Journal of Ornithology

, Volume 159, Issue 2, pp 379–388 | Cite as

Vocal variation in relation to genetic structure in an Atlantic forest woodcreeper (Xiphorhynchus fuscus): evolutionary and taxonomic implications

  • Natalia C. García
  • Luciano N. Naka
  • Gustavo S. Cabanne
Original Article
First Online:
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Revised:
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Abstract

The analysis of intra-specific geographical variation is central to the study of the evolutionary and speciation processes, providing insights into the mechanisms leading to current diversity patterns. In the last decades, analyses of within-species variation moved its focus from phenotypic traits to the analysis of variation in genetic markers. Modern phylogeographic studies could be significantly improved by including detailed phenotypic variation analyses, allowing a better understanding of the biological processes driving similar or opposing patterns in phenotype and molecular markers differentiation. Here, we analyze vocal variation within the Lesser Woodcreeper (Xiphorhynchus fuscus), an Atlantic forest suboscine passerine, in relation to the genetic lineages previously described for this species. Our results show that two of the genetic clades within this species have their own vocal type, while the other two lineages share a common type. This finding supports the notion that the same events which modeled part of the genetic structure within X. fuscus also led to the accumulation of vocal differences. It also provides evidence to support the elevation of the subspecies atlanticus to a species-level taxon.

Keywords

Bird song Intra-specific variation Neotropics Suboscines Subspecies 

Zusammenfassung

Stimmliche Variation in Relation zur genetischen Struktur bei einer Baumsteigerart (Xiphorhynchus fuscus) atlantischer Wälder und ihre Bedeutung für Evolution und Taxonomie

Für Studien der Evolution und von Artbildungsprozessen ist die Untersuchung intraspezifischer geografischer Variation von zentraler Bedeutung und ermöglicht Rückschlüsse auf die Mechanismen, welche zu den derzeitigen Diversitätsmustern geführt haben. Bei Analysen innerartlicher Variation hat sich während der letzten Jahrzehnte der Schwerpunkt von phänotypischen Merkmalen zur Analyse der Variation genetischer Marker verlagert. Die Einbeziehung detaillierter Analysen phänotypischer Variation wäre ein signifikanter Gewinn für heutige phylogeografische Untersuchungen und würde zu einem besseren Verständnis der biologischen Prozesse führen, welche ähnliche oder entgegengesetzte Muster bei der Differenzierung phänotypischer und molekularer Marker entstehen lassen. Hier untersuchen wir die stimmliche Variation beim Blasskehl-Baumsteiger (Xiphorhynchus fuscus), einer suboszinen Singvogelart atlantischer Wälder, in Relation zu den bisher beschriebenen genetischen Abstammungslinien für diese Art. Unsere Ergebnisse zeigen, dass zwei der genetischen Kladen innerhalb der Art ihren eigenen Stimmtyp besitzen, während sich die zwei übrigen Abstammungslinien einen gemeinsamen Typ teilen. Dies bestätigt die Theorie, dass dieselben Ereignisse, welche Teile der genetischen Struktur innerhalb von X. fuscus geprägt haben, auch zur Herausbildung stimmlicher Unterschiede geführt haben. Außerdem dient dies als Beleg zur Untermauerung der Erhebung der Unterart atlanticus zu einem Taxon auf Artebene.

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Notes

Acknowledgements

We thank the editor and the two anonymous reviewers for their comments, which significantly improved previous versions of the manuscript. We thank the Macaulay Library (Cornell Laboratory of Ornithology), the Fonoteca Neotropical Jacques Vielliard (Museu de Zoologia “Adão José Cardoso”–Universidade Estadual de Campinas), and the Colección Nacional de Sonidos Naturales (Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”) for providing recordings. We also thank all sound recordists who collected the recordings we used (detailed in ESM Table S1), especially Glauco Pereira, Sidnei de Melo Dantas, and Roney Assis Souzsa, for sending their recordings upon our request. We thank Ana S. Barreira, who classified recordings into song types, for her help. This work was supported by the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina), the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT, Argentina), and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil)

Compliance with ethical standards

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Supplementary material

10336_2017_1509_MOESM1_ESM.xlsx (13 kb)
Supplementary material 1 (XLSX 12 kb)

References

  1. Becker PH (1982) The coding of species-specific characteristics in bird sounds. In: Kroodsma DE, Miller EH (eds) Acoustic communication in birds. Academic Press, New York, pp 214–252Google Scholar
  2. Behling H (2002) South and southeast Brazilian grassland during late quaternary times: a synthesis. Palaeogeogr Palaeocl 177:19–27CrossRefGoogle Scholar
  3. BirdLife International (2017) Species factsheet: Xiphorhynchus atlanticus. http://www.birdlife.org. Accessed 17 May 2017
  4. BirdLife International and NatureServe (2015) Bird species distribution maps of the world. BirdLife International/NatureServe, Cambridge/ArlingtonGoogle Scholar
  5. Bivand R, Lewin-Koh N (2016) Maptools: tools for reading and handling spatial objects. R package version 0.8-39. https://CRAN.R-project.org/package=maptools
  6. Cabanne GS, Santos FR, Miyaki CY (2007) Phylogeography of Xiphorhynchusfuscus (Passeriformes, Dendrocolaptidae): vicariance and recent demographic expansion in southern Atlantic forest. Biol J Linn Soc 91:73–84CrossRefGoogle Scholar
  7. Cabanne GS, d’Horta FM, Sari EH, Santos FR, Miyaki CY (2008) Nuclear and mitochondrial phylogeography of the Atlantic forest endemic Xiphorhynchusfuscus (Aves: Dendrocolaptidae): biogeography and systematics implications. Mol Phylogenetevol 49:760–773CrossRefGoogle Scholar
  8. Cabanne GS, Trujillo-Arias N, Calderón L, d’Horta FM, Miyaki CY (2014) Phenotypic evolution of an Atlantic Forest passerine (Xiphorhynchusfuscus): biogeographic and systematic implications. Biol J Linn Soc 113:1047–1066CrossRefGoogle Scholar
  9. Carnaval AC, Moritz C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest. J Biogeogr 35:1187–1201CrossRefGoogle Scholar
  10. Carnaval AC, Waltari E, Rodrigues MT, Rosauer D, VanDerWal J, Damasceno R, Prates I, Strangas M, Spanos Z, Rivera D, Pie MR, Firkowski CR, Bornschein MR, Ribeiro LF, Moritz C (2014) Prediction of phylogeographic endemism in an environmentally complex biome. Proc R Soc B-Biol Sci 281:20141461CrossRefGoogle Scholar
  11. Comitê Brasileiro de Registros Ornitológicos (2014) Listas das aves do Brasil. 11ª Edição. http://www.cbro.org.br
  12. Cracraft J (1983) Species concepts and speciation analysis. Curr Ornithol 1:159–187CrossRefGoogle Scholar
  13. De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886CrossRefPubMedGoogle Scholar
  14. Derryberry EP, Seddon N, Claramunt S, Tobias JA, Baker A, Aleixo A, Brumfield RT (2012) Correlated evolution of beak morphology and song in the Neotropical woodcreeper radiation. Evolution 66:2784–2797CrossRefPubMedGoogle Scholar
  15. Endler JA (1977) Geographic variation, speciation, and clines, vol 10. Princeton University Press, PrincetonGoogle Scholar
  16. Galindo Leal C, Câmara IdG (2003) The Atlantic Forest of South America: biodiversity status, threats, and outlook. Island Press, Washington D.C.Google Scholar
  17. García NC, Barreira AS, Kopuchian C, Tubaro PL (2014) Intraspecific and interspecific vocal variation in three Neotropical cardinalids (Passeriformes: Fringillidae) and its relationship with body mass. Emu 114:129–136Google Scholar
  18. García NC, Arrieta RS, Kopuchian C, Tubaro PL (2015) Stability and change through time in the dialects of a Neotropical songbird, the rufous-collared Sparrow. Emu 115:309–316CrossRefGoogle Scholar
  19. García NC, Barreira AS, Lavinia PD, Tubaro PL (2016) Congruence of phenotypic and genetic variation at the subspecific level in a Neotropical passerine. Ibis 158:844–856CrossRefGoogle Scholar
  20. Greig EI, Webster MS (2013) Spatial decoupling of song and plumage generates novel phenotypes between 2 avian subspecies. Behav Ecol 24:1004–1013CrossRefGoogle Scholar
  21. Remsen Jr. JV, Areta JI., Cadena CD, Claramunt S, Jaramillo S, Pacheco JF, Pérez-Emán J, Robbins MB, Stiles FG, Stotz DF, Zimmer KJ (2017) A classification of the bird species of South America. Version 22 April 2017. American Ornithologists’ Union, Chicago. http://www.museum.lsu.edu/~Remsen/SACCBaseline.htm
  22. Ledru MP, Rousseau DD, Cruz FW, Riccomini C, Karmann I, Martin L (2005) Paleoclimate changes during the last 100, 000 year from a record in the Brazilian Atlantic rainforest region and interhemispheric comparison. Quat Res 64:444–450CrossRefGoogle Scholar
  23. Lougheed SC, Campagna L, Dávila JA, Tubaro PL, Lijtmaer DA, Handford P (2013) Continental phylogeography of an ecologically and morphologically diverse Neotropical songbird Zonotrichia capensis. BMC Evol Biol 13:58CrossRefPubMedPubMedCentralGoogle Scholar
  24. Marantz CA, Aleixo A, Bevier LR, Patten MA (2003) Family Dendrocolaptidae (woodcreepers). In: del Hoyo J, Elliot A, Christie D (eds) Handbook of the birds of the world, vol 8. Broadbills to tapaculos. Lynx Edicions, Barcelona, pp 358–447Google Scholar
  25. Marler P (1957) Specific distinctiveness in the communication signals of birds. Behaviour 11:13–39CrossRefGoogle Scholar
  26. Miller MJ, Lelevier MJ, Bermingham E, Klicka JT, Escalante P, Winker K (2011) Phylogeography of the Rufous-tailed Hummingbird (Amazilia tzacatl). The Condor 113:806–816CrossRefGoogle Scholar
  27. Minns JC, Buzzetti DRC, Albano CG, Whittaker A, Grosset AE, Parrini E (2009) Birds of Brasil/Aves do Brasil. DVD-ROM. Aves Brasilis Editora, VinhedoGoogle Scholar
  28. Morton ES (1975) Ecological sources of selection on avian sounds. Am Nat 109:17–34CrossRefGoogle Scholar
  29. Naka LN, Bechtoldt CL, Herniques 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:E115–E132CrossRefPubMedGoogle Scholar
  30. Piacentini VQ (2015) Lista comentada das aves do Brasil pelo Comitê Brasileiro de Registros Ornitológicos. Rev Bras Ornitol 23:91–298Google Scholar
  31. Podos J, Warren PS (2007) The evolution of geographic variation in birdsong. Adv Stud Behav 37:403–458CrossRefGoogle Scholar
  32. Price T (2007) Speciation in birds. Roberts and Company, Greenwood VillageGoogle Scholar
  33. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  34. Remsen JV Jr (2005) Pattern, process, and rigor meet classification. Auk 122:403–413CrossRefGoogle Scholar
  35. Rheindt FE, Norman JA, Christidis L (2008) DNA evidence shows vocalizations to be a better indicator of taxonomic limits than plumage patterns in Zimmerius tyrant-flycatchers. Mol Phylogenet Evol 48:150–156CrossRefPubMedGoogle Scholar
  36. Riede T, Goller F (2014) Morphological basis for the evolution of acoustic diversity in oscine songbirds. Proc R Soc B: Biol Sci 281(1779):20132306CrossRefGoogle Scholar
  37. Seddon N (2005) Ecological adaptation and species recognition drives vocal evolution in neotropical suboscine birds. Evolution 59(1):200–215CrossRefPubMedGoogle Scholar
  38. Slabbekoorn H, Smith TB (2002) Bird song, ecology and speciation. Philos Trans R Soc B 357:493–503CrossRefGoogle Scholar
  39. Tubaro PL, Mahler B (1998) Acoustic frequencies and body mass in New World doves. Condor 100(1):54–61CrossRefGoogle Scholar
  40. Wilkins MR, Seddon N, Safran RJ (2013) Evolutionary divergence in acoustic signals: causes and consequences. Trends Ecol Evol 28:156–166CrossRefPubMedGoogle Scholar
  41. Winker K (2009) Reuniting genotype and phenotype in biodiversity research. Bioscience 59:657–665CrossRefGoogle Scholar
  42. Winker K (2010) Subspecies represent geographically partitioned variation, a gold mine of evolutionary biology, and a challenge for conservation. Ornithol Monogr 67:6–23CrossRefGoogle Scholar
  43. Zamudio KR, Bell RC, Mason NA (2016) Phenotypes in phylogeography: Species’ traits, environmental variation, and vertebrate diversification. Proc Natl Acad Sci USA 113:8041–8048CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2017

Authors and Affiliations

  • Natalia C. García
    • 1
  • Luciano N. Naka
    • 2
  • Gustavo S. Cabanne
    • 1
  1. 1.División OrnitologíaMuseo Argentino de Ciencias Naturales “Bernardino Rivadavia”–CONICETBuenos AiresArgentina
  2. 2.Laboratório de Ornitologia, Departamento de ZoologiaUniversidade Federal de PernambucoRecifeBrazil

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