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Phylogeny and biogeography of a subclade of mangoes (Aves, Trochilidae)

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Abstract

In this study we explore the phylogenetic relationships within the hummingbird genera Doryfera, Schistes and Colibri (Family Trochilidae), distributed in the Andes, the Pantepui, the southern Brazilian uplands and the lowlands of South America including the Chocó, the Amazon Basin, the Chaco, the Cerrado, and the southeastern Brazilian coast, as well as Central and Mesoamerica. To do this, we included a comprehensive sampling of the 16 traditionally recognized subspecies within this group. We found that Doryfera, Schistes and Colibri form a well-supported monophyletic group, and that most of the traditionally recognized subspecies are indeed evolutionary lineages. As there is a high likelihood that the ancestors of this clade of hummingbirds were distributed in the lowlands, we ask: what events might account for the diversification of this subclade of mangoes into the Andes with a later potential dispersal episode from the Andes to the lowlands? We found that several phenomena such as the uplift of the Andes, the marine transgressions of the Plio–Pleistocene, the final closure of the Isthmus of Panama and the climatic oscillations of the Pleistocene might be at least, in part, responsible for the diversification of this group in both the lowlands and the highlands of this region of South America.

Zusammenfassung

Phylogenie und Biogeografie einer Untergruppe von Mangokolibris (Aves, Trochilidae) Diese Studie untersucht die phylogenetischen Beziehungen innerhalb der Kolibrigattungen Doryfera, Schistes und Colibri (Trochilidae), deren Verbreitung sich über die Anden, den Pantepui, das südbrasilianische Hochland und das südamerikanische Tiefland einschließlich der Provinzen Choco (Kolumbien) und Chaco (Argentinien), dazu die Savannen in Zentral-Brasilien (Cerrados), das Amazonas Becken, die südöstliche Küste Brasiliens sowie über Zentral- und Mittelamerika erstreckt. In die Studie wurden in einer umfangreichen Beprobung 16 bekannte Unterarten aus der genannten Untergruppe einbezogen. Doryfera, Schistes und Colibri bilden eine monophyletische Gruppe. Die meisten der bekannten Unterarten haben eine gemeinsame evolutionäre Abstammung. Da mit hoher Wahrscheinlichkeit die Vorfahren dieser Kolibri-Gruppe im Tiefland verbreitet waren, stellt sich die Frage, welche Ereignisse für die Diversifizierung der Untergruppe der Mangokolibris in die Anden mit einer späteren potentiellen Ausbreitungsperiode von den Anden in das Tiefland verantwortlich waren. Wir fanden heraus, dass mehrere Phänomene, wie beispielsweise die Hebung der Anden, die marinen Transgressionen im Plio-Pleistozän, die endgültige Schließung der Landenge von Panama sowie die klimatischen Schwankungen im Pleistozän zumindest in Teilen verantwortlich sein könnten für die Diversifizierung dieser Gruppe in das Tiefland und in das Hochland in dieser Region in Südamerika.

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References

  • Almeida FC, Bonvicino CR, Cordeiro-Estrela P (2007) Phylogeny and temporal diversification of Calomys (Rodentia, Sigmodontinae): implications for the biogeography of an endemic genus of the open/dry biomes of South America. Mol Phylogenet Evol 42:449–466

    Article  CAS  PubMed  Google Scholar 

  • Bleiweiss R (1998) Origin of hummingbird faunas. Biol J Linn Soc 65:77–97

    Article  Google Scholar 

  • Bleiweiss R, Kirsch JA, Matheus JC (1994) DNA–DNA hybridization evidence for subfamily structure among hummingbirds. Auk 111:8–19

    Article  Google Scholar 

  • Bleiweiss R, Kirsch JA, Matheus JC (1997) DNA hybridization evidence for the principal lineages of hummingbirds (Aves: Trochilidae). Mol Biol Evol 14:325–343

    Article  CAS  PubMed  Google Scholar 

  • Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10(4):e1003537. doi:10.1371/journal.pcbi.1003537

    Article  PubMed  PubMed Central  Google Scholar 

  • Braun MJ, Isler ML, Isler PR, Bates JM, Robbins MB (2005) Avian speciation in the Pantepui: the case of the Roraiman Antbird (Percnostola [Schistocichla] “leucostigmasaturata). Condor 107:327–341. doi:10.1650/7647

    Article  Google Scholar 

  • Brumfield RT, Edwards SV (2007) Evolution into and out of the Andes: a Bayesian analysis of historical diversification in Thamnophilus antshrikes. Evolution 61:346–367

    Article  CAS  PubMed  Google Scholar 

  • Burns KJ, Naoki K (2004) Molecular phylogenetics and biogeography of Neotropical tanagers in the genus Tangara. Mol Phylogenet Evol 32:838–854

    Article  CAS  PubMed  Google Scholar 

  • Chapman FM (1917) The distribution of bird-life in Colombia: a contribution to a biological survey of South America. B Am Mus Nat Hist 36:1–728

    Google Scholar 

  • Chapman FM (1926) The distribution of bird-life in Ecuador: a contribution to a study of the origin of Andean bird-life. B Am Mus Nat Hist 55:1–784

    Google Scholar 

  • Chapman FM (1931) The upper zonal bird-life of Mts. Roraima and Duida. B Am Mus Nat Hist 63:1–135

    Google Scholar 

  • Chaves JA, Pollinger JP, Smith TB, LeBuhn G (2007) The role of geography and ecology in shaping the phylogeography of the Speckled Hummingbird (Adelomyia melanogenys) in Ecuador. Mol Phylogenet Evol 43:795–807

    Article  PubMed  Google Scholar 

  • Chesser RT (2004) Systematics, evolution, and biogeography of the South American ovenbird genus Cinclodes. Auk 121:752–766

    Article  Google Scholar 

  • Claramunt S, Cracraft J (2015) A new time tree reveals Earth history’s imprint on the evolution of modern birds. Sci Adv 11:e1501005

    Article  Google Scholar 

  • Coates AG, Jackson JBC, Collins LS, Cronin TM, Dowsett HJ, Bybell LM, Jung P, Obando JA (1992) Closure of the Isthmus of Panama: the near-shore marine record of Costa Rica and western Panama. Geol Soc Am Bull 104:814–828

    Article  Google Scholar 

  • Cook RE (1974) Origin of the highland avifauna of southern Venezuela. Syst Zool 23:257–264

    Article  Google Scholar 

  • Cory CB (1918) Catalogue of birds of the Americas and adjacent islands etc. Publications of the Field Museum of Natural History (Zoological Series), Chicago

    Google Scholar 

  • Cracraft J (1985) Historical biogeography and patterns of differentiation within the South American avifauna: areas of endemism. Am Ornithol Union Monogr 36:49–84

    Article  Google Scholar 

  • De-Silva DL, Elias M, Willmott K, Mallet J, Day JJ (2016) Diversification of clearwing butterflies with the rise of the Andes. J Biogeog 43:44–58

    Article  Google Scholar 

  • Dickinson E (2003) The Howard and Moore complete checklist of the birds of the world. Princeton University Press, Princeton

    Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed  PubMed Central  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with beauty and the beast 1.7. Mol Biol Evol 29:1969–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Fjeldså J (1995) Geographical patterns of neoendemic and older relict species of Andean forest birds: the significance of ecologically stable areas. In: Churchill SP, Balslev H, Forero E, Luteyn JL (eds) Biodiversity and conservation of Neotropical montane forests. New York Botanical Garden Press, New York, pp 89–102

    Google Scholar 

  • Fjeldså J, Krabbe N (1990) Birds of the high Andes. Zoological Museum, University of Copenhagen and Apollo Books, Denmark

    Google Scholar 

  • Fjeldså J, Rahbek C (2006) Diversification of tanagers, a species rich bird group, from lowlands to montane regions of South America. Integr Comp Biol 46:72–81

    Article  PubMed  Google Scholar 

  • Garcia-Moreno J, Arctander P, Fjeldså J (1999) A case of rapid diversification in the Neotropics: phylogenetic relationships among Cranioleuca spinetails (Aves, Furnariidae). Mol Phylogenet Evol 12:273–281

    Article  CAS  PubMed  Google Scholar 

  • Garzione CN, Hoke GD, Libarkin JC, Withers S, MacFadden B, Eiler J, Ghosh P, Mulch A (2008) Rise of the Andes. Science 320:1304–1307

    Article  CAS  PubMed  Google Scholar 

  • Gerwin JA, Zink RM (1989) Phylogenetic patterns in the genus Heliodoxa (aves: Trochilidae): an allozymic perspective. Wilson Bull 101:525–544

    Google Scholar 

  • Gregory-Wodzicki KM (2000) Uplift histroy of the Central and Norhern Andes: a review. Geol Soc Am Bull 112:1091–1105

    Article  Google Scholar 

  • Haag T, Muschner VC, Freitas LB, Oliveira LFB, Langguth AR, Mattevi MS (2007) Phylogenetic relationships among species of the genus Calomys with emphasis on South American lowland taxa. J Mamm 88:769–776

    Article  Google Scholar 

  • Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han KL, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768

    Article  CAS  PubMed  Google Scholar 

  • Haffer J (1974) Avian speciation in tropical America. Nuttall Ornithological Club, Cambridge

    Google Scholar 

  • Ho SYW, Phillips MJ (2009) Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Systematic Biol 58:367–380

    Article  Google Scholar 

  • Hooghiemstra H, Van der Hammen T, Cleef A (2000) Evolution of forests in the northern Andes and Amazonian lowlands during the Tertiary and Quaternary. In: Guariguata M (ed) Ecology of Neotropical rainforests. Wageningen University, The Netherlands

    Google Scholar 

  • Hooghiemstra H, Wijninga VM, Cleef AM (2006) The paleobotanical record of Colombia: implications for biogeography and biodiversity. Ann Mo Bot Gard 93:297–324

    Article  Google Scholar 

  • Hoorn C, Guerrero J, Sarmiento GA, Lorente MA (1995) Andean tectonics as a cause for changing drainage patterns in Miocene northern South America. Geology 23:237–240

    Article  Google Scholar 

  • Hoorn C, Wesselingh FP, ter Steege H, Bermudez MA, Mora A, Sevink J, Sanmartín I, Sanchez-Meseguer A, Anderson CL, Figueiredo JP, Jaramillo C, Riff D, Negri FR, Hooghiemstra H, Lundberg J, Stadler T, Särkinen T, Antonelli A (2010) Amazonia through time: andean uplift, climate change, landscape evolution, and biodiversity. Science 330:927–931

    Article  CAS  PubMed  Google Scholar 

  • Huber O (1988) Guayana highlands versus Guayana lowlands, a reappraisal. Taxon 37:595–614

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MrBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Hughes C, Eastwood R (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. P Natl Acad Sci USA 103:10334–10339

    Article  CAS  Google Scholar 

  • Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C et al (2014) Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346:1320–1331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kennan L, Lamb SH, Hoke L (1997) High-altitude palaeosurfaces in the Bolivian Andes: evidence for late Cenozoic surface uplift. In: Widdowson M (ed) Palaeosurfaces: recognition, reconstruction and palaeoenvironmental interpretation, vol 120. Geological Society Special Publication, London, pp 307–323

    Google Scholar 

  • Kieswetter CM, Schneide CJ (2013) Phylogeography in the northern Andes: complex history and cryptic diversity in a cloud forest frog, Pristimantis w-nigrum (Craugastoridae). Mol Phylogenet Evol 69:417–429

    Article  PubMed  Google Scholar 

  • Lamb S, Hoke L (1997) Origin of the high plateau in the Central Andes, Bolivia, South America. Tectonics 16:623–649

    Article  Google Scholar 

  • Lutz HL, Weckstein JD, Patané JS, Bates JM, Aleixo A (2013) Biogeography and spatio-temporal diversification of Selenidera and Andigena Toucans (Aves: Ramphastidae). Mol Phylogenet Evol 69:873–883

    Article  PubMed  Google Scholar 

  • Mauck WMIII, Burns KJ (2009) Phylogeny, biogeography, and recurrent evolution of divergent bill types in the nectar-stealing flowerpiercers (Thraupini: Diglossa and Diglossopis). Biol J Linn Soc 98:14–28

    Article  Google Scholar 

  • Mayr E, Phelps WEJ (1967) The origin of the bird fauna of the south Venezuelan highlands. B Am Mus Nat Hist 136:269–328

    Google Scholar 

  • McGuire JA, Witt CC, Altshuler DL, Remsen JV (2007) Phylogenetic systematics and biogeography of hummingbirds: Bayesian and maximum likelihood analyses of partitioned data and selection of an appropriate partitioning strategy. Syst Biol 56:837–856

    Article  CAS  PubMed  Google Scholar 

  • McGuire JA, Witt CC, Remsen JV, Dudley R, Altshuler DL (2008) A higher-level taxonomy for hummingbirds. J Ornithol 150:155–165

    Article  Google Scholar 

  • McGuire JA, Witt CC, Remsen JV, Corl A, Rabosky DL, Altshuler DL, Dudley R (2014) Molecular phylogenetics and the diversification of hummingbirds. Curr Biol 24:1038

    Article  CAS  Google Scholar 

  • Meyer De Schauensee R (1970) A guide to the birds of South America. Livingston, Wynnwood

    Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, pp 1–8

  • Nores M (2000) Species richness in the Amazonian bird fauna from an evolutionary perspective. Emu 100:419–430

    Article  Google Scholar 

  • 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 Ecol Biogeogr 13:149–161

    Article  Google Scholar 

  • Nylander JAA (2004) MrModeltest v2.3 (Program distributed by the author). Evolutionary Biology Centre, Uppsala University

  • O’Dea A, Lessios HA, Coates AG, Eytan RI, Restrepo-Moreno SA, Cione AL et al (2016) Formation of the Isthmus of Panama. Sci Adv 2:e1600883

    Article  PubMed  PubMed Central  Google Scholar 

  • Perktas U, Quintero E (2013) A wide geographical survey of mitochondrial DNA variation in the Great Spotted Woodpecker complex, Dendrocopos major (Aves: Picidae). Biol J Linn Soc 108:173–188

    Article  Google Scholar 

  • Perktas U, Barrowclough GF, Groth JG (2011) Phylogeography and species limits in the Green Woodpecker complex (Aves: Picidae): multiple Pleistocene refugia and range expansion across Europe and the Near East. Biol J Linn Soc 104:710–723

    Article  Google Scholar 

  • Perktas U, Peterson AT, Dyer D (2017) Integrating morphology, phylogeography, and ecological niche modeling to explore population differentiation in North African Common Chaffinches. J Ornithol 158:1–13

    Article  Google Scholar 

  • Peters JL (1945) Check-list of birds of the world. Museum of Comparative Zoology, Harvard University, Cambridge

    Google Scholar 

  • Phelps WH, Phelps WHJ (1952) Nine new subspecies of birds from Venezuela. Proc Biol Soc Wash 65:39–54

    Google Scholar 

  • Quintero E, Ribas CC, Cracraft J (2013) The Andean Hapalopsittaca parrots (Psittacidae, Aves): an example of montane-tropical lowland vicariance. Zool Scr 42:28–43

    Article  Google Scholar 

  • Ribas CC, Gaban-Lima R, Miyaki CY, Cracraft J (2005) Historical biogeography and diversification within the Neotropical parrot genus Pionopsitta (Aves: Psittacidae). J Biogeog 32:1409–1427

    Article  Google Scholar 

  • Ribas CC, Moyle RG, Miyaki CY, Cracraft J (2007) Deciphering the origins of montane biotas: linking Andean tectonics and climatic oscillations to independent regimes of diversification in Pionus parrot. P R Soc B 274:2399–2408

    Article  Google Scholar 

  • Rull V (2004) An evaluation of the lost world and vertical displacement hypotheses in the Chimantá Massif, Venezuelan Guayana. Global Ecol Biogeogr 13:141–148

    Article  Google Scholar 

  • Rull V (2005) Biotic diversification in the Guayana highlands: a proposal. J Biogeog 32:921–927

    Article  Google Scholar 

  • Ruschi A (1963) A atual distiribucao geografica das especies e sub-especies do genero Augastes, como a descricao des uma nova sub-especie: Augastes scutatus soaresis ruschi, e a chave artificial e analitica para o reconhecimiento das mesmas. Boletim do Museu de Biologia Mello Leitao (Serie Divulgacao), pp 1–4

  • Salerno PE, Ron SR, Señaris JC, Rojas-Runjaic FJM, Noonan BP, Cannatella DC (2012) Ancient tepui summits harbor young rather than old lineages of endemic frogs. Evolution 66:3000–3013

    Article  PubMed  Google Scholar 

  • Schuchmann KL (1999) Family Trochilidae (hummingbirds). In: Del Hoyo J, Elliott A, Sargatal J (eds) Handbook of the birds of the world. Barn Owls to hummingbirds, vol 5. Lynx, Barcelona, pp 468–535

    Google Scholar 

  • Sikes DS, Lewis PO (2001) Beta software, version 1. PAUPRat: PAUP* implementation of the parsimony ratchet. Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, USA. (Program distributed by the authors)

  • Smith BT, McCormack JE, Cuervo AM, Hickerson MJ, Aleixo A, Cadena CD, Brumfield RT (2014) The drivers of tropical speciation. Nature 515:406–409. doi:10.1038/nature13687 (Letter)

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL (2002) PAUP: phylogenetic analysis using parsimony (and other methods). Version 4.0b10. Sinauer, Sunderland

  • Terborgh J (1971) Distribution on environmental gradients: theory and a preliminary interpretation of distributional patterns in the avifauna of the Cordillera Vilcabamba, Peru. Ecology 52:23–40

    Article  Google Scholar 

  • Torres-Carvajal O (2007) Phylogeny and biogeography of a large radiation of Andean lizards (Iguania, Stenocercus). Zool Scr 36:311–326

    Article  Google Scholar 

  • van der Hammen T, Cleef AM (1986) Development of the high Andean Paramo flora and vegetation. In: Vuilleumier F, Monasterio M (eds) High altitude tropical biogeography. Oxford University Press, New York, pp 153–201

    Google Scholar 

  • Weir JT, Schluter D (2008) Calibrating the avian molecular clock. Mol Ecol 17:2321–2328

    Article  CAS  PubMed  Google Scholar 

  • Winger BM, Hosner PA, Bravo GA, Cuervo AM, Aristizábal N, Cueto LE, Bates JM (2015) Inferring speciation history in the Andes with reduced-representation sequence data: an example in the Bay-backed Antpittas (Aves; Grallariidae; Grallaria hypoleuca s.l.). Mol Ecol 24:6256–6277

    Article  CAS  PubMed  Google Scholar 

  • Winterton C, Richardson JE, Hollingsworth M, Clark A, Zamora N, Pennington RT (2014) Historical biogeography of the Neotropical legume genus Dussia: the Andes, the Panama Isthmus and the Chocó. Paleobotany and biogeography: a festschrift for Alan Graham in his 80th year. Missouri Botanical Garden Press, St. Louis, pp 389–404

    Google Scholar 

  • Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Dissertation, University of Texas at Austin

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Acknowledgements

We wish to thank the following individuals and institutions for providing tissues and toe pads for this study: the Academy of Natural Sciences of Philadelphia (Nate Rice), the Field Museum of Natural History (David E. Willard and John Bates), and the National Museum of Natural History (James P. Dean and Storrs L. Olson), Louisiana State University Museum of Natural Science (Donna Dittman and Robb Brumfield), and the Natural History Museum of Denmark (Jon Fjeldså). E. Q. is extremely thankful to Joel Cracraft, John Bates, Eleanor Sterling, Nancy Simmons, and A. Townsend Peterson for making valuable comments and additions to earlier versions of this manuscript, as well as to two anonymous reviewers and the subject editor who suggested improvements to this final version. This paper was part of E. Q.’s doctoral dissertation. Research funding for E. Q.’s doctoral degree was provided by Fulbright, the OAS, the GSAS at Columbia University, the American Museum of Natural History Graduate Student Fellowship Program, CONACyT (145857), and the Frank. M. Chapman Memorial Fund of the American Museum of Natural History. Research funding for U. P. was provided by a Frank M. Chapman Postdoctoral Fellowship from the American Museum Of Natural History. This paper is a contribution from the Monell Molecular Laboratory and the Cullman Research Facility of the Department of Ornithology, American Museum of Natural History, and has received generous support from the Lewis B. and Dorothy Cullman Program for Molecular Systematics Studies, a joint initiative of the New York Botanical Garden, the American Museum of Natural History, and the Sackler Institute of Comparative Genomics.

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Communicated by J. T. Lifjeld.

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Quintero, E., Perktaş, U. Phylogeny and biogeography of a subclade of mangoes (Aves, Trochilidae). J Ornithol 159, 29–46 (2018). https://doi.org/10.1007/s10336-017-1486-z

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