Advertisement

Evolutionary Ecology

, Volume 32, Issue 2–3, pp 191–214 | Cite as

Spatial and environmental correlates of intraspecific morphological variation in three species of passerine birds from the Purus–Madeira interfluvium, Central Amazonia

  • Fernando Henrique Teófilo de Abreu
  • Juliana Schietti
  • Marina Anciães
Original Paper

Abstract

Biogeographic studies in Amazonia typically describe biodiversity across interfluvia, rarely within them, where geographic variability in morphological traits might be observed. We tested for intraspecific phenotypic variation in three bird species within the Purus–Madeira interfluvium (Central Amazon) and whether phenotypes were correlated with environmental heterogeneity or geographic distance among sites. We compared coloration indexes derived from reflectance spectra and morphometrics of up to five adult individuals of each sex among 11 sites within the interfluvium and contrasted them with proxies for geographic distance and environmental variation (tree basal area and bird community). Environmental heterogeneity was minimally spatially autocorrelated, and there were no obvious geographical barriers to dispersal in the study region. The null hypothesis was that we would see either no phenotypic variation or random variation that was not explained by the tested variables. Half of the cases analyzed showed intraspecific morphological variation. Coloration varied more frequently than morphometrics, and color was better explained by environmental heterogeneity, particularly in males, whereas brightness also varied with geographic distance. Geographic distance explained the only case of variation in morphometrics. Our results indicate that coloration, particularly plumage brightness, is more labile than morphometric traits and that plumage color might be under stronger effects of local adaptation than brightness, which also seems to be under effects of neutral drift and gene flow among populations. Higher frequencies of association between male coloration and the environment suggest a role of non-arbitrary mechanisms of sexual selection on the expression of male phenotypes, whereas arbitrary intersexual selection might explain the randomly distributed variation that is not explained by environmental heterogeneity or geographic distance. We revealed intraspecific phenotypic variation in a spatial extent usually not considered in biogeographic studies in the Amazon and demonstrate that both local adaptation and neutral drift are important to explain intraspecific trait diversification at this geographical scale.

Keywords

Arbitrary preferences Coloration Neotropics Phenotypic variation Suboscines Sensory drive 

Notes

Acknowledgements

We are grateful to I. Kaefer, P. Simões, S. Borges, R. Cintra, F. Werneck and two anonymous referees for helpful comments on the manuscript and to A. Lima, W. Magnuson, M. J. Fortin and A. Stow for helpful sampling design suggestions. Centro Nacional de Pesquisa para Conservação das Aves Silvestres—CEMAVE (Number: 3245/3) and Instituto Chico Mendes de Conservação da Biodiversidade—ICMBio (Number: 5873-1) granted permits, and Fundação de Amparo à Pesquisa do Estado do Amazonas (PRONEX/FAPEAM/CNPQ 003/2009 to MA); Conselho Nacional de Desenvolvimento Científico e Tecnológico (UNIVERSAL—MCTI/CNPq 471092/2012-6 to MA); PRONEX/FAPEAM (1600/2006 to W. Magnusson), Hidroveg Universal CNPq (473308/2009-6), Centre for Amazonian Biodiversity Studies (INCT CENBAM), The Large Scale Biosphere–Atmosphere Experiment (LBA) and CAPES (fellowship to FHTA) funded the research. We thank the curators and collection managers at Instituto Nacional de Pesquisas da Amazônia (INPA) and the Museu Paraense Emilio Goeldi (MPEG) for access to specimens. The Brazilian Biodiversity Research Programme (PPBio) offered logistical support, and T. Emilio shared data on palm plant species and soil. We thank F. Assunção, A. Sousa, M. Bosholn, N. Soto, H. Santana, E. Dantas, S. Pereira, R. Dário, J. Capurucho and G. Leite for field assistance.

Supplementary material

10682_2018_9929_MOESM1_ESM.docx (909 kb)
Supplementary material 1 (DOCX 908 kb)

References

  1. Akaike H (1973) Information theory and the maximum likelihood principle in 2nd International Symposium on Information Theory (B.N. Petrov and F. Cs ä ki, eds.). Akademiai Ki à do, BudapestGoogle Scholar
  2. Amézquita A, Lima AP, Jehle R, Castellanos L, Ramos O, Crawford AJ, Gasser H, Hödl W (2009) Calls, colors, shape, and genes: a multi-trait approach to the study of geographic variation in the Amazonian frog Allobates femoralis. Biol J Linn Soc 98:826–838CrossRefGoogle Scholar
  3. Anciães M, Prum R (2008) Manakin display and visiting behavior: a comparative test of sensory drive. Anim Behav 75:783–790CrossRefGoogle Scholar
  4. Anciães M, Durães R, Cerqueira MC, Fortuna J, Sohn N, Cohn-Haft M, Farias IP (2009) Diversidade de piprídeos (Aves: pipridae) amazônicos: seleção sexual, ecologia e evolução. Oecol Bras 13:165–189CrossRefGoogle Scholar
  5. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  6. Andersson S (1999) Morphology of UV reflectance in a Whistling-Thrush: implications for the study of structural color signalling in birds. J Avian Biol 30:193–204CrossRefGoogle Scholar
  7. Andersson S (2000) Efficacy and content in avian color signals. In: Espmark Y, Amundsen T, Rosenqvist G (eds) Animal signals: signalling and signal design in animal communication. Tapir Academic, Trondheim, pp 47–60Google Scholar
  8. Badyaev AV, Hill GE (2003) Avian sexual dichromatism in relation to phylogeny and ecology. Annu Rev Ecol Evol Syst 34:27–49CrossRefGoogle Scholar
  9. Bates JM (2001) Avian diversification in Amazonia: evidence for historical complexity and a vicariance model for a basic diversification pattern. In: Diversidade Biológica e Cultural da Amazônia (Vieira, I., M. A. D’Incao, J. M. C. da Silva and D. Oren), 119–138. Museu Paraense Emilio Goeldi, Belém, Pará, BrazilGoogle Scholar
  10. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol 57:289–300Google Scholar
  11. Bueno AS, Bruno RS, Pimentel TP, Sanaiotti TM, Magnusson WE (2012) The width of riparian habitats for understory birds in an Amazonian forest. Ecol Appl 22:722–734PubMedCrossRefGoogle Scholar
  12. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  13. Cadena CD, Cheviron ZA, Funk WC (2011) Testing the molecular and evolutionary causes of a “leapfrog” pattern of geographical variation in coloration. Evol Biol 24:402–414CrossRefGoogle Scholar
  14. Calsbeek R, Smith TB, Bardeleben C (2007) Intraspecific variation in Anolis sagrei mirrors the adaptive radiation of Greater Antillean anoles. Biol J Linn Soc 90:189–199CrossRefGoogle Scholar
  15. 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. Mol Phylogenet Evol 36:336–357CrossRefGoogle Scholar
  16. Cintra R, Cancelli J (2008) Effects of forest heterogeneity on occurrence and abundance of the scale-backed antbird, Hylophylax poecilinotus (Aves: Thamnophilidae), in the Amazon forest. Rev Bras Zool 25:630–639CrossRefGoogle Scholar
  17. Cintra BBL, Schietti J, Emillio T, Martins D, Moulatlet G, Souza P, Levis C, Quesada CA, Schöngart J (2013) Soil physical restrictions and hydrology regulate stand age and wood biomass turnover rates of Purus–Madeira interfluvial wetlands in Amazonia. Biogeosciences 10:7759–7774CrossRefGoogle Scholar
  18. Cohn-Haft M, Pacheco AMF, Bechtoldt CL, Torres MFNM, Fernandes AM, Sardelli CH, Macêdo IT (2007) Inventário ornitológico. p. 145-178. Em: Rapp Py-Daniel L, Deus CP, Henriques, A.L., Pimpão, D.M., Ribeiro, O.M. (orgs.). Biodiversidade do Médio Madeira: Bases científicas para propostas de conservação. INPA: ManausGoogle Scholar
  19. Cracraft J (1985) Historical biogeography and patterns of differentiation within the South American avifauna: areas of endemism. Ornithol Monogr 36:49–84CrossRefGoogle Scholar
  20. Creegan HP, Osborne PE (2005) Gap-crossing decisions of woodland songbirds in Scotland: an experimental approach. J Appl Ecol 42:678–687CrossRefGoogle Scholar
  21. Cuthill IC (2006) Color perception. In: Hill G, McGraw K (eds) Bird coloration. Harvard, Cambridge, pp 1–40Google Scholar
  22. Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85:407–415CrossRefGoogle Scholar
  23. Durães R (2009) Lek structure and male display repertoire of blue-crowned manakins in eastern ecuador. Condor 111:453–461CrossRefGoogle Scholar
  24. Emilio TLS (2007) Distribuição de Palmeiras (Areaceae) ao longo de gradientes ambientais no Baixo Interflúvio Purus–Madeira, Brasil. Dissertação de mestrado. Instituto Nacional de Pesquisas da Amazônia, ManausGoogle Scholar
  25. Emilio T, Quesada CA, Costa FRC et al (2013) Soil physical conditions limit palm and tree basal area in Amazonian forests. Plant Ecol Divers 7:215–229CrossRefGoogle Scholar
  26. Endler JA (1977) Geographic variation, speciation and clines. Princeton University Press, PrincetonGoogle Scholar
  27. Endler JA (1982) Pleistocene forest refuges: fact or fancy? In: Prance GT (ed) Biological diversification in the tropics. Columbia University Press, New York, pp 641–657Google Scholar
  28. Endler JA (1990) On the measurement and classification of color in studies of animal color patterns. Biol J Linn Soc 41:15–352CrossRefGoogle Scholar
  29. Endler JA (1991) Interactions between predators and prey. In: Krebs JA, Davies NB (eds) Behavioural ecology: an evolutionary approach, 3rd edn. Blackwell Scientific, Oxford, pp 169–196Google Scholar
  30. Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:125–153CrossRefGoogle Scholar
  31. Endler JA (1993) The color of light in forests and its implications. Ecol Monogr 63:1–27CrossRefGoogle Scholar
  32. Endler JA, Basolo AL (1998) Sensory ecology, receiver biases and sexual selection. Tree 13:415–420PubMedGoogle Scholar
  33. Endler J, Houde AE (1995) Geographic variation in female preferences for male traits in Poecilia reticulata. Evolution 49:456–468PubMedCrossRefGoogle Scholar
  34. Endler JA, Mclellan T (1988) The processes of evolution: toward a newer synthesis. Annu Rev Ecol Evol Syst 19:395–421CrossRefGoogle Scholar
  35. Endler JA, Théry M (1996) Interacting effects of lek placement, display behavior, ambient light, and color patterns in three neotropical forest-dwelling birds. Am Nat 148:421–452CrossRefGoogle Scholar
  36. Engen S, Sæther B (2016) Phenotypic evolution by distance in fluctuating environments: the contribution of dispersal, selection and random genetic drift. Theor Popul Biol 109:16–27PubMedCrossRefGoogle Scholar
  37. Faria ES (2014) Evolução da variação intraespecífica em cantos de anúncio de Allobates sp. Dissertação de mestrado. Instituto Nacional de Pesquisas da Amazônia, ManausGoogle Scholar
  38. Fearnside PM, Graça PMLA (2009) BR-319: a rodovia Manaus-Porto Velho e o impacto potencial de conectar o arco de desmatamento à Amazônia central. NCN 12:19–50Google Scholar
  39. Fernandes AM (2013) Fine-scale endemism of Amazonian birds in a threatened landscape. Biodivers Conserv 22:2683–2694CrossRefGoogle Scholar
  40. Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, OxfordCrossRefGoogle Scholar
  41. Goldberg EE, Lande R (2006) Ecological and reproductive character displacement on an environmental gradient. Evolution 60:1344–1357PubMedGoogle Scholar
  42. Gomez D (2006) AVICOL, a program to analyse spectrometric data. Last update October 2011. http://sites.google.com/site/avicolprogram/or from the author at dodogomez@yahoo.fr
  43. Gomez D, Théry M (2004) Influence of ambient light on the evolution of color signals: comparative analysis of a Neotropical rainforest bird community. Ecol Lett 7:279–284CrossRefGoogle Scholar
  44. Gotmark F (1993) Conspicuous coloration in male birds is favoured by predation in some species and disfavoured in others. Proc R Soc Lond B Biol Sci 253(143):146Google Scholar
  45. Grant BR, Grant PR (1993) Evolution of Darwin’s finches caused by a rare climatic event. Proc R Soc Lond B Biol Sci 251:111–117CrossRefGoogle Scholar
  46. Grant PR, Grant BR (2000) Non-random fitness variation in two populations of Darwin’s finches. Proc R Soc Lond B Biol Sci 267:131–138CrossRefGoogle Scholar
  47. Haffer J (1969) Speciation in amazonian forest birds. Sci New Ser 165:3889Google Scholar
  48. Haffer J (1997) Alternative models of vertebrate speciation in Amazonia: an overview. Biodivers Conserv 6:451–476CrossRefGoogle Scholar
  49. Harris EF, Smith RN (2009) Accounting for measurement error: a critical but often overlooked process. Arch Oral Biol 1:107–117CrossRefGoogle Scholar
  50. Hegna RH, Saporito RA, Donnelly MA (2012) Not all colors are equal: predation and color polytypism in the aposematic poison frog Oophaga pumilio. Evol Ecol 27:831–846CrossRefGoogle Scholar
  51. Heindl M, Winkler H (2003a) Interacting effects of ambient light and plumage color patterns in displaying Wire-tailed Manakins (Aves, Pipridae). Behav Ecol Sociobiol 53:153–162Google Scholar
  52. Heindl M, Winkler H (2003b) Vertical lek placement of forest-dwelling manakin species (Aves, Pipridae) is associated with vertical gradients of ambient light. Biol J Linn Soc 80:647–658CrossRefGoogle Scholar
  53. Hellmayr CE (1929) Catalogue of the birds of the Americas and the adjacent Islands in field museum of natural history. Science 66:153–154Google Scholar
  54. Hill EG, Mcgraw KJ (2006) Bird coloration: function and evolution, vol II. Harvard University Press, CambridgeGoogle Scholar
  55. Hoagstrom CW, Berry CR (2008) Morphological diversity among fishes in a Great Plains river drainage. Hydrobiologia 596:367–386CrossRefGoogle Scholar
  56. Hsu YC, Shaner PJ, Chang CI, Ke L, Kao SJ (2014) Trophic niche width increases with bill-size variation in a generalist passerine: a test of niche variation hypothesis. J Anim Ecol 83:450–459PubMedCrossRefGoogle Scholar
  57. IBGE (1997) Recursos naturais e meio ambiente: uma visão do Brasil. Instituto Brasileiro de Geografia e Estatística. Rio de Janeiro 2:208Google Scholar
  58. Isler ML, Whitney BM (2011) Species limits in antbirds (Thamnophilidae): the Scale-backed Antbird (Willisornis poecilinotus) complex. J Wilson Ornithol 123:1–14CrossRefGoogle Scholar
  59. Johnson EI, Wolfe JD, Ryder TB, Pyle P (2011) Modifications to a molt-based ageing system proposed by Wolfe et al. 2010. J Field Ornithol 82:421–423Google Scholar
  60. Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38CrossRefGoogle Scholar
  61. Kirwan GM, Green G (2011) Cotingas and manakins. Princeton University Press, PrincetonGoogle Scholar
  62. Lee K, Shaner PL, Lin Y, Lin S (2016) Geographic variation in advertisement calls of a Microhylid frog—testing the role of drift and ecology. Ecol Evol 6:3289–3298PubMedPubMedCentralCrossRefGoogle Scholar
  63. Levin SA (1992) The problem of pattern and scale in ecology. Ecology 73:1943–1967CrossRefGoogle Scholar
  64. Lundberg A, Alatalo RV (1992) The pied flycatcher. Poyser, LondonGoogle Scholar
  65. Maan ME, Seehausen O (2011) Ecology, sexual selection and speciation. Ecol Lett 14:591–602PubMedCrossRefGoogle Scholar
  66. MacArthur RH, Pianka EE (1966) On optimal use of a patchy environment. Am Nat 100:603–609CrossRefGoogle Scholar
  67. Magnusson WE, Lima AP, Luizão R, Luizão F, Costa FRC, Castilho CV, Kinupp V (2005) RAPELD: a modification of the Gentry method for biodiversity surveys in long-term ecological research sites. Biota Neotrop 5:19–24CrossRefGoogle Scholar
  68. Maia R, Eliason CM, Bitton PP, Doucet SM, Shawkey MD (2013a) Pavo: an R package for the analysis, visualization and organization of spectral data. Methods Ecol Evol 4:906–913Google Scholar
  69. Maia R, Dustin RR, Matthew DS (2013b) Key ornamental innovations facilitate diversification in an avian radiation. Proc Natl Acad Sci USA 110:10687–10692PubMedPubMedCentralCrossRefGoogle Scholar
  70. Marchetti K (1993) Dark habitats and bright birds illustrate the role of the environment in species divergence. Nature 362:149–152CrossRefGoogle Scholar
  71. Marciente R (2012) Efeito da obstrução gerada pela densidade da vegetação sub-bosque sobre morcegos frugívoros e animalívoros catadores (Chiroptera: Phyllostomidae) na Amazônia Central. Dissertação de Mestrado. Instituto Nacional de Pesquisas da Amazônia. ManausGoogle Scholar
  72. Martin MD, Mendelson TC (2014) Changes in sexual signals are greater than changes in ecological traits in a dichromatic group of fishes. Evolution 68:3618–3628PubMedCrossRefGoogle Scholar
  73. Martins DL, Schietti J, Feldpausch TR, Luizão FJ, Phillips OL, Andrade A, Castilho CV, Laurance SG, Oliveira A, Amaral IL, Toledo JJ, Lugli LF, Pinto JLPV, Mendoz EMO, Quesada CA (2014) Soil-induced impacts on forest structure drive coarse woody debris stocks across central Amazonia. Plant Ecol Div 8:229–241CrossRefGoogle Scholar
  74. Mayr E (1947) Ecological factors in speciation. Evolution 1:263–288CrossRefGoogle Scholar
  75. Mcnaught MK, Owens IPF (2002) Interspecific variation in plumage color among birds: species recognition or light environment? J Evol Biol 15:505–514CrossRefGoogle Scholar
  76. Menger JS (2011) Fatores Determinantes Da Distribuição De Aves No Interflúvio Purus-Madeira. Dissertação de Mestrado. Instituto Nacional de Pesquisas da Amazônia. ManausGoogle Scholar
  77. Moulatlet GM, Costa FRC, Rennó CD, Emilio T, Schietti J (2014) Local hydrological conditions explain floristic composition in lowland Amazonian forests. Biotropica 46:395–403CrossRefGoogle Scholar
  78. Mullen P, Pohland G (2007) Studies on UV reflection in feathers of some 1000 bird species: are UV-peaks in feathers correlated with VS/UVS cones? Ibis 150:59–68CrossRefGoogle Scholar
  79. Naka LN, Bechtoldt CL, Henriques LMP, Brumfield RT (2012) The role of physical barriers in the location of avian suture zones in the guiana shield, northern amazonia. Am Nat 179:115–132CrossRefGoogle Scholar
  80. Nokelainen O, Valkonen J, Lindstedt C, Mappes J (2014) Changes in predator community structure shifts the efficacy of two warning signals in Arctiid moths. J Anim Ecol 83:598–605PubMedCrossRefGoogle Scholar
  81. Ödeen A, Håstad O (2013) The phylogenetic distribution of ultraviolet sensitivity in birds. BMC Evol Biol 13:36PubMedPubMedCentralCrossRefGoogle Scholar
  82. Owens IPF, Hartley IR (1998) Sexual dimorphism in birds: why are there so many diferent forms of dimorphism? Proc R Soc Lond B Biol Sci 265:397–407CrossRefGoogle Scholar
  83. Padial JM, Miralles A, De la Riva I, Vences M (2010) The integrative future of taxonomy. Front Zool 7:16PubMedPubMedCentralCrossRefGoogle Scholar
  84. Patton JL, da Silva MNF (1998) Rivers, refuges, and ridges: the geography of speciation of Amazonian mammals. In: Haward DJ, Berlocher ST (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 202–213Google Scholar
  85. Peterson AT (1996) Geographic variation in sexual dichromatism in birds. Bull Br Orn Club 116:156–172Google Scholar
  86. Price T (2008) Speciation in Birds. Roberts and Company Publishers, Greenwood VillageGoogle Scholar
  87. Prum RO (1997) Phylogenetic tests of alternative intersexual selection mechanisms: trait macroevolution in a polygynous clade (Aves: Pipridae). Am Nat 149:668–692CrossRefGoogle Scholar
  88. Prum RO (2010) The Lande–Kirpatrick mechanism is the null model of intersexual selection: implications for meaning, honesty, and design of intersexual signals. Evolution 64:3085–3100PubMedCrossRefGoogle Scholar
  89. Prum RO (2012) Aesthetic evolution by mate choice: Darwin’s really dangerous idea. Philos Trans R Soc Lond B Biol Sci 367:2253–2265PubMedPubMedCentralCrossRefGoogle Scholar
  90. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  91. Ranta E, Kaitala V, Lundberg P (1998) Population variability in space and time: the dynamics of synchronous population fluctuations. Oikos 83:376–382CrossRefGoogle Scholar
  92. Ribas CC, Aleixo A, Nogueira ACR, Miyaki CY, Cracraf J (2012) A palaeobiogeographic model for biotic diversification within Amazonia over the past three million years. Proc R Soc Lond Ser B Biol sci 279:681–689CrossRefGoogle Scholar
  93. Ribeiro AM, Lloyd P, Dean JRJ, Brow M, Bowie RCK (2014) The ecological and geographic context of morphological and genetic divergence in an understory-dwelling bird. PLoS ONE 9:85903CrossRefGoogle Scholar
  94. Ryder TB, Durães R (2005) It’s not easy being Green: using molt and morphological criteria to age and sex Green-plumage manakin (Aves: Pipridae). Ornitología Neotropical 16:481–491Google Scholar
  95. Safran RJ, McGraw KJ (2004) Plumage coloration, not length or symmetry of tail-streamers, is a sexually selected trait in North American barn swallows. Behav Ecol 15:455–461CrossRefGoogle Scholar
  96. Safran RJ, Flaxman SM, Kopp M, Irwin DE, Briggs D, Evans MR, Funk WC, Gray DA, Hebets EA, Seddon N, Scordato E, Symes LB, Tobias JA, Toews DPL, Uy JAC (2012) A robust new metric of phenotypic distance to estimate and compare multiple trait differences among populations. Curr Zool 58:426–439CrossRefGoogle Scholar
  97. Schietti J, Martins D, Emilio T, Souza PF, Levis C, Baccaro FB, Pinto JLPDV, Moulatlet GM, Stark SK, Sarmento K, de Araújo RNO, Costa FRC, Schöngart J, Quesada CA, Saleska SR, Tomasella J, Magnusson WE (2016) Forest structure along a 600 km transect of natural disturbances and seasonality gradients in central-southern Amazonia. J Ecol 104:1335–1346CrossRefGoogle Scholar
  98. Schluter D (1998) Ecological causes of speciation. In: Howard D, Berlocher S (eds) Endless forms: species and speciation. Oxford University Press, Oxford, pp 114–129Google Scholar
  99. Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380PubMedCrossRefGoogle Scholar
  100. Schluter D (2009) Evidence for ecological speciation and its alternative. Science 323:737–741PubMedCrossRefGoogle Scholar
  101. Schulenberg TS (1983) Foraging behaviour, ecomorphology and systematic of some antshrikes (Formicariidae: Thamnomanes). Wilson Bull 95:505–521Google Scholar
  102. Seddon N, Merrill RM, Tobias JA (2008) Sexually selected traits predict patterns of species richness in a diverse clade of suboscine birds. Am Nat 171:620–631PubMedCrossRefGoogle Scholar
  103. Seddon N, Botero CA, Tobias JA, Dunn PO, Macgregor HE, Rubenstein DR, Uy JA, Weir JT, Whittingham LA, Safran RJ (2013) Sexual selection accelerates signal evolution during speciation in birds. Proc R Soc Lond B Biol Sci 280:20131065CrossRefGoogle Scholar
  104. Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, Miyagi R, van der Sluijs I, Schneider MV, Maan ME, Tachida H (2008) Speciation through sensory drive in cichlid fish. Nature 455:620–627PubMedCrossRefGoogle Scholar
  105. Sick H (1997) Ornitologia brasileira. Editora Nova Fronteira, Rio de JaneiroGoogle Scholar
  106. Siddiqi A, Cronin TW, Loew ER, Vorobyev M, Summers K (2004) Interspecific and intraspecific views of color signals in the strawberry poison dart frog Dendrobates pumilio. J Exp Biol 207:2471–2485PubMedCrossRefGoogle Scholar
  107. Sokal RR, Rohlf FJ (1995) Biometry. The principles and practice of statistics in biological research. W. H. Freeman, New YorkGoogle Scholar
  108. Souza PF (2012) Florística, distribuição e diversidade beta da Comunidade arbórea ao longo do gradiente ambiental hídrico em uma floresta de terra firme no interflúvio Purus-Madeira, Amazônia Central. Dissertação de mestrado. Instituto Nacional de Pesquisas da Amazônia, ManausGoogle Scholar
  109. Sun K, Luo L, Kimball RT, Wei X, Jin L, Jiang T, Li G, Feng J (2013) Geographic variation in the acoustic traits of greater horseshoe bats: testing the importance of drift and ecological selection in evolutionary processes. PLoS ONE 8:1–11CrossRefGoogle Scholar
  110. Tobias JA, Aben J, Brumfield RT (2010) Song divergence by sensory drive in amazonian birds. Evolution 64:2820–2839PubMedGoogle Scholar
  111. Tobias JA, Brawn JD, Brumfield RT, Derryberry EP, Kirschel ANG, Seddon N (2012) The importance of Neotropical Suboscine birds as study systems in ecology and evolution. Ornitol Neotrop 23:259–272Google Scholar
  112. Uy JAC, Endler JA (2004) Modification of the visual background increases the conspicuousness of golden-collared manakin displays. Behav Ecol 15:1003–1010CrossRefGoogle Scholar
  113. Uy JA, Stein AC (2007) Variable visual habitats may influence the spread of colorful. J Evol Biol 20:1847–1858PubMedCrossRefGoogle Scholar
  114. Uy JAC, Moyle RG, Filardi CE (2008) Plumage color and song differences mediate species recognition between incipient flycatcher species of the solomon islands. Evolution 63:153–164PubMedCrossRefGoogle Scholar
  115. Vorobyev M, Osorio D (1998) Receptor noise as a determinant of color thresholds. Proc R Soc Lond Ser B Biol Sci 265:351–358CrossRefGoogle Scholar
  116. Vorobyev M, Brandt R, Peitsch D, Laughlin SB, Menzel R (2001) Color thresholds and receptor noise: behavior and physiology compared. Vis Res 41:639–653PubMedCrossRefGoogle Scholar
  117. Wallace AR (1858) On the tendency of species to form varieties; and on the perpetuation of the varieties and species by natural means of selection. J Proc Linn Soc Lond 2:53–62Google Scholar
  118. Wang IJ, Shaffer HB (2008) Rapid color evolution in an aposematic species: a phylogenetic analysis of color variation in the strikingly polymorphic strawberry poison-dart frog. Evolution 62:2742–2759PubMedCrossRefGoogle Scholar
  119. Wang IJ, Summers K (2010) Genetic structure is correlated with phenotypic divergence rather than geographic isolation in the highly polymorphic strawberry poison-dart frog. Mol Ecol 19:447–458PubMedCrossRefGoogle Scholar
  120. Weir JT, Faccio MS, Pulido-Santacruz P, Barrera-Guzmán AO, Aleixo A (2015) Hybridization in headwater regions, and the role of rivers as drivers of speciation in Amazonian birds. Evolution 69:1823–1834PubMedCrossRefGoogle Scholar
  121. WilIis EO (1968) Taxonomy and behavior of Pale-faced Antbirds. Auk 85:253–264CrossRefGoogle Scholar
  122. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159PubMedPubMedCentralGoogle Scholar
  123. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedPubMedCentralGoogle Scholar
  124. Ximenes AC (2008) Mapas auto-organizáveis para a identificação de ecorregiões no interflúvio Purus-Madeira: uma abordagem da biogeografia ecológica. Dissertação. Instituto Nacional de Pesquisas Espaciais: São José dos CamposGoogle Scholar
  125. Zahavi A, Zahavi A (1997) The handcap principle. Oxford University Press, OxfordGoogle Scholar
  126. Zimmer KJ, Isler ML (2003) Family Thamnophilidae (Typical Antbirds). In: Del Hoyo J, Elliott A, Christie DA (eds) Handbook of the birds of the world, vol 8. Lynx Edicions, Barcelona, pp 448–681Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Fernando Henrique Teófilo de Abreu
    • 1
    • 3
  • Juliana Schietti
    • 1
    • 2
  • Marina Anciães
    • 1
    • 2
    • 3
  1. 1.Programa de Pós-Graduação em EcologiaInstituto Nacional de Pesquisas da Amazônia (INPA)ManausBrazil
  2. 2.Coordenação de Biodiversidade (COBIO)Instituto Nacional de Pesquisas da Amazônia (INPA)ManausBrazil
  3. 3.Laboratório de Evolução e Comportamento Animal (LABECA)Instituto Nacional de Pesquisas da Amazônia (INPA)ManausBrazil

Personalised recommendations