic measurements were adjusted for temperature and for both temperature and body size through linear regressions. The number and percentage of individuals correctly assigned to each genetic cluster are indicated. (PDF 24 kb)

References

  1. Adams, D. C., Berns, C. M., Kozak, K. H., & Wiens, J. (2009). Are rates of species diversification correlated with rates of morphological evolution? Proceedings of the Royal Society B, 276, 2729–2738.PubMedCrossRefGoogle Scholar
  2. Amézquita, A., Lima, A. P., Jehle, R., Castellanos, L., Ramos, O., Crawford, A. J., et al. (2009). Calls, colours, shapes, and genes: A multi–trait approach to the study of geographic variation in the Amazonian frog Allobates femoralis. Biological Journal of the Linnean Society, 98, 826–838.CrossRefGoogle Scholar
  3. Anderson, M. J., & Legendre, P. (1999). An empirical comparison of permutation methods for tests of partial regression coefficients in a linear model. Journal of Statistical Computation and Simulation, 62, 271–303.CrossRefGoogle Scholar
  4. 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, 58–77.Google Scholar
  5. Antonelli, A., Quijada-Mascareñas, A., Crawford, A. J., Bates, J. M., Velazco, P. M., & Wüster, W. (2010). Molecular studies and phylogeography of Amazonian tetrapods and their relation to geological and climatic models. In C. Hoorn & F. P. Wesselingh (Eds.), Amazonia, landscape and species evolution (pp. 386–403). Oxford: Blackwell Publishing.Google Scholar
  6. Avise, J. C. (2000). Phylogeography: The history and formation of species. Cambridge: Harvard University Press.Google Scholar
  7. Avise, J. C. (2004). Molecular markers, natural history and evolution (2nd ed.). Sunderland: Sinauer Associates Inc.Google Scholar
  8. Ayres, J. M., & Clutton-Brock, T. H. (1992). River boundaries and species range size in Amazonian primates. The American Naturalist, 140, 531–537.PubMedCrossRefGoogle Scholar
  9. Blomberg, S. P., Garland, T., Jr, & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57, 717–745.PubMedGoogle Scholar
  10. Bonnet, E., & Van de Peer, Y. (2002). ZT: A software tool for simple and partial Mantel tests. Journal of Statistical Software, 7, 1–12.Google Scholar
  11. Boul, K. E., Funk, W. C., Darst, C. R., Cannatella, D. C., & Ryan, M. J. (2007). Sexual selection drives speciation in an Amazonian frog. Proceedings of the Royal Society B, 274, 399–406.PubMedCrossRefGoogle Scholar
  12. Caldwell, J. P., & Lima, A. P. (2003). A new Amazonian species of Colostethus (Anura: Dendrobatidae) with a nidicolous tadpole. Herpetologica, 59, 219–234.CrossRefGoogle Scholar
  13. Camargo, A., de Sá, R., & Heyer, W. R. (2006). Phylogenetic analyses of mtDNA sequences reveal three cryptic lineages in the widespread neotropical frog Leptodactylus fuscus (Schneider, 1799) (Anura, Leptodactylidae). Biological Journal of the Linnean Society, 87, 325–341.CrossRefGoogle Scholar
  14. Campbell, P., Pasch, B., Pino, J. L., Crino, O. L., Phillips, M., & Phelps, S. M. (2010). Geographic variation in the songs of neotropical singing mice: Testing the relative importance of drift and local adaptation. Evolution, 64, 1955–1972.PubMedGoogle Scholar
  15. Capparella, A. P. (1988). Genetic variation in Neotropical birds: Implications for the speciation process. In H. Ouellet (Ed.), Acta XIX Congressus Internationalis Ornithologici (pp. 1658–1664). Ottawa: University of Ottawa Press.Google Scholar
  16. Charif, R. A., Clark, C. W., & Fristrup, K. M. (2004). Raven 1.2 User’s manual. Ithaca: Cornell Laboratory of Ornithology.Google Scholar
  17. Charif, R. A., Waack, A. M., & Strickman, L. M. (2008). Raven Pro 1.3 User’s manual. Ithaca: Cornell Laboratory of Ornithology.Google Scholar
  18. Cherry, L. M., Case, S. M., & Wilson, A. C. (1978). Frog perspective on the morphological difference between humans and chimpanzees. Science, 200, 209–211.CrossRefGoogle Scholar
  19. Clement, M., Posada, D., & Crandall, K. A. (2000). TCS: A computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.PubMedCrossRefGoogle Scholar
  20. Cohn-Haft, M. (2000). A case study in amazonian biogeography: Vocal and DNA sequence variation in Hemitriccus flycatchers. PhD thesis. Luisiana State University.Google Scholar
  21. Colwell, R. K. (2000). A barrier runs through it… or maybe just a river. Proceedings of the National Academy of Sciences, 97, 13470–13472.CrossRefGoogle Scholar
  22. Corander, J., Marttinen, P., Sirén, J., & Tang, J. (2008). Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics, 9, 539.PubMedCrossRefGoogle Scholar
  23. Costa, J. B. S., Bemerguy, R. L., Hasui, Y., & Borges, M. S. (2001). Tectonics and paleogeography along the Amazon River. Journal of South American Earth Sciences, 14, 335–347.CrossRefGoogle Scholar
  24. Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland: Sinauer Associates Inc.Google Scholar
  25. Crawford, A. J. (2003). Huge populations and old species of Costa Rican and Panamanian dirt frogs inferred from mitochondrial and nuclear gene sequences. Molecular Ecology, 12, 2525–2540.PubMedCrossRefGoogle Scholar
  26. Crawford, A. J., Lips, K. R., & Bermingham, E. (2010). Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proceedings of the National Academy of Sciences, 107, 13777–13782.CrossRefGoogle Scholar
  27. Creer, S., Thorpe, R. S., Malhotra, A., Chou, W. H., & Stenson, A. G. (2004). The utility of AFLPs for supporting mitochondrial DNA phylogeographical analyses in the Taiwanese bamboo viper, Trimeresurus stejnegeri. Journal of Evolutionary Biology, 17, 100–107.PubMedCrossRefGoogle Scholar
  28. Crisci, J. V., Katinas, L., & Posadas, P. (2003). Historical biogeography: An introduction. Cambridge: Harvard University Press.Google Scholar
  29. Dall, S. R. X. (1997). Behaviour and speciation. Trends in Ecology & Evolution, 12, 209–210.CrossRefGoogle Scholar
  30. Dayrat, B. (2005). Towards integrative taxonomy. Biological Journal of the Linnean Society, 85, 407–415.CrossRefGoogle Scholar
  31. de Queiroz, K. (2007). Species concepts and species delineation. Systematic Biology, 56, 879–886.PubMedCrossRefGoogle Scholar
  32. Diniz-Filho, J. A. F., Telles, M. P. C., Bonatto, S. L., Eizirik, E., Freitas, T. R. O., de Marco, P., et al. (2008). Mapping the evolutionary twilight zone: Molecular markers, populations and geography. Journal of Biogeography, 35, 753–763.CrossRefGoogle Scholar
  33. Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.PubMedCrossRefGoogle Scholar
  34. Elmer, K. R., Dávila, J. A., & Lougheed, S. C. (2007). Cryptic diversity and deep divergence in an upper Amazonian leaflitter frog, Eleutherodactylus ockendeni. BMC Evolutionary Biology, 7, 247.PubMedCrossRefGoogle Scholar
  35. Erdtmann, L., & Amézquita, A. (2009). Differential evolution of advertisement call traits in Dart–Poison Frogs (Anura: Dendrobatidae). Ethology, 115, 801–811.CrossRefGoogle Scholar
  36. Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Research, 10, 564–567.CrossRefGoogle Scholar
  37. Excoffier, L., Smouse, P., & Quattro, J. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics, 131, 479–491.PubMedGoogle Scholar
  38. Fernandes, A. M., Wink, M., & Aleixo, A. (2012). Phylogeography of the chestnut tailed antbird (Myrmeciza hemimelaena) clarifies the role of rivers in Amazonian biogeography. Journal of Biogeography, 39, 1524–1535.CrossRefGoogle Scholar
  39. Figueiredo, J., Hoorn, C., van der Ven, P., & Soares, E. (2009). Late Miocene onset of the Amazon River and the Amazon deep-sea fan: Evidence from the Foz do Amazonas Basin. Geology, 37, 619–622.CrossRefGoogle Scholar
  40. Fouquet, A., Gilles, A., Vences, M., Marty, C., Blanc, M., & Gemmell, N. J. (2007). Underestimation of species richness in Neotropical frogs revealed by mtDNA analyses. PLoS ONE, 10, e1109.CrossRefGoogle Scholar
  41. Fouquet, A., Noonan, B. P., Rodrigues, M. T., Pech, N., Gilles, A., & Gemmell, N. J. (2012a). Multiple quaternary Refugia in the Eastern Guiana shield revealed by comparative phylogeography of 12 frog species. Systematic Biology, 61, 461–489.PubMedCrossRefGoogle Scholar
  42. Fouquet, A., Recoder, R., Teixeira, M., Jr, Cassimiro, J., Amaro, R. C., Camacho, A., et al. (2012b). Molecular phylogeny and morphometric analyses reveal deep divergence between Amazonia and Atlantic Forest species of Dendrophryniscus. Molecular Phylogenetics and Evolution, 62, 826–838.PubMedCrossRefGoogle Scholar
  43. Fu, Y. X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915–925.PubMedGoogle Scholar
  44. Funk, W. C., Caldwell, J. P., Peden, C. E., Padial, J. M., de la Riva, I., & Cannatella, D. C. (2007). Tests of biogeographic hypotheses for diversification in the Amazonian forest frog, Physalaemus petersi. Molecular Phylogenetics and Evolution, 44, 825–837.PubMedCrossRefGoogle Scholar
  45. Funk, W. C., Caminer, M., & Ron, S. R. (2012). High levels of cryptic species diversity uncovered in Amazonian frogs. Proceedings of the Royal Society B, 279, 1806–1814.PubMedCrossRefGoogle Scholar
  46. Funk, D. J., & Omland, K. E. (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.CrossRefGoogle Scholar
  47. Gascon, C., Lougheed, S. C., & Bogart, J. P. (1996). Genetic and morphological variation in Vanzolinius discodactylus: a direct test of the riverine barrier hypothesis. Biotropica, 28, 376–387.CrossRefGoogle Scholar
  48. Gascon, C., Lougheed, S. C., & Bogart, J. P. (1998). Patterns of genetic population differentiation in four species of Amazonian frogs: A test of the Riverine Barrier Hypothesis. Biotropica, 30, 104–119.CrossRefGoogle Scholar
  49. Gascon, C., Malcolm, J. R., Patton, J. L., Silva, M. N. F., Bogart, J. P., Lougheed, S. C., et al. (2000). Riverine barriers and the geographic distribution of Amazonian species. Proceedings of the National Academy of Sciences, 97, 13672–13677.CrossRefGoogle Scholar
  50. Gerhardt, H. C., & Huber, F. (2002). Acoustic communication in insects and anurans: Common problems and diverse solutions. Chicago: University of Chicago Press.Google Scholar
  51. Goicochea, N., De La Riva, I., & Padial, J. M. (2009). Recovering phylogenetic signal from frog mating calls. Zoologica Scripta, 39, 141–154.CrossRefGoogle Scholar
  52. Grant, T., Frost, D. R., Caldwell, J. P., Gagliardo, R., Haddad, C. F. B., Kok, P. J. R., et al. (2006). Phylogenetic systematics of dart–poison frogs and their relatives (Anura: Athesphatanura: Dendrobatidae). Bulletin of the American Museum of Natural History, 299, 1–262.CrossRefGoogle Scholar
  53. Groeneveld, L. F., Weisrock, D. W., Rasoloarison, R. M., Yoder, A. D., & Kappeler, P. M. (2009). Species delimitation in lemurs: Multiple genetic loci reveal low levels of species diversity in the genus Cheirogaleus. BMC Evolutionary Biology, 9, 30.PubMedCrossRefGoogle Scholar
  54. Guerra, M. A., & Ron, S. R. (2008). Mate choice and courtship signal differentiation promotes speciation in an Amazonian frog. Behavioral Ecology, 19, 1128–1135.CrossRefGoogle Scholar
  55. Guillot, G., Renaud, S., Ledevin, R., Michaux, J., & Claude, J. (2012). A unifying model for the analysis of phenotypic, genetic and geographic data. Systematic Biology,. doi:10.1093/sysbio/sys038.PubMedGoogle Scholar
  56. Haffer, J. (1969). Speciation in Amazonian Forest Birds. Science, 165, 131–137.PubMedCrossRefGoogle Scholar
  57. Hafner, J. C., & Upham, N. S. (2011). Phylogeography of the dark kangaroo mouse, Microdipodops megacephalus: cryptic lineages and dispersal routes in North America’s Great Basin. Journal of Biogeography, 38, 1077–1097.PubMedCrossRefGoogle Scholar
  58. Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.Google Scholar
  59. Harpending, R. C. (1994). Signature of ancient population growth in a low–resolution mitochondrial DNA mismatch distribution. Human Biology, 66, 591–600.PubMedGoogle Scholar
  60. Hayes, F. E., & Sewlal, J. N. (2004). The Amazon River as a dispersal barrier to passerine birds: Effects of river width, habitat and taxonomy. Journal of Biogeography, 31, 1809–1818.CrossRefGoogle Scholar
  61. Hoorn, C. (1994). An environmental reconstruction of the palaeo-Amazon River system (Middle-Late Miocene, NW Amazonia). Palaeogeography, Palaeoclimatology, Palaeoecology, 112, 187–238.CrossRefGoogle Scholar
  62. Hoorn, C., Wesselingh, F. P., ter Steege, H., Bermudez, M. A., Mora, A., Sevink, J., et al. (2010). Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science, 330, 927–931.PubMedCrossRefGoogle Scholar
  63. Hubert, N., Meyer, C. P., Bruggemann, H. J., Guérin, F., Komeno, R. J. L., Espiau, B., et al. (2012). Cryptic diversity in Indo–Pacific coral–reef fishes revealed by DNA–barcoding provides new support to the centre–of–overlap hypothesis. PLoS ONE, 7, e28987.PubMedCrossRefGoogle Scholar
  64. Hutchison, D. W., & Templeton, A. R. (1999). Correlation of pairwise genetic and geographic distance measures: Inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution, 53, 1898–1914.CrossRefGoogle Scholar
  65. Irion, G., & Kalliola, R. (2010). Long–term landscape development processes in Amazonia. In C. Hoorn & F. P. Wesselingh (Eds.), Amazonia, landscape and species evolution (pp. 185–197). Oxford: Blackwell Publishing.Google Scholar
  66. Kaefer, I. L., & Lima, A. P. (2012). Sexual signals of the Amazonian frog Allobates paleovarzensis: Geographic variation and stereotypy of acoustic traits. Behaviour, 149, 15–33.CrossRefGoogle Scholar
  67. Kaefer, I. L., Montanarin, A., Costa, R. S., & Lima, A. P. (in press). Temporal patterns of reproductive activity and site attachment of the Brilliant–thighed Frog Allobates femoralis from Central Amazonia. Journal of Herpetology.Google Scholar
  68. Kaefer, I. L., Tsuji-Nishikido, B. M., & Lima, A. P. (2012). Beyond the river: underlying determinants of population acoustic signal variability in Amazonian direct–developing Allobates (Anura: Dendrobatoidea). Acta Ethologica, 15, 187–194.CrossRefGoogle Scholar
  69. 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.PubMedCrossRefGoogle Scholar
  70. Lemmon, E. M. (2009). Diversification of conspecific signals in sympatry: Geographic overlap drives multidimensional reproductive character displacement in frogs. Evolution, 63, 1155–1170.PubMedCrossRefGoogle Scholar
  71. Librado, P., & Rozas, J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.PubMedCrossRefGoogle Scholar
  72. Lima, A. P., Caldwell, J. P., Biavati, G., & Montanarin, A. (2010). A new species of Allobates (Anura: Aromobatidae) from paleovárzea forest in Amazonas, Brazil. Zootaxa, 2337, 1–17.Google Scholar
  73. Lougheed, S. C., Austin, J. D., Bogart, J. P., Boag, P. T., & Chek, A. A. (2006). Multi–character perspectives on the evolution of intraspecific differentiation in a neotropical hylid frog. BMC Evolutionary Biology, 6, 23.PubMedCrossRefGoogle Scholar
  74. Lougheed, S. C., Gascon, C., Jones, D. A., Bogart, J. P., & Boag, P. T. (1999). Ridges and rivers: a test of competing hypothesis of Amazonian diversification using a dart–poison frog (Epipedobates femoralis). Proceedings of the Royal Society B, 266, 1829–1835.PubMedCrossRefGoogle Scholar
  75. Lynch, M., & Crease, T. J. (1990). The analysis of population survey data on DNA sequence variation. Molecular Biology and Evolution, 7, 377–394.PubMedGoogle Scholar
  76. Mantel, N. (1967). The detection of disease clustering and a generalized regression approach. Cancer Research, 27, 209–220.PubMedGoogle Scholar
  77. McKay, B. D., & Zink, R. M. (2009). The causes of mitochondrial DNA gene tree paraphyly in birds. Molecuar Phylogenetics and Evolution, 54, 647–650.CrossRefGoogle Scholar
  78. Morales, V. R. (2002). Sistematica y biogeografía del grupo trilineatus (Amphibia, Anura, Dendrobatidae, Colostethus), con descripción de once nuevas especies. Publicación de la Asociación Amigos Doñana, 13, 1–59.Google Scholar
  79. Moritz, C., Patton, J. L., Schneider, C. J., & Smith, T. B. (2000). Diversification of rainforest faunas: An integrated molecular approach. Annual Review of Ecology and Systematics, 31, 533–563.CrossRefGoogle Scholar
  80. Noonan, B. P., & Gaucher, P. (2006). Refugial isolation and secondary contact in the dyeing poison frog Dendrobates tinctorius. Molecular Ecology, 15, 4425–4435.PubMedCrossRefGoogle Scholar
  81. Nosil, P., Harmon, L. J., & Seehausen, O. (2009). Ecological explanations for (incomplete) speciation. Trends in Ecology & Evolution, 24, 145–156.CrossRefGoogle Scholar
  82. Palumbi, S. R. (1996). Nucleic acids II: the polymerase chain reaction. In D. M. Hillis, C. Moritz, & B. K. Mable (Eds.), Molecular systematics (pp. 205–247). Sunderland: Sinauer Associates Inc.Google Scholar
  83. Panhuis, T. M., Butlin, R., Zuk, M., & Tregenza, T. (2001). Sexual selection and speciation. Trends in Ecology & Evolution, 16, 364–371.CrossRefGoogle Scholar
  84. Patton, J. L., Silva, M. N. F., & Malcolm, J. R. (1994). Gene genealogy and differentiation among arboreal spiny rats (Rodentia: Echymidae) of the Amazon Basin: a test of the riverine barrier hypothesis. Evolution, 48, 1314–1323.CrossRefGoogle Scholar
  85. Pröhl, H. (2005). Territorial behavior in dendrobatid frogs. Journal of Herpetology, 39, 354–365.CrossRefGoogle Scholar
  86. Pröhl, H., Hagemann, S., Karsch, J., & Höbel, G. (2007). Geographic variation in male sexual signals in Strawberry Poison Frogs (Dendrobates pumilio). Ethology, 113, 825–837.CrossRefGoogle Scholar
  87. Pröhl, H., Koshy, R. A., Mueller, U. G., Rand, A. S., & Ryan, M. J. (2006). Geographic variation of genetic and behavioral traits in northern and southern túngara frogs. Evolution, 60, 1669–1679.PubMedGoogle Scholar
  88. Rambaut, A., & Drummond, A. J. (2007). Tracer v. 1.5. [http://beast.bio.ed.ac.uk/Tracer]. Accessed 04 May 2012.
  89. Ramos–Onsins, S. E., & Rozas, J. (2002). Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution, 19, 2092–2100.PubMedCrossRefGoogle Scholar
  90. Ribas, C. C., Aleixo, A., Nogueira, A. C. R., Miyaki, C. Y., & Cracraft, J. (2011). A palaeobiogeographic model for biotic diversification within Amazonia over the past three million years. Proceedings of the Royal Society B, 279, 681–689.PubMedCrossRefGoogle Scholar
  91. Rosen, D. E. (1978). Vicariant patterns and historical explanation in biogeography. Systematic Zoology, 27, 159–188.CrossRefGoogle Scholar
  92. Rossetti, D. F., de Toledo, P. M., & Góes, A. M. (2005). New geological framework for Western Amazonia (Brazil) and implications for biogeography and evolution. Quaternary Research, 63, 78–89.CrossRefGoogle Scholar
  93. Ryan, M. J., Rand, A. S., & Weigt, L. A. (1996). Allozyme and advertisement call variation in the túngara frog, Physalaemus pustulosus. Evolution, 50, 2435–2453.CrossRefGoogle Scholar
  94. Santini, F., Miglietta, M. P., & Faucci, A. (2012). Where are we now? An introduction to a special issue on speciation. Evolutionary Biology, 39, 141–147.CrossRefGoogle Scholar
  95. Santos, J. C., Coloma, L. A., Summers, K., Caldwell, J. P., Ree, R., & Cannatella, D. C. (2009). Amazonian amphibian diversity is primarily derived from Late Miocene Andean lineages. PLoS Biology, 7, e1000056.CrossRefGoogle Scholar
  96. Santos, S., Hrbek, T., Farias, I. P., Schneider, H., & Sampaio, I. (2006). Population genetic structuring of the king weakfish, Macrodon ancylodon (Sciaenidae), in Atlantic coastal waters of South America: Deep genetic divergence without morphological change. Molecular Ecology, 15, 4361–4373.PubMedCrossRefGoogle Scholar
  97. Schneider, S., & Excoffier, L. (1999). Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: Application to human mitochondrial DNA. Genetics, 152, 1079–1089.PubMedGoogle Scholar
  98. Sequeira, F., Sodré, D., Ferrand, N., Bernardi, J., Sampaio, I., Schneider, H., et al. (2011). Hybridization and massive mtDNA unidirectional introgression between the closely related Neotropical toads Rhinella marina and R. schneideri inferred from mtDNA and nuclear markers. BMC Evolutionary Biology, 11, 264.PubMedCrossRefGoogle Scholar
  99. Silva, M. N. F., & Patton, J. L. (1998). Molecular phylogeography and the evolution and conservation of mammals. Molecular Ecology, 7, 475–486.PubMedCrossRefGoogle Scholar
  100. Simões, P. I. (2010). Diversificação do complexo Allobates femoralis (Anura, Dendrobatidae) em florestas da Amazônia brasileira: desvendando padrões atuais e históricos. PhD thesis. Manaus: Instituto Nacional de Pesquisas da Amazônia.Google Scholar
  101. Simões, P. I., Lima, A. P., Magnusson, W. E., Hödl, W., & Amézquita, A. (2008). Acoustic and morphological differentiation in the frog Allobates femoralis: Relationships with the Upper Madeira River and other potential geological barriers. Biotropica, 40, 607–614.CrossRefGoogle Scholar
  102. Sioli, H. (1984). The Amazon: Limnology and landscape ecology of a mighty tropical river and its basin. Dordrecht: Dr W. Junk Publisher.Google Scholar
  103. Smouse, P. E., Long, J. C., & Sokal, R. R. (1986). Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Systematic Zoology, 35, 727–732.CrossRefGoogle Scholar
  104. Solomon, S. E., Bacci, M., Martins, J., Vinha, G. G., & Mueller, U. G. (2008). Paleodistributions and comparative molecular phylogeography of leafcutter ants (Atta spp.) provide new insight into the origins of Amazonian diversity. PLoS ONE, 3, e2738.PubMedCrossRefGoogle Scholar
  105. Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595.PubMedGoogle Scholar
  106. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.PubMedCrossRefGoogle Scholar
  107. Telles, M. P. C., Silva, R. S. M., Chaves, L. J., Coelho, A. S. G., & Diniz–Filho, J. A. F. (2001). Divergência entre subpopulações de cagaiteira (Eugenia dysenterica) em resposta a padrões edáficos e distribuição espacial. Pesquisa Agropecuária Brasileira, 36, 1387–1394.CrossRefGoogle Scholar
  108. Templeton, A. R., Crandall, K. A., & Sing, C. F. (1992). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132, 619–633.PubMedGoogle Scholar
  109. Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). Improved sensitivity of profile searches through the use of sequence weights and gap excision. Computer Applications in the Biosciences, 10, 19–29.PubMedGoogle Scholar
  110. Tsuji-Nishikido, B. M., Kaefer, I. L., Freitas, F. C., Menin, M., & Lima, A. P. (2012). Significant but not diagnostic: Differentiation through morphology and calls in the Amazonian frogs Allobates nidicola and A. masniger. Herpetological Journal, 22, 105–114.Google Scholar
  111. Turmelle, A. S., Kunz, T. H., & Sorenson, M. D. (2011). A tale of two genomes: contrasting patterns of phylogeographic structure in a widely distributed bat. Molecular Ecology, 20, 357–375.PubMedCrossRefGoogle Scholar
  112. Vences, M., Kosuch, J., Lötters, S., Widmer, A., Jungfer, K., Köhler, J., et al. (2000). Phylogeny and classification of Poison Frogs (Amphibia: Dendrobatidae), based on mitochondrial 16S and 12S ribosomal RNA gene sequences. Molecular Phylogenetics and Evolution, 15, 34–40.PubMedCrossRefGoogle Scholar
  113. Vences, M., Thomas, M., Meijden, A., Chiari, Y., & Vieites, D. R. (2005). Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Frontiers in Zoology, 2, 5.PubMedCrossRefGoogle Scholar
  114. Vences, M., & Wake, D. B. (2007). Speciation, species boundaries and phylogeography of amphibians. In H. H. Heatwole & M. Tyler (Eds.), Amphibian biology. Volume 6: Systematics (pp. 2613–2669). Chipping Norton: Surrey Beatty & Sons.Google Scholar
  115. Verdade, V. K., & Rodrigues, M. T. (2007). Taxonomic review of Allobates (Anura, Aromobatidae) from the Atlantic Forest, Brazil. Journal of Herpetology, 41, 566–580.CrossRefGoogle Scholar
  116. Vieites, D. R., Wollenberg, K. C., Adreone, F., Köhler, J., Glaw, F., & Vences, M. (2009). Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences, 106, 8267–8272.CrossRefGoogle Scholar
  117. Wallace, A. R. (1852). On the monkeys of the Amazon. Proceedings of the Zoological Society of London, 20, 107–110.Google Scholar
  118. West-Eberhard, M. J. (1989). Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics, 20, 249–278.CrossRefGoogle Scholar
  119. Wiens, J. J. (2007). Species delimitation: New approaches for discovering diversity. Systematic Biology, 56, 875–878.PubMedCrossRefGoogle Scholar
  120. Wiens, J. J. (2008). Systematics and herpetology in the age of genomics. BioScience, 58, 297–307.CrossRefGoogle Scholar
  121. Wiley, E. O. (1978). The evolutionary species concept reconsidered. Systematic Zoology, 27, 17–26.CrossRefGoogle Scholar
  122. Wright, S. (1951). The genetical structure of populations. Annals of Human Genetics, 15, 323–354.Google Scholar
  123. Wycherley, J., Doran, S., & Beebee, T. J. C. (2002). Male advertisement call characters as phylogeographical indicators in European water frogs. Biological Journal of the Linnean Society, 77, 355–365.CrossRefGoogle Scholar
  124. Zeisset, I., & Beebee, T. J. C. (2008). Amphibian phylogeography: a model for understanding historical aspects of species distributions. Heredity, 101, 109–119.PubMedCrossRefGoogle Scholar
  125. Zhang, D. X., & Hewitt, G. M. (2003). Nuclear DNA analyses in genetic studies of populations: Practice, problems and prospects. Molecular Ecology, 12, 563–584.PubMedCrossRefGoogle Scholar
  126. Zink, R. M., & Barrowclough, G. F. (2008). Mitochondrial DNA under siege in avian phylogeography. Molecular Ecology, 17, 2107–2121.PubMedCrossRefGoogle Scholar
  127. Zink, R. M., Blackwell-Rago, R. C., & Ronquist, F. (2000). The shifting roles of vicariance in biogeography. Proceedings of the Royal Society B, 267, 497–503.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Igor L. Kaefer
    • 1
  • Bruno M. Tsuji-Nishikido
    • 2
  • Edvaldo P. Mota
    • 2
  • Izeni P. Farias
    • 2
  • Albertina P. Lima
    • 1
  1. 1.Programa de Pós-Graduação em EcologiaInstituto Nacional de Pesquisas da AmazôniaManausBrazil
  2. 2.Instituto de Ciências BiológicasUniversidade Federal do AmazonasManausBrazil

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