Defining the phylogeographic relationship between cis- and trans-Andean populations of Dendrocincla fuliginosa and Xenops minutus in Colombia


  • Enrique Arbeláez-Cortés Grupo de Estudios en Biodiversidad, Escuela de Biología, Facultad de Ciencias, Universidad Industrial de Santander, Carrera 27 Calle 9, Bucaramanga, Santander, Colombia


Palabras clave:

Amazonia, Birds, Orinoquia, Lowlands, mtDNA, nDNA, South America


Due to the position of Colombia between Central and South America, and the presence of several ecosystems in its territory, phylogeographic information from populations across this country is fundamental to understand the
evolutionary history of widespread Neotropical species. The Andes have long been noted for their influence isolating lowland species into cis- and trans-Andean populations. However, detailed sampling across cis-Andean zones adjacent to the Andes (i.e., Orinoquia) has been lacking in avian phylogeographic studies. Information from DNA sequences, from 2 passerine birds: Dendrocincla fuliginosa and Xenops minutus is presented herein; to depict their phylogeographic patterns, focusing on the relationship between cis- and trans-Andean populations from Colombia. The analyses, regarding
Colombian samples indicated that cis-Andean populations (i.e., Orinoquia and Amazon) are not closely related, rather the Orinoquia populations are more closely related to trans-Andean populations in both species. These relationships
suggest that populations on both sides of the Andes were connected in the recent past (less than 1 myA). I propose that phylogeographic differentiation in lowland species in this region is not only explained by the presence of the 
Andean mountains, but also based on the ecological shifts between major ecosystems such as Amazonia and Orinoquia.


Arbeláez-Cortés, E. (2013) Knowledge of Colombian biodiversity: published and indexed. Biodiversity and Conservation, 22, 2875-2906.

Arbeláez-Cortés, E., Roldán-Piña, D. and Navarro-Sigüenza, A.G. (2014) Multilocus phylogeography and morphology give insights into the recent evolution of a Mexican endemic songbird: Vireo hypochryseus. Journal of Avian Biology, 45, 253-263.

Arbeláez-Cortés, E., Torres, M.F., López-Álvarez, D., Palacio-Mejía, J.D., Mendoza, Á.M. and Medina, C.A. (2015) Colombian frozen biodiversity: 16 years of the tissue collection of the Humboldt Institute. Acta Biologica Colombiana, 20, 163-173.

Arbogast, B.S., Drovetski, S.V., Curry, R.L., Boag, P.T., Seu- tin, G., Grant, P.R., Grant, B.R. and Anderson, D.J. (2006) The origin and diversification of Galapagos mockingbirds. Evoution, 60, 370-382.

Armenteras, D., Rodríguez, N., Retana, J. and Morales, M. (2011) Understanding deforestation in montane and lowland forests of the Colombian Andes. Regional Environmental Change, 11, 693-705.

Armenteras, D., Romero, M. and Galindo, G. (2005) Vegetation fire in the savannas of the Llanos Orientales of Colombia. World Resource Review, 17, 628-647.

Avendaño, J.E., Arbeláez-Cortés, E. and Cadena, C.D. (2017a) On the importance of geographic and taxonomic sampling in phylogeography: A reevaluation of diversification and species limits in a Neotropical thrush (Aves, Turdidae). Molecular Phylogenetics and Evolution, 111, 87-97.

Avendaño, J.E., Bohórquez, C.I., Rosselli, L., Arzuza-Buelvas, D., Estela, F.A., Cuervo, A.M., Stiles, F. Gary and Renjifo, L.M. (2017b) Lista de chequeo de las aves de Colombia: Una síntesis del estado del conocimiento desde Hilty & Brown (1986) Ornitologia Colombiana, 16, 1-83.

Avendaño, J.E., Cortés-Herrera, J.O., Briceño-Lara, E.R. and Rincón-Guarín, D.A. (2013) Crossing or bypassing the Andes: a commentary on recent range extensions of cis-Andean birds to the West of the Andes of Colombia. Orinoquia, 17, 208-214.

Backström, N., Fagerberg, S. and Ellegren, H. (2008) Genomics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genome. Molecular Ecology, 17, 964-980.

Bandelt, H.J., Forster, P. and Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48.

Benham, P.M., Cuervo, A.M., McGuire, J.A. and Witt, C.C. (2015) Biogeography of the Andean metaltail hummingbirds: contrasting evolutionary histories of tree line and habitat-generalist clades. Journal of Biogeography, 42, 763-777.

Botero, S., Stevenson, P.R. and Di Fiore, A. (2015) A primer on the phylogeography of Lagothrix lagotricha (sensu Fooden) in northern South America. Molecular Phylogenetics and Evolution, 82, 511-517.

Brumfield, R.T. (2012) Inferring the origins of lowland Neotropical birds. Auk, 129, 367-376.

Cadena, C.D. (2007) Testing the role of interspecific competition in the evolutionary origin of elevational zonation: An example with Buarremon brush-finches (Aves, Emberizidae) in the Neotropical mountains. Evolution, 61, 1120-1136.

Cadena, C.D., Gutiérrez-Pinto, N., Dávila, N. and Terry Chesser, R. (2011) No population genetic structure in a widespread aquatic songbird from the Neotropics. Molecular Phylogenetics and Evolution, 58, 540-545.

Cadena, C.D., Klicka, J. and Ricklefs, R.E. (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.

Cadena, C.D., Pedraza, C.A. and Brumfield, R.T. (2016) Climate, habitat associations and the potential distributions of Neotropical birds: Implications for diversification across the Andes. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, 40, 275-287.

Caro, L.M., Caycedo-Rosales, P.C., Bowie, R.C.K., Slabbekoorn, H. and Cadena, C.D. (2013) Ecological speciation along an elevational gradient in a tropical passerine bird? Journal of Evolutionary Biology, 26, 357-374.

Claramunt, S., Derryberry, E.P., Chesser, R.T., Aleixo, A. and Brumfield, R.T. (2010) Polyphyly of Campylorhamphus, and description of a new genus for C. pucherani (Dendrocolaptinae). Auk, 127, 430-439.

Cracraft, J. (1985) Historical biogeography and patterns of diversification within the South American areas of endemism. In: P.A. Buckley, M.S, F., E.S. Morton, R.S. Ridgely & F.G. Buckley (Eds.) Ornithological Monographs (pp. 49-84). The American Ornithologist Union.

Cheviron, Z.A., Hackett, S.J. and Capparella, A.P. (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.

Del Hoyo, J., Elliot, A. and Christie, D.A. (2003) Handbook of the Birds of the World. Broadbills to Tapaculos. Lynx Edicions, Barcelona.

Derryberry, E.P., Claramunt, S., Derryberry, G., Chesser, R.T., Cracraft, J., Aleixo, A., Pérez-Emán, J., Remsen, J.J.V. and Brumfield, R.T. (2011) Lineage diversification and morphological evolution in a large-scale continental radiation: The Neotropical ovenbirds and woodcreepers (Aves: Furnariidae). Evolution, 65, 2973-2986.

Donegan, T., Quevedo, A., Verhelst, J.C., Cortés, O., Pacheco, J.A. and Salaman, P. (2014) Revision of the status of bird species occurring or reported in Colombia 2014. Conservación Colombiana, 21, 3-11.

Donegan, T.M., McMullan, W.M., Quevedo, A. and Salaman, P. (2013) Revision of the status of bird species occurring or reported in Colombia 2013. Conservación Colombiana, 19, 3-10.

Drummond, A.J., Rambaut, A. and Suchard, M. (2012a) BEAST v1.7.4 Bayesian Evolutionary Analysis Sampling Trees. Department of Computer Science University of Auckland, Institute of Evolutionary Biology University of Edinburgh, David Geffen School of Medicine University of California, Los Angeles, Available at:,

Drummond, A.J., Suchard, M.A., Xie, D. and Rambaut, A. (2012b) Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969-1973.

Etter, A., McAlpine, C., Wilson, K., Phinn, S. and Possingham, H. (2006) Regional patterns of agricultural land use and deforestation in Colombia. Agriculture, Ecosystems and Environment, 114, 369-386.

Fernandes, A.M., Wink, M., Sardelli, C.H., Aleixo, A. and Ebach, M. (2014) Multiple speciation across the Andes and throughout Amazonia: the case of the spot-backed antbird species complex (Hylophylax naevius/Hylophylax naevioides). Journal of Biogeography, 41, 1094-1104.

Flantua, S.A., van Boxel, J., Hooghiemstra, H. and van Smaalen, J. (2007) Application of GIS and logistic regression to fossil pollen data in modelling present and past spatial distribution of the Colombian savanna. Climate Dynamics, 29, 697-712.

Fuchs, J., Chen, S., Johnson, J.A. and Mindell, D.P. (2011) Pliocene diversification within the South American Forest falcons (Falconidae: Micrastur). Molecular Phylogenetics and Evolution, 60, 398-407.

GeoNames. (2013) GeoNames geographical database, Retrieved January 15, 2013, from:

Gill, F. and Donsker, D. (2018) IOC World Bird Names v 8.2, Retrieved September 30, 2018, from:

Google. (2010) Google Earth.

Gregory-Wodzicki, K.M. (2000) Uplift history of the Central and Northern Andes: A review. Geological Society of America Bulletin, 112, 1091-1105.

Haffer, J. (1967) Speciation in Colombian forest birds west of the Andes. American Museum Novitates, 1-57.

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.

Hammer, Ø., Harper, D.A.T. and Ryan, P.D. (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4, 1-9.

Harvey, M.G. and Brumfield, R.T. (2015) Genomic variation in a widespread Neotropical bird (Xenops minutus) reveals divergence, population expansion, and gene flow. Molecular Phylogenetics and Evolution, 83, 305-316.

Johnson, K.P. and Weckstein, J.D. (2011) The Central Ameri- can land bridge as an engine of diversification in New World doves. Journal of Biogeography, 38, 1069–1076.

Lerner, Heather R.L., Meyer, M., James, Helen F., Hofreiter, M. and Fleischer, Robert C. (2011) Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian Honeycreepers. Current biology : CB, 21, 1838-1844.

Librado, P. and Rozas, J. (2009) DNAsp v5: A software for comprehensive analysis of DNA polimorphism data. Bioinformatics, 25, 1451-1452.

Link, A., Valencia, L.M., Céspedes, L.N., Duque, L.D., Cadena, C.D. and Fiore, A.D. (2015) Phylogeography of the critically endangered brown spider monkey (Ateles hybridus): Testing the riverine barrier hypothesis. International Journal of Primatology, 36, 530-547.

Lozano-Zambrano, F.H. and Fernández, F. (2007) Aproximación al análisis zoogeográfico de las hormigas cazadoras (Hymenoptera: Formicidae) de Colombia. Boletin del Museo de Entomologia de la Universidad del Valle, 8, 22-31.

Lynch, J.W., Cortés-Ortiz, L., Di Fiore, A. and Boubli, J.P. (2015) Special issue: Comparative biogeography of Neotropical primates. Molecular Phylogenetics and Evolution, 82, 518-529.

Marks, B.D., Hackett, S.J. and Capparella, A.P. (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.

Miller, M.J., Bermingham, E., Klicka, J., Escalante, P., Amaral, F.S.R.d., Weir, J.T. and Winker, K. (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.

Morrone, J.J. (2014) Biogeographical regionalisation of the Neotropical region. Zootaxa, 3782, 1-110.

Naka, L.N., Bechtoldt, C.L., Henriques, L.M.P. and Brumfield, R.T. (2012) The role of physical barriers in the location of avian suture zones in the Guiana Shield, northern Amazonia. The American Naturalist, 179, E115-E132.

Nores, M. (2004) The implications of Tertiary and Quaternary sea level rise events for avian distribution patterns in the lowlands of northern South America. Global Ecology and Biogeography, 13, 149-161.

Nyári, Á.S. (2007) Phylogeographic patterns, molecular and vocal differentiation, and species limits in Schiffornis turdina (Aves). Molecular Phylogenetics and Evolution, 44, 154-164.

Parra, J.L., Remsen Jr, J.V., Álvarez-Rebolledo, M. and McGuire, J.A. (2009) Molecular phylogenetics of the hummingbird genus Coeligena. Molecular Phylogenetics and Evolution, 53, 425-434.

Patel, S., Weckstein, J.D., Patané, J.S.L., Bates, J.M. and Aleixo, A. (2011) Temporal and spatial diversification of Pteroglossus araçaris (Aves: Ramphastidae) in the neotropics: Constant rate of diversification does not support an increase in radiation during the Pleistocene. Molecular Phylogenetics and Evolution, 58, 105-115.

Posada, D. and Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817–818.

Rambaut, A. and Drummond, A.J. (2012) TreeAnnotator v1.7.4. Institute of Evolutionary Biology, University of Edinburgh, Department of Computer Science, University of Auckland, Available as part of the BEAST package at,

Restall, R., Rodner, C. and Lentino, M. (2006) Birds of Northern South America: An identification guide. Yale University Press, New Haven.

Rheindt, F.E., Christidis, L., Cabanne, G.S., Miyaki, C. and Norman, J.A. (2009) The timing of Neotropical speciation dynamics: A reconstruction of Myiopagis flycatcher diversification using phylogenetic and paleogeographic data. Molecular Phylogenetics and Evolution, 53, 961-971.

Romero-Ruiz, M.H., Flantua, S.G.A., Tansey, K. and Berrio, J.C. (2012) Landscape transformations in savannas of northern South America: Land use/cover changes since 1987 in the Llanos Orientales of Colombia. Applied Geography, 32, 766-776.

Schultz, E.D., Burney, C.W., Brumfield, R.T., Polo, E.M., Cracraft, J. and Ribas, C.C. (2017) Systematics and biogeography of the Automolus infuscatus complex (Aves; Furnariidae): Cryptic diversity reveals western Amazonia as the origin of a transcontinental radiation. Molecular Phylogenetics and Evolution, 107, 503-515.

Sigrist, M.S. and Carvalho, C.J.B.d. (2009) Historical relationships among areas of endemism in the tropical South America using Brooks Parsimony Analysis (BPA). Biota Neotropica, 9, 79-90.

Smith, B.T., Harvey, M.G., Faircloth, B.C., Glenn, T.C. and Brumfield, R.T. (2014a) Target capture and massively parallel sequencing of ultraconserved elements for comparative studies at shallow evolutionary time scales. Systematic Biology, 63, 83-95.

Smith, B.T., McCormack, J.E., Cuervo, A.M., Hickerson, M.J., Aleixo, A., Cadena, C.D., Pérez-Emán, J., Burney, C.W., Xie, X., Harvey, M.G., Faircloth, B.C., Glenn, T.C., Derryberry, E.P., Prejean, J., Fields, S. and Brumfield, R.T. (2014b) The drivers of tropical speciation. Nature, 515, 406–409.

Sparrman, A. (1788) In quo novas et selectas Aves, coloribus ad vivum brevique descriptione illustratas, suasu et sumtibus generosissimi possessoris. Museum Carlsonianum, 68,

Stephens, M. and Donnelly, P. (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. American Journal of Human Genetics, 73, 1162-1169.

Stephens, M., Smith, N.J. and Donnelly, P. (2001) A new statistical method for haplotype reconstruction from population data. The American Journal of Human Genetics, 68, 978-989.

Stiles, F.G., Cuervo, A.M., Rosselli, L., Bohórquez, C.I., Estela, F. and Arzuza, D. (2011) Species lists of birds for South American countries and territories: Colombia, Retrieved 03 December, 2012, from:

Valderrama, E., Pérez-Emán, J.L., Brumfield, R.T., Cuervo, A.M. and Cadena, C.D. (2014) The influence of the complex topography and dynamic history of the montane Neotropics on the evolutionary differentiation of a cloud forest bird (Premnoplex brunnescens, Furnariidae). Journal of Biogeography, 41, 1533-1546.

Vieillot, L.J.P. (1818) Nouveau dictionnaire d'Histoire Naturelle appliquée aux arts , à l'agriculture, à l'économie rurale et domestique, à la médecine, etc. Paris.

Weir, J.T., Bermingham, E. and Schluter, D. (2009) The great American biotic interchange in birds. Proceedings of the National Academy of Sciences, 106, 21737–21742.

Weir, J.T. and Price, M. (2011) Andean uplift promotes lowland speciation through vicariance and dispersal in Dendrocincla woodcreepers. Molecular Ecology, 20, 4550-4563.

Weir, J.T. and Schluter, D. (2008) Calibrating the avian molecular clock. Molecular Ecology, 17, 2321-2328.