Abstract
It is suggested that dispersal and vicariance led to speciation in Mesoamerican taxa during the Pleistocene, as a consequence of climatic fluctuations and resulting range disjunctions, but few biogeographic studies have been developed to assess their relative roles. Based on a mitochondrial DNA dataset, we analyzed the evolutionary history of Turdus assimilis, a species distributed in Mesoamerica and northwestern South America. Phylogenetic patterns, divergence times, and biogeographic analyses suggest a South American ancestor for T. assimilis, which split from T. albicollis between 1.4 and 3.0 Ma ago. The analysis suggests the colonization of Mesoamerica and the Chocó region by small numbers of founder individuals. Furthermore, genetic divergence, reciprocal monophyly, an ancient disjunction, and clear phenotypic differences suggest that the population from the Chocó region, T. a. daguae, represents a separate species from T. assimilis.
Zusammenfassung
Diversifizierung und Artbildung bei der Weißkehldrossel ( Turdus assimilis ; Aves: Turdidae) im Pleistozän Ausbreitung und Vikarianz gelten weithin als die Faktoren, die als ein Ergebnis von Klimaveränderungen und daraus resultierenden Brüchen in ihren Siedlungsgebieten bei den mittelamerikanischen Taxa während des Pleistozäns zur Artbildung geführt haben. Aber bislang sind nur wenige biogeographische Studien aufgesetzt worden, um die Rolle dieser Faktoren zu untersuchen. Anhand einer Datensammlung mitochondrialer DNA haben wir die Evolutionsgeschichte der Weißkehldrossel (Turdus assimilis), einer in Mittelamerika und Nordwest-Südamerika verbreiteten Art, analysiert. Phylogenetische Muster, Zeiten ausgeprägter Divergenzen und biogeographische Analysen legen nahe, dass es einen südamerikanischen Vorläufer der Weißkehldrossel gab, der sich vor 1,4 bis 3,0 Millionen Jahren von T. albicollis abspaltete. Die Analyse weist darauf hin, dass Mittelamerika und die Chocó-Gegend von einer kleinen Anzahl Gründer-Individuen besiedelt wurde. Ferner legen genetische Divergenzen, wechselseitige Monophylie, eine frühe Chromosomentrennung und klare phänotypische Unterschiede nahe, dass die Population der Chocó-Region, T. a. daguae, eine von T. assimilis unterschiedliche Art darstellt.
Similar content being viewed by others
References
Arbeláez-Cortés E, Navarro-Sigüenza AG (2013) Molecular evidence of the taxonomic status of western Mexican populations of Phaethornis longirostris (Aves: Trochilidae). Zootaxa 3716:081–097
Arbeláez-Cortés E, Nyári ÁS, Navarro-Sigüenza AG (2010) The differential effect of lowlands on the phylogeographic pattern of a Mesoamerican montane species (Lepidocolaptes affinis, Aves: Furnariidae). Mol Phylogenet Evol 57:658–668
Bacon CD, Silvestro D, Jaramillo C, Smith BT, Chakrabarty P, Antonelli A (2015) Biological evidence supports an early and complex emergence of the Isthmus of Panama. Proc Natl Acad Sci USA 112:6110–6115
Bagley JC, Johnson JB (2014) Phylogeography and biogeography of the lower Central American Neotropics: diversification between two continents and between two seas. Biol Rev 89:767–790
Barker FK (2007) Avifaunal interchange across the Panamanian isthmus: insights from Campylorhynchus wrens. Biol J Linn Soc 90:687–702
Bates JM, Hackett SJ, Cracraft J (1998) Area-relationships in the Neotropical lowlands: an hypothesis based on raw distributions of passerine birds. J Biogeogr 25:783–793
Becker CD, Ágreda A (2005) Bird community differences in mature and second growth garúa forest in Machalilla National Park, Ecuador. Ornitologia Neotropical 16:297–319
Bermingham E, Martin AP (1998) Comparative mtDNA phylogeography of neotropical freshwater fishes: testing shared history to infer the evolutionary landscape of lower Central America. Mol Ecol 7:499–517
Brumfield RT, Capparella AP (1996) Historical diversification of birds in northwestern South America: a molecular perspective on the role of vicariant events. Evolution 50:1607–1624
Clark JR, Ree RH, Alfaro ME, King MG, Wagner WL, Roalson EH (2008) A comparative study in ancestral range reconstruction methods: retracing the uncertain histories of insular lineages. Syst Biol 57:693–707
Clements JF, Schulenberg TS, Iliff MJ, Roberson D, Fredericks TA, Sullivan BL, Wood CL (2014) The eBird/Clements checklist of birds of the world: version 6.9. http://www.birds.cornell.edu/clementschecklist/download/
Coates A, Obando J (1996) The geologic evolution of the Central American isthmus. In: Jackson J, Budd A, Coates A (eds) Evolution and environment in Tropical America. University of Chicago Press, pp 21–56
Collar NJ (2015) White-throated Thrush (Turdus albicollis). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx Edicions, Barcelona
d’Horta FM, Cuervo AS, Ribas CC, Brumfield RT, Miyaki CY (2013) Phylogeny and comparative phylogeography of Sclerurus (Aves: Furnariidae) reveal constant and cryptic diversification in an old radiation of rain forest understorey specialists. J Biogeogr 40:37–49
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2014) InfoStat versión 2014. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Córdoba
Dickinson EC, Christidis L (2014) The Howard & Moore complete checklist of the birds of the world. Vol. 2. Passerines, 4th edn. Princeton University Press, Princeton
Drummond AJ, Rambaut A (2007) BEAST: Bayesian Evolutionary Analysis by Sampling Trees. BMC Evol Biol 7:214
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973
Eberhard JR, Bermingham E (2004) Phylogeny and biogeography of the Amazona ochrocephala (Aves: Psittacidae) complex. Auk 121:318–332
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Fernandes AM, Wink M, Sardelli CH, Aleixo A (2014) Multiple speciation across the Andes and throughout Amazonia: the case of the spot-backed antbird species complex (Hylophylax naevius/Hylophylax naevioides). J Biogeogr 41:1094–1104
García-Moreno J, Cortés N, García-Deras GM, Hernández-Baños BE (2006) Local origin and diversification among Lampornis hummingbirds: a Mesoamerican taxon. Mol Phylogenet Evol 38:488–498
Gernhard T (2008) The conditioned reconstructed process. J Theor Biol 253:769–778
Gill FB (2014) Species taxonomy of birds: which null hypothesis? Auk 131:150–161
Gill F, Donsker D (eds) (2015) IOC World Bird List (v 5.4). http://www.worldbirdnames.org/
González MA, Eberhard JR, Lovette IJ, Olson SL, Bermingham E (2003) Mitochondrial DNA phylogeography of the Bay Wren (Troglodytidae: Thryothorus nigricapillus) complex. Condor 105:228–238
González C, Ornelas JF, Gutiérrez-Rodríguez C (2011) Selection and geographic isolation influence hummingbird speciation: genetic, acoustic and morphological divergence in the Wedge-tailed Sabrewing (Campylopterus curvipennis). BMC Evol Biol 11:38
Gosler AG, Greenwood JJD, Baker JK, Davidson NC (1998) The field determination of body size and condition in passerines: a report to the British Ringing Committee. Bird Study 45:92–103
Gregory-Wodzicki KM (2000) Uplift history of the Central and Northern Andes: a review. Geol Soc Am Bull 112:1091–1105
Haffer J (1967) Speciation in Colombian forest birds west of the Andes. Am Mus Novit 294:1–57
Helbig AJ, Knox AG, Parkin DT, Sangster G, Collinson M (2002) Guidelines for assigning species rank. Ibis 144:518–525
Hilty SL, Brown WL (1986) A guide to the birds of Colombia. Princeton University Press, Princeton
Howell SNG, Webb S (1995) A guide to the birds of Mexico and Northern Central America. Oxford University Press, Oxford
Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Huelsenbeck JP, Rannala B, Masly JP (2000) Accommodating phylogenetic uncertainty in evolutionary studies. Science 288:2349–2350
Klicka J, Voelker G, Spellman GM (2005) A molecular systematic revision of the “true thrushes” (Turdinae). Mol Phylogenet Evol 34:486–500
Landis M, Matzke NJ, Moore BR, Huelsenbeck JP (2013) Bayesian analysis of biogeography when the number of areas is large. Syst Biol 62:789–804
Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701
Larget B, Simon D (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759
Lerner HRL, Meyer M, James HF, Hofreiter M, Fleischer RC (2011) Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers. Curr Biol 21:1838–1844
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Marchese C (2015) Biodiversity hotspots: a shortcut for a more complicated concept. Glob Ecol Conserv 3:297–309
Marks BD, Hackett SJ, Capparella AP (2002) Historical relationships among Neotropical lowland forest areas of endemism as determined by mitochondrial DNA sequence variation within the Wedge-billed Woodcreeper (Aves: Dendrocolaptidae: Glyphorynchus spirurus). Mol Phylogenet Evol 24:153–167
Marshall LG, Butler RF, Drake RE, Curtis GH, Tedford RH (1979) Calibration of the Great American Interchange. Science 204:272–279
Matzke NJ (2013) Probabilistic historical biogeography: new models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model testing. Dissertation. University of California, Berkeley
Matzke NJ (2014a) BioGeoBEARS: BioGeography with Bayesian (and likelihood) evolutionary analysis in R scripts. CRAN: The Comprehensive R Archive Network, Vienna. http://cran.r-project.org/package=BioGeoBEARS. Accessed 17 Dec 2015
Matzke NJ (2014b) Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades. Syst Biol 61:951–970
Milá B, Tavares ES, Muñoz Saldaña A, Karubian J, Smith TB, Baker AJ (2012) A trans-Amazonian screening of mtDNA reveals deep intraspecific divergence in forest birds and suggests a vast underestimation of species diversity. PLoS ONE 7:e40541
Miller MJ, Bermingham E, Klicka J, Escalante P, Raposo do Amaral FS, Weir JT, Winker K (2008) Out of Amazonia again and again: episodic crossing of the Andes promotes diversification in a lowland forest flycatcher. P Roy Soc Lond B 275:1133–1142
Miller MJ, Lelevier MJ, Bermingham E, Klicka JT, Escalante P, Winker K (2011) Phylogeography of the Rufous-tailed Hummingbird (Amazilia tzacatl). Condor 113:806–816
Montes C, Cardona A, Jaramillo C, Pardo A, Silva JC, Valencia V, Ayala C, Pérez-Angel LC, Rodríguez-Parra LA, Ramirez V, Niño H (2015) Middle Miocene closure of the Central American seaway. Science 348:226–229
Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Navarro-Sigüenza AG, Peterson AT (2004) An alternative species taxonomy of the birds of Mexico. Biota Neotropica 4:1–32
Navarro-Sigüenza AG, Peterson AT, Gordillo-Martínez A (2003) Museums working together: the atlas of the birds of Mexico. Bull Brit Ornithol Club 123A:207–225
Navarro-Sigüenza AG, Peterson AT, Nyári AS, García-Deras GM, García-Moreno J (2008) Phylogeography of the Buarremon brush-finch complex (Aves, Emberizidae) in Mesoamerica. Mol Phylogenet Evol 47:21–35
Nylander JAA, Olsson U, Alström P, Sanmartín I (2008) Accounting for phylogenetic uncertainty in biogeography: a Bayesian approach to dispersal-vicariance analysis of the thrushes (Aves: Turdus). Syst Biol 57:257–268
O’Neill JP, Lane DF, Naka LN (2011) A cryptic new species of thrush (Turdidae: Turdus) from Western Amazonia. Condor 113:869–880
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB et al (2012) Vegan: Community Ecology Package. R package version 2.0–5. 2012. https://cran.r-project.org/web/packages/vegan/index.html
Ornelas JF, González C, Espinosa de los Monteros A, Rodríguez-Gómez F, García-Feria LM (2014) In and out of Mesoamerica: temporal divergence of Amazilia hummingbirds pre-dates the orthodox account of the completion of the Isthmus of Panama. J Biogeogr 41:168–181
Ortiz-Ramírez MF, Andersen MJ, Zaldívar-Riverón A, Ornelas JF, Navarro-Sigüenza AG (2016) Geographic isolation drives divergence of uncorrelated genetic and song variation in the Ruddy-capped Nightingale-Thrush (Catharus frantzii; Aves: Turdidae). Mol Phyl Evol 94:74–86
Overtone LC, Rhoads DD (2006) Molecular phylogenetic relationships of Xiphidiopicus percussus, Melanerpes, and Sphyrapicus (Aves: Picidae) based on cytochrome b sequence. Mol Phylogenet Evol 41:288–294
Patané JSL, Weckstein JD, Aleixo A, Bates J (2009) Evolutionary history of Ramphastos toucans: molecular phylogenetics, temporal diversification, and biogeography. Mol Phylogenet Evol 53:923–934
Patel S, Weckstein JD, Patané JSL, Bates JM, Aleixo A (2011) Temporal and spatial diversification of Pteroglossus aracaris (Aves: Ramphastidae) in the Neotropics: constant rate of diversification does not support an increase in radiation during the Pleistocene. Mol Phylogenet Evol 58:105–115
Rambaut A (2009) FigTree 1.2.2 (computer program). http://tree.bio.ed.ac.uk/software/figtree/
Rambaut A, Drummond AJ (2007) Tracer v1.5 (computer program). http://beast.bio.ed.ac.uk/Tracer
Ree RH, Sanmartín I (2009) Prospects and challenges for parametric models in historical biogeographical inference. J Biogeogr 36:1211–1220
Ree RH, Smith SA (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst Biol 57:4–14
Ree RH, Moore BR, Webb CO, Donoghue MJ (2005) A likelihood framework for inferring the evolution of geographic range on phylogenetic trees. Evolution 59:2299–2311
Reeves RG, Bermingham E (2006) Colonization, population expansion, and lineage turnover: phylogeography of Mesoamerican characiform fish. Biol J Linn Soc 88:235–255
Ribas CC, Gaban-Lima R, Miyaki CY, Cracraft J (2005) Historical biogeography and diversification within the Neotropical parrot genus Pionopsitta (Aves: Psittacidae). J Biogeogr 32:1409–1427
Ridgely RS, Greenfield PJ (2001) The birds of Ecuador, volumes I and II. Cornell University Press, Ithaca
Ridgely RS, Tudor G (2009) Field guide of the songbirds of South America. Texas University Press, Austin
Ripley SD (1964) Family Muscicapidae, Subfamily Turdinae. In: Mayr E, Paynter RA (eds) Check-list of birds of the world: a continuation of the work of James L. Peters, vol. 10. Museum of Comparative Zoology, Cambridge, pp 13–227
Ripley B, Venables B, Bates DM, Hornik K, Gebhardt A, Firth D (2015) Support functions and datasets for Venables and Ripley’s MASS. R package version 7.3-37. http://CRAN.R-project.org/
Rising JD, Somers KM (1989) The measurement of overall body size in birds. Auk 106:666–674
Ronquist F (1997) Dispersal–vicariance analysis: a new approach to the quantification of historical biogeography. Syst Biol 46:195–203
Ronquist F, Sanmartín I (2011) Phylogenetic methods in biogeography. Annu Rev Ecol Syst 42:441–464
Sánchez-González LA, Moyle RG (2011) Molecular systematics and species limits in the Philippine fantails (Aves: Rhipidura). Mol Phylogenet Evol 61:290–299
Sangster G (2014) The application of species criteria in avian taxonomy and its implications for the debate over species concepts. Biol Rev Camb Philos Soc 89:199–214
Sanmartín I (2012) Historical biogeography: evolution in time and space. Evo Edu Outreach 5:555–568
Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464
Schweizer M, Wright TF, Peñalba JV, Schirtzinger EE, Joseph L (2015) Molecular phylogenetics suggests a New Guinean origin and frequent episodes of founder-event speciation in the nectarivorous lories and lorikeets (Aves: Psittaciformes). Mol Phyl Evol 90:34–48
Silvestro D, Michalak I (2012) RaxmlGUI: a graphical front-end for RAxML. Organ Divers Evol 12:335–337
Smith BT, Klicka J (2010) The profound influence of the Late Pliocene Panamanian uplift on the exchange, diversification, and distribution of New World birds. Ecography 33:333–342
Sorenson MD, Ast JC, Dimcheff DE, Yuri T, Mindell DP (1999) Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. Mol Phylogenet Evol 12:105–114
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729
Templeton AR (1980) The theory of speciation via the founder principle. Genetics 94:1011–1038
Templeton AR (2008) The reality and importance of founder speciation in evolution. BioEssays 30:470–479
Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Voelker G, Rohwer S, Bowie RCK, Outlaw DC (2007) Molecular systematics of a speciose, cosmopolitan songbird genus: defining the limits of, and relationships among, the Turdus thrushes. Mol Phylogenet Evol 42:422–434
Voelker G, Rohwer S, Outlaw DC, Bowie RCK (2009) Repeated trans-Atlantic dispersal catalysed a global songbird radiation. Global Ecol Biogeogr 18:41–49
Voelker G, Peñalba JV, Huntley JW, Bowie RCK (2014) Diversification in an Afro-Asian songbird clade (Erythropygia–Copsychus) reveals founder-event speciation via trans-oceanic dispersals and a southern to northern colonization pattern in Africa. Mol Phyl Evol 73:97–105
Webb SD (1976) Mammalian fauna dynamics of the great American interchange. Paleobiology 2:220–234
Webb SD (2006) The Great American Biotic Interchange: patterns and processes. Ann Mo Bot Gard 93:245–257
Wiley EO (1981) Phylogenetics: the theory and practice of phylogenetic systematics. Wiley, New York
Winger BM, Barker FK, Ree RH (2014) Temperate origins of long-distance seasonal migration in New World songbirds. Proc Natl Acad Sci USA 111:12115–12120
Yu Y, Harris AJ, He XJ (2010) S-DIVA (statistical dispersal–vicariance analysis): a tool for inferring biogeographic histories. Mol Phylogenet Evol 56:848–850
Acknowledgments
This contribution was supported by a postdoctoral fellowship from DGAPA-UNAM to JN-Z. We thank Alejandro Gordillo, Marco Ortiz, Fernanda Bibriesca, Alan Palacios, Aura Puga, Sahid Robles, Luis Antonio Sánchez, Ruth Bennett, Justin Hite, Mary Ferraro, and Oliver Komar for logistic support on field trips that resulted in key material for this study. We thank Luis Antonio Sánchez, Michael Wink, and two anonymous reviewers for helpful comments on the manuscript. We thank the individuals and institutions that provided tissue samples and helped with access to specimens (Fanny Rebón and Diego Roldán, MZFC; Nathan Rice, Academy of Natural Sciences; Thomas J. Trombone and Paul R. Sweet, American Museum of Natural History; and Mark Robbins, University of Kansas). Financial support for different stages of the project was obtained from CONACYT (152,060) and PAPIIT-UNAM (IN 217212 and 215515).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Wink.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Núñez-Zapata, J., Townsend Peterson, A. & Navarro-Sigüenza, A.G. Pleistocene diversification and speciation of White-throated Thrush (Turdus assimilis; Aves: Turdidae). J Ornithol 157, 1073–1085 (2016). https://doi.org/10.1007/s10336-016-1350-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-016-1350-6