Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 4175 No. 1: 12 Oct. 2016
Type: Article
Published: 2016-10-12
DOI: 10.11646/zootaxa.4175.1.3
Page range: 23–42
Abstract views: 88
PDF downloaded: 1

A new member of the greater double-collared sunbird complex (Passeriformes: Nectariniidae) from the Eastern Arc Mountains of Africa

Museum of Vertebrate Zoology and Department of Integrative Biology, 3101 Valley Life Science Building, University of California, Berkeley, CA 94720, U.S.A. Percy FitzPatrick Institute, DST-NRF Centre of Excellence, University of Cape Town, Rondebosch 7701, South Africa
Center for Macroecology, Evloution and Climate, Natural History Museum, University of Copenhagen, DK-2100 Copenhagen, Denmark
P.O. Box 12993, Dar es Salaam, Tanzania (Deceased)
Center for Macroecology, Evloution and Climate, Natural History Museum, University of Copenhagen, DK-2100 Copenhagen, Denmark
Aves Rubeho Udzungwa Tanzania biodiversity hotspot microsatellite loci

Abstract

We document the discovery of the first population of greater double-collared sunbird (Cinnyris afer complex) from the Eastern Arc Mountains of Tanzania. We assessed phylogenetic relationships and taxonomic rank based on mtDNA sequence data, nine microsatellite loci and morphology. This new taxon, locally distributed in the Rubeho and Udzungwa Highlands, has close affinities (< 1% uncorrected sequence divergence) with C. whytei (split here from C. ludovicensis) of the Nyika Plateau in Malawi, but differs in having longer tarsi and in subtle plumage details. Although the birds from Nyika and Udzungwa-Rubeho are reciprocally monophyletic for mitochondrial DNA, coalescent analyses of the microsatellite data and the total molecular dataset could not reject the possibility of continued gene flow between the two populations. Thus, although we favour the phylogenetic species concept, we adopt a cautious approach and formally describe the Rubeho and Udzungwa greater double-collared sunbird population as a subspecies of Cinnyris whytei. This new sunbird taxon has been recorded only above 1700 m in scrub on the forest/grassland ecotone in a very restricted area in the Rubeho and Udzungwa Highlands of Tanzania. The effects of human settlement and agriculture threaten this taxon.

 

References

  1. Bowie, R.C.K. (2003) Birds, Molecules, and Evolutionary Patterns among Africa's Islands in the Sky. Ph.D. Thesis, University of Cape Town, Cape Town, 370 pp.

    Bowie, R.C.K., Fjeldså, J., Hackett, S.J. & Crowe, T.M. (2004a) Systematics and biogeography of Double-collared Sunbirds from the Eastern Arc Mountains, Tanzania. Auk, 121, 660–681.
    http://dx.doi.org/10.1642/0004-8038(2004)121[0660:SABODS]2.0.CO;2

    Bowie, R.C.K., Fjeldså, J., Hackett, S.J. & Crowe, T.M. (2004b) Molecular evolution in space and through time: mtDNA phylogeography of the Olive Sunbird (Nectarinia olivacea/obscura) throughout continental Africa. Molecular Phylogenetics and Evolution, 33, 56–76.
    http://dx.doi.org/10.1016/j.ympev.2004.04.013

    Bowie, R.C.K. & Fjeldså, J. (2005) Genetic and morphological evidence for two species in the Udzungwa forest partridge Xenoperdix udzungwensis. Journal of East African Natural History, 94, 191–201.
    http://dx.doi.org/10.2982/0012-8317(2005)94[191:GAMEFT]2.0.CO;2

    Bowie, R.C.K., Fjeldså, J., Hackett, S.J., Bates, J.M. & Crowe, T.M. (2006) Coalescent models reveal the relative roles of ancestral polymorphism, vicariance and dispersal in shaping phylogeographical structure of an African montane forest robin. Molecular Phylogenetics and Evolution, 38, 171–188.
    http://dx.doi.org/10.1016/j.ympev.2005.06.001

    Bowie, R.C.K., Fjeldså, J. & Kiure, J. (2009) Multilocus molecular DNA variation in Winifred's Warbler Scepomycter winifredae suggests cryptic speciation and the existence of a threatened species in the Rubeho-Ukaguru Mountains of Tanzania. Ibis, 151, 709–719.
    http://dx.doi.org/10.1111/j.1474-919X.2009.00954.x

    Bowie, R.C.K., Sellas, A.B. & Feldheim, K.A. (2010) Development of ten highly polymorphic microsatellite markers for sunbirds (Aves: Nectariniidae) with broad cross-amplification utility in at least eight species. Conservation Genetics, 11, 1159–1162.
    http://dx.doi.org/10.1007/s10592-009-9907-z

    Burgess, N.D., Butynski, T.M., Cordeiro, N.J., Doggart, N.H., Fjeldså, J., Howell, K.M., Kilahama, F.B., Loader, S.P., Lovett, J.C., Mbilinyi, B., Menegon, M., Moyer, D.C., Nashanda, E., Perkin, A., Rovero, F., Stanley, W.T. & Stuart, S.N. (2007) The biological importance of the Eastern Arc Mountains of Tanzania and Kenya. Biological Conservation, 134, 209–231.
    http://dx.doi.org/10.1016/j.biocon.2006.08.015

    Cheke, R.A. & Mann, C.F. (2008) Family Nectariniidae (Sunbirds). In: del Hoyo, J., Elliot, A. & Christie, D. (Eds.), Handbook of the Birds of the World. Vol. 13. Lynx Edicions, Barcelona, pp. 196–321.

    Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.

    Cracraft, J. (1983) Species concepts and speciation analysis. Current Ornithology, 1, 159–187.
    http://dx.doi.org/10.1007/978-1-4615-6781-3_6

    Crowe, T.M., Bowie, R.C.K., Bloomer, P., Mandiwana, T., Hedderson, T., Randi, E., Pereira, S.L. & Wakeling, J. (2006) Phylogenetics and biogeography of, and character evolution in gamebirds (Aves: Galliformes): effects of character exclusion, partitioning and missing data. Cladistics, 22, 495–532.
    http://dx.doi.org/10.1111/j.1096-0031.2006.00120.x

    De Queiroz, K. (1998) The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations. In: Howard, S.J. & Berlocher, S.H. (Eds.), Endless Forms: Species and Speciation. Oxford University Press, New York, pp. 57–75.

    De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 879–886.
    http://dx.doi.org/10.1080/10635150701701083

    Dickinson, E.C. & Christidis, L. (Eds.) (2014) The Howard and Moore Complete Checklist of the Birds of the World. Vol. 2. 4th Edition. Aves Press, Eastbourne, 752 pp.

    Dowsett-Lemaire, F. & Dowsett, R.J. (2006) The Birds of Malawi. Tauraco Press & Aves, Liège, 556 pp.

    Earl, D.A. & vonHoldt, B.M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359–361.
    http://dx.doi.org/10.1007/s12686-011-9548-7

    Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611–2620.
    http://dx.doi.org/10.1111/j.1365-294X.2005.02553.x

    Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequín 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics, 1, 47–50.

    Fjeldså, J. & Lovett, J.C. (1997) Geographical patterns of old and young species in African forest biota: the significance of specific montane areas as evolutionary centres. Biodiversity and Conservation, 6, 325–246.
    http://dx.doi.org/10.1023/A:1018356506390

    Fjeldså, J., Howell, K. & Andersen, M. (1997) An ornithological survey of the Rubeho Mountains, Tanzania. Scopus, 19, 73–82.

    Fjeldså, J., Bowie, R.C.K. & Kiure, J. (2006) The Forest Batis, Batis mixta, is two species: description of a new, narrowly distributed Batis species in the Eastern Arc biodiversity hotspot. Journal of Ornithology, 147, 578–590.
    http://dx.doi.org/10.1007/s10336-006-0082-4

    Fjeldså, J. & Bowie, R.C.K. (2008) New perspectives on the origin and diversification of Africa's forest avifauna. African Journal of Ecology, 46, 235–247.
    http://dx.doi.org/10.1111/j.1365-2028.2008.00992.x

    Fjeldså, J. & Burgess, N.D. (2008) The coincidence of biodiversity and human settlement in Africa. African Journal of Ecology, 46, 33–42.
    http://dx.doi.org/10.1111/j.1365-2028.2008.00927.x

    Fjeldså, J., Kiure, J., Doggart, N., Hansen, L.A. & Perkin, A. (2010) Distribution of highland forest birds across a potential dispersal barrier in the Eastern Arc Mountains of Tanzania. Steenstrupia, 32, 1–43.

    Fjeldså, J., Bowie, R.C.K. & Rahbek, R. (2012) The role of mountain ranges in the diversification of birds. Annual Review of Ecology, Evolution and Systematics, 43, 249–265.
    http://dx.doi.org/10.1146/annurev-ecolsys-102710-145113

    Fry, C.H., Keith, S. & Urban, E.K. (Eds) (2000) The Birds of Africa Vol. VI. Academic Press, London, 724 pp.

    Gill, F. & Donsker, D. (Eds.) (2016) IOC World Bird List (v. 6.2). Available from: http://www.worldbirdnames.org/ioc-lists/crossref/ (Accessed 28 May 2016)
    http://dx.doi.org/10.14344/IOC.ML.6.2

    Griffiths, C.J. (1993) The geological history of East Africa. In: Lovett, J.C. & Wasser, S.K. (Eds.), Biogeography and Ecology of the Rain Forest of Eastern Africa. Cambridge University Press, Cambridge, pp. 9–22.
    http://dx.doi.org/10.1017/CBO9780511895692.002

    Hey, J. & Nielson, R. (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proceedings of the National Academy of Science USA, 104, 2785–2790.
    http://dx.doi.org/10.1073/pnas.0611164104

    Hubisz, M.J., Falush, D., Stephens, M. & Pritchard, J.K. (2009) Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources, 9, 1322–1332.
    http://dx.doi.org/10.1111/j.1755-0998.2009.02591.x

    Hunt, J.S., Bermingham, E. & Ricklefs, R.E. (2001) Molecular systematics and biogeography of Antillean thrashers, tremblers, and mockingbirds (Aves: Mimidae). Auk, 118, 35–55.
    http://dx.doi.org/10.1642/0004-8038(2001)118[0035:MSABOA]2.0.CO;2

    Jakobsson, M. & Rosenberg, N.A. (2007) CLUMPP: a cluster matching and permutation program for dealing with multimodality in analysis of population structure. Bioinformatics, 23, 1801–1806.
    http://dx.doi.org/10.1093/bioinformatics/btm233

    Johansson, U.S., Fjeldså, J. & Bowie, R.C.K. (2008) Phylogenetic relationships within Passerida (Aves: Passeriformes): a review and a new molecular phylogeny based on three nuclear intron markers. Molecular Phylogenetics and Evolution, 48, 858–876.
    http://dx.doi.org/10.1016/j.ympev.2008.05.029

    Klicka, J., Zink, R.M., Barlow, J.C., McGillivray, W.B. & Doyle, T.J. (1999) Evidence supporting the recent origin and species status of the Timberline Sparrow. Condor, 101, 577–588.
    http://dx.doi.org/10.2307/1370187

    Lovett, J.C. & Wasser, S.K. (Eds.) (1993) Biogeography and Ecology of the Rain Forest of Eastern Africa. Cambridge University Press, Cambridge, 341 pp.
    http://dx.doi.org/10.1017/CBO9780511895692

    Marchant, R., Mumbi, C.T., Behera, S. & Yamagata, T. (2007) The Indian Ocean Dipole–The unsung driver of climatic variability in East Africa. African Journal of Ecology, 45, 4–16.
    http://dx.doi.org/10.1111/j.1365-2028.2006.00707.x

    Mayr, E. (1942) Systematics and the Origin of Species. Columbia University Press, New York, 334 pp.

    McEntee, J.P., Peñalba, J.V., Werema, C., Mulungu, E., Mbilinyi, M., Moyer, D., Hansen, L., Fjeldså, J. & Bowie, R.C.K. (2016) Social selection parapatry in Afrotropical sunbirds. Evolution, 70 (6), 1307–1321.
    http://dx.doi.org/10.1111/evo.12950

    Miller, M.A., 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, New Orleans, pp. 1–8.
    http://dx.doi.org/10.1109/gce.2010.5676129

    Mittermeier, R.A., Gil, P.R., Hoffman, M., Pilgrim, J., Brooks, T, Mittermeier, C.G., Lamoreux, J. & da Fonseca, G.A.B. (2005) Hotspots Revisited: Earth’s Biologically Richest and Most Endangered Terrestrial Ecoregions. Conservation International, Washington, D.C., 391 pp.

    Mumbi, C.T., Marchant, R., Hooghiemstra, H. & Wooller, M.J. (2008) Late Quaternary vegetation reconstruction from the Eastern Arc Mountains, Tanzania. Quaternary Research, 69, 326–341.
    http://dx.doi.org/10.1016/j.yqres.2007.10.012

    Pritchard, J.K., Stephens, K. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.

    Raymond, M. & Rousset, F. (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248–249.

    Ribeiro, A., Lloyd, P., Feldheim, K.A. & Bowie, R.C.K. (2012) Microgeographic socio-genetic structure of an African cooperative breeding passerine revealed. Molecular Ecology, 21, 662–672.
    http://dx.doi.org/10.1111/j.1365-294X.2011.05236.x

    Ridgway, R. (1912) Color Standards and Color Nomenclature. United States National Museum, Washington, D.C., 42 pp. + LIII plates.
    http://dx.doi.org/10.5962/bhl.title.62375

    Rousset, F. (2008) Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources, 8, 103–106.
    http://dx.doi.org/10.1111/j.1471-8286.2007.01931.x

    Stamatakis, A. (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.
    http://dx.doi.org/10.1093/bioinformatics/btl446

    Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxMLweb-servers. Systematic Biology, 75, 758–771.
    http://dx.doi.org/10.1080/10635150802429642

    Swofford, D.L. (2002) PAUP*10b: Phylogenetic Analysis Using Parsimony (*And Other Methods). Sinauer Associates, Sutherland, Massachusetts. Computer Software.

    Tello, J.G. & Bates, J.M. (2007) Molecular phylogenetics of the tody-tyrant and flatbill assemblage of tyrant flycatchers (Tyrannidae). Auk, 124, 134–154.
    http://dx.doi.org/10.1642/0004-8038(2007)124[134:MPOTTA]2.0.CO;2

    Tolley, K.A., Tilbury, C.R., Measey, G.J., Menegon, M., Branch, W.R. & Matthee, C.A. (2011) Ancient forest fragmentation or recent radiation? Testing refugial speciation models in chameleons within an African biodiversity hotspot. Journal of Biogeography, 38, 1748–1760.
    http://dx.doi.org/10.1111/j.1365-2699.2011.02529.x

    Voelker, G., Outlaw, R.K. & Bowie, R.C.K. (2010) Pliocene forest dynamics as a primary driver of African bird speciation. Global Ecology and Biogeography, 19, 111–121.
    http://dx.doi.org/10.1111/j.1466-8238.2009.00500.x