Organisms Diversity & Evolution

, Volume 12, Issue 4, pp 433–444 | Cite as

Historical biogeography of tits (Aves: Paridae, Remizidae)

  • Dieter Thomas TietzeEmail author
  • Udayan Borthakur
Original Article


Tits (Aves: Paroidea) are distributed all over the northern hemisphere and tropical Africa, with highest species numbers in China and the Afrotropic. In order to find out if these areas are also the centers of origin, ancestral areas were reconstructed based on a molecular phylogeny. The Bayesian phylogenetic reconstruction was based on sequences for three mitochondrial genes and one nuclear gene. This phylogeny confirmed most of the results of previous studies, but also indicated that the Remizidae are not monophyletic and that, in particular, Cephalopyrus flammiceps is sister to the Paridae. Four approaches, parsimony- and likelihood-based ones, were applied to derive the areas occupied by ancestors of 75 % of the extant species for which sequence data were available. The common ancestor of the Paridae and the Remizidae inhabited tropical Africa and China. The Paridae, as well as most of its (sub)genera, originated in China, but Baeolophus originated in the Nearctic and Cyanistes in the Western Palearctic. Almost all biogeographic reconstruction methods produced similar results, but those which consider the likelihood of the transition from one area to another should be preferred.


Lagrange S-DIVA Weighted ancestral area analysis Mesquite ancestral states reconstruction package Passeriformes 



T.D. Price motivated this study. Many colleagues have shared their DNA sequences on GenBank. D.C. Outlaw explained how to perform Weighted Ancestral Area Analyses and C.D. Buchanan helped with coding this in R. J. Martens and M. Päckert shared their long-lasting experience on parid systematics and phylogeography as well as sequences for Cephalopyrus flammiceps with us and commented on an early draft of this paper. D.T.T. was funded by the Deutsche Forschungsgemeinschaft (Ti 679/1-1, Ti 679/2-1). Some sequencing was supported by the NSF (USA). Two reviewers and the (guest) editors helped to improve the paper. Many cordial thanks are owing to all friends, colleagues and organizations mentioned.

Supplementary material

13127_2012_101_MOESM1_ESM.pdf (226 kb)
ESM 1 (PDF 147 kb)


  1. Alström, P., Ericson, P. G. P., Olsson, U., et al. (2006). Phylogeny and classification of the avian superfamily Sylvioidea. Molecular Phylogenetics and Evolution, 38, 381–397.PubMedCrossRefGoogle Scholar
  2. Ancochea, E., Fuster, J. M., Ibarrola, E., et al. (1990). Volcanic evolution of the island of Tenerife (Canary Islands) in the light of new K-Ar data. Journal of Volcanology and Geothermal Research, 44, 231–249.CrossRefGoogle Scholar
  3. Barker, F. K., Cibois, A., Schikler, P., et al. (2004). Phylogeny and diversification of the largest avian radiation. Proceedings of the National Academy of Sciences of the United States of America, 101, 11040–11045.PubMedCrossRefGoogle Scholar
  4. Beresford, P., Barker, F. K., Ryan, P. G., et al. (2005). African endemics span the tree of songbirds (Passeri): molecular systematics of several evolutionary ‘enigmas’. Proceedings of the Royal Society of London B, 272, 849–858.CrossRefGoogle Scholar
  5. BirdLife International and NatureServe (2011). Bird species distribution maps of the world. Cambridge: BirdLife International and NatureServe.Google Scholar
  6. Bocheński, Z. (1998). Systematyczne implikacje oparte na budowie gniazd remizów [the nest building of penduline tits and its systematic implications]. Notatki Ornitologiczne, 39, 231–241.Google Scholar
  7. Bremer, K. (1992). Ancestral areas: a cladistic reinterpretation of the center of origin concept. Systematic Biology, 41, 436–445.Google Scholar
  8. Croizat, L., Nelson, G., & Rosen, D. E. (1974). Centers of origin and related concepts. Systematic Zoology, 23, 265–287.CrossRefGoogle Scholar
  9. Dai, C., Chen, K., Zhang, R., et al. (2010). Molecular phylogenetic analysis among species of Paridae, Remizidae and Aegithalos based on mtDNA sequences of COI and cyt b. Chinese Birds, 1, 112–123.CrossRefGoogle Scholar
  10. Darwin, C. (1859). On the origin of species by means of natural selection. London: John Murray.Google Scholar
  11. del Hoyo, J., Elliot, A., & Christie, D. (Eds.). (2007). Handbook of the birds of the world. Volume 12. Picathartes to tits and chickadees. Barcelona: Lynx Edicions.Google Scholar
  12. del Hoyo, J., Elliot, A., & Christie, D. (Eds.). (2008). Handbook of the birds of the world. Volume 13: Penduline tits to shrikes. Barcelona: Lynx Edicions.Google Scholar
  13. Dickinson, E. C. (Ed.). (2003). The Howard & Moore complete checklist of the birds of the world (3rd ed.). London: Christopher Helm.Google Scholar
  14. Dietzen, C., Garcia-del-Rey, E., Delgado Castro, G., et al. (2008). Phylogeography of the blue tit (Parus teneriffae-group) on the Canary Islands based on mitochondrial DNA sequence data and morphometrics. Journal of Ornithology, 149, 1–12.CrossRefGoogle Scholar
  15. Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.PubMedCrossRefGoogle Scholar
  16. Eck, S. (2006). The Palaearctic titmouse species (Aves: Paridae: Parus sensu lato) – a current survey. Zootaxa, 1325, 7–54.Google Scholar
  17. Eck, S., & Martens, J. (2006). Systematic notes on Asian birds. 49. A preliminary review of the Aegithalidae, Remizidae and Paridae. Zoologische Mededelingen (Leiden), 80–5, 1–63.Google Scholar
  18. Ekman, S. (1953). Zoogeography of the Sea. London: Sidgwick and Jackson.Google Scholar
  19. Frenzel, B. (1968). The pleistocene vegetation of Northern Eurasia. Science, 161, 637–649.PubMedCrossRefGoogle Scholar
  20. Gaston, K. J., & Blackburn, T. M. (1996). The tropics as a museum of biological diversity: an analysis of the New World avifauna. Proceedings of the Royal Society of London B, 263, 63–68.CrossRefGoogle Scholar
  21. Gill, F. B., Funk, D. H., & Silverin, B. (1989). Protein relationships among titmice (Parus). Wilson Bulletin, 101, 182–197.Google Scholar
  22. Gill, F. B., Mostrom, A., & Mack, A. L. (1993). Speciation in North American chickadees: I. Patterns of mtDNA genetic divergence. Evolution, 47, 195–212.CrossRefGoogle Scholar
  23. Gill, F. B., Slikas, B., & Sheldon, F. H. (2005). Phylogeny of titmice (Paridae): II. Species relationships based on sequences of the mitochondrial cytochrome-b gene. The Auk, 122, 121–143.CrossRefGoogle Scholar
  24. Gladenkov, A. Y., Oleinik, A. E., Marincovich, L., Jr., et al. (2002). A refined age for the earliest opening of Bering Strait. Palaeogeography, Palaeoclimatology, Palaeoecology, 183, 321–328.CrossRefGoogle Scholar
  25. Glutz von Blotzheim, U. N. (Ed.) (1993). Handbuch der Vögel Mitteleuropas. Band 13/I. Passeriformes (4. Teil). Muscicapidae – Paridae. Wiesbaden: Aula.Google Scholar
  26. Goldberg, E. E., Roy, K., Lande, R., et al. (2005). Diversity, endemism, and age distributions in macroevolutionary sources and sinks. The American Naturalist, 165, 623–633.PubMedCrossRefGoogle Scholar
  27. Greenwood, P. J., Harvey, P. H., & Perrins, C. M. (1979). The role of dispersal in the great tit (Parus major): the causes, consequences and heritability of natal dispersal. The Journal of Animal Ecology, 48, 123–142.CrossRefGoogle Scholar
  28. Grubb, T. C., & Pravosudov, V. V. (1994). Tufted titmouse (Parus bicolor). In A. Poole & F. Gill (Eds.), The birds of North America. No. 86. Washington, DC: AOU.Google Scholar
  29. Harrap, S., & Quinn, D. (1995). Chickadees, tits, nuthatches & treecreepers. Princeton, NJ: Princeton University Press.Google Scholar
  30. Hausdorf, B. (1998). Weighted ancestral area analysis and a solution of the redundant distribution problem. Systematic Biology, 47, 445–456.PubMedCrossRefGoogle Scholar
  31. Hewitt, G. M. (1996). Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society, 58, 247–276.Google Scholar
  32. Illera, J. C., Koivula, K., Broggi, J., et al. (2011). A multi-gene approach reveals a complex evolutionary history in the Cyanistes species group. Molecular Ecology, 20, 4123–4139.PubMedCrossRefGoogle Scholar
  33. James, H. F., Ericson, P. G. P., Slikas, B., et al. (2003). Pseudopodoces humilis, a misclassified terrestrial tit (Paridae) of the Tibetan Plateau: evolutionary consequences of shifting adaptive zones. Ibis, 145, 185–202.CrossRefGoogle Scholar
  34. Kodandaramaiah, U. (2010). Use of dispersal-vicariance analysis in biogeography – a critique. Journal of Biogeography, 37, 3–11.CrossRefGoogle Scholar
  35. Krijgsman, W., Hilgen, F. J., Raffi, I., et al. (1999). Chronology, causes and progression of the Messinian salinity crisis. Nature, 400, 652–655.CrossRefGoogle Scholar
  36. Kvist, L., Ruokonen, M., Orell, M., et al. (1996). Evolutionary patterns and phylogeny of tits and chickadees (genus Parus) based on the sequence of the mitochondrial cytochrome b gene. Ornis Fennica, 73, 145–156.Google Scholar
  37. Kvist, L., Martens, J., Ahola, A., et al. (2001). Phylogeography of a Palaearctic sedentary passerine, the willow tit (Parus montanus). Journal of Evolutionary Biology, 14, 930–941.CrossRefGoogle Scholar
  38. Kvist, L., Martens, J., Higuchi, H., et al. (2003). Evolution and genetic structure of the great tit (Parus major) complex. Proceedings of the Royal Society of London B, 270, 1447–1454.CrossRefGoogle Scholar
  39. Kvist, L., Broggi, J., Illera, J. C., et al. (2005). Colonisation and diversification of the blue tits (Parus caeruleus teneriffae-group) in the Canary Islands. Molecular Phylogenetics and Evolution, 34, 501–511.PubMedCrossRefGoogle Scholar
  40. Ladd, H. S. (1960). Origin of the Pacific island molluscan fauna. American Journal of Science, 258-A, 137–150.Google Scholar
  41. Löhrl, H. (1967). Zur verwandtschaftlichen Stellung von Cephalopyrus flammiceps auf Grund des Verhaltens. Bonner zoologische Beiträge, 18, 127–138.Google Scholar
  42. Löhrl, H. (1981). Verhaltensmerkmale der Familie Remizidae. Journal für Ornithologie, 122, 307–309.CrossRefGoogle Scholar
  43. Maddison, W. P., & Maddison, D. R. (2011). Mesquite: a modular system for evolutionary analysis. Version 2.75.
  44. Martens, J., & Eck, S. (1995). Towards an ornithology of the Himalayas. Systematics, ecology and vocalizations of Nepal birds. Bonner zoologische Monographien, 38, 247–251.Google Scholar
  45. Martens, J., & Schottler, B. (1991). Akustische Barrieren zwischen Blaumeise (Parus caeruleus) und Lasurmeise (Parus cyanus)? Journal für Ornithologie, 132, 61–80.CrossRefGoogle Scholar
  46. Martens, J., Ernst, S., & Petri, B. (1995). Reviergesänge ostasiatischer Weidenmeisen Parus montanus und ihre mikroevolutive Ableitung. Journal für Ornithologie, 136, 367–388.CrossRefGoogle Scholar
  47. Martens, J., Tietze, D. T., & Sun, Y.-H. (2006). Molecular phylogeny of Parus (Periparus), a Eurasian radiation of tits (Aves: Passeriformes: Paridae). Zoologische Abhandlungen (Dresden), 55, 103–120.Google Scholar
  48. Matthew, W. D. (1915). Climate and evolution. Annals of the New York Academy of Sciences, 24, 171–318.CrossRefGoogle Scholar
  49. McCain, C. M. (2009). Global analysis of bird elevational diversity. Global Ecology and Biogeography, 18, 346–360.CrossRefGoogle Scholar
  50. McCallum, D. A., Gill, F. B., & Gaunt, S. L. L. (2001). Community assembly patterns of parids along an elevational gradient in western China. Wilson Bulletin, 113, 53–64.CrossRefGoogle Scholar
  51. McCoy, E. D., & Heck, K. L., Jr. (1983). Centers of origin revisited. Paleobiology, 9, 17–19.Google Scholar
  52. Nylander, J. A. A. (2004). MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.Google Scholar
  53. Nylander, J. A., Olsson, U., Alström, P., et al. (2008). Accounting for phylogenetic uncertainty in biogeography: a Bayesian approach to dispersal-vicariance analysis of the thrushes (Aves: Turdus). Systematic Biology, 57, 257–268.PubMedCrossRefGoogle Scholar
  54. Päckert, M., & Martens, J. (2008). Taxonomic pitfalls in tits – comments on the Paridae chapter of the Handbook of the Birds of the World. Ibis, 150, 829–831.CrossRefGoogle Scholar
  55. Päckert, M., Martens, J., Nazarenko, A. A., et al. (2005). Parus major – a misclassified ring species. Biological Journal of the Linnean Society, 86, 153–174.CrossRefGoogle Scholar
  56. Päckert, M., Martens, J., Tietze, D. T., et al. (2007). Calibration of a molecular clock in tits (Paridae) – do nucleotide substitution rates of mitochondrial genes deviate from the 2% rule? Molecular Phylogenetics and Evolution, 44, 1–14.PubMedCrossRefGoogle Scholar
  57. Päckert, M., Martens, J., Sun, Y.-H., et al. (2012). Horizontal and elevational phylogeographic patterns of Himalayan and Southeast Asian forest passerines (Aves: Passeriformes). Journal of Biogeography, 39, 556–573.CrossRefGoogle Scholar
  58. Paradis, E., Baillie, S. R., Sutherland, W. J., & Gregory, R. D. (1998). Patterns of natal and breeding dispersal in birds. Journal of Animal Ecology, 67, 518–536.Google Scholar
  59. Paradis, E., Claude, J., & Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289–290.Google Scholar
  60. Pavlova, A., Rohwer, S., Drovetski, S. V., et al. (2006). Different post-pleistocene histories of Eurasian parids. The Journal of Heredity, 97, 389–402.PubMedCrossRefGoogle Scholar
  61. Price, T. D. (2010). The roles of time and ecology in the continental radiation of the Old World leaf warblers (Phylloscopus and Seicercus). Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 1749–1762.CrossRefGoogle Scholar
  62. Price, T. D., Mohan, D., Tietze, D. T., et al. (2011). Determinants of northerly range limits along the avian Himalayan diversity gradient. The American Naturalist, 178, S97–S108.PubMedCrossRefGoogle Scholar
  63. R Development Core Team (2011). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
  64. Rambaut, A. (2009). FigTree v1.3.1.
  65. Rambaut, A., & Drummond, A. J. (2007). Tracer v1.5.
  66. Ree, R. H., & Smith, S. A. (2008). Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology, 57, 4–14.PubMedCrossRefGoogle Scholar
  67. Ricklefs, R. E., & Schluter, D. (1993). Species diversity in ecological communities. Historical and geographical perspectives. Chicago: University of Chicago Press.Google Scholar
  68. Ronquist, F. (1997). Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology, 46, 195–203.CrossRefGoogle Scholar
  69. Salzburger, W., Martens, J., Nazarenko, A. A., et al. (2002a). Phylogeography of the Eurasian Willow Tit (Parus montanus) based on DNA sequences of the mitochondrial cytochrome b gene. Molecular Phylogenetics and Evolution, 24, 26–34.PubMedCrossRefGoogle Scholar
  70. Salzburger, W., Martens, J., & Sturmbauer, C. (2002b). Paraphyly of the Blue Tit (Parus caeruleus) suggested from cytochrome b sequences. Molecular Phylogenetics and Evolution, 24, 19–25.PubMedCrossRefGoogle Scholar
  71. Sheldon, F. H., & Gill, F. B. (1996). A reconsideration of songbird phylogeny, with emphasis on the evolution of titmice and their sylvioid relatives. Systematic Biology, 45, 473–495.CrossRefGoogle Scholar
  72. Slikas, B., Sheldon, F. H., & Gill, F. B. (1996). Phylogeny of titmice (Paridae): I. Estimate of relationships among subgenera based on DNA-DNA hybridization. Journal of Avian Biology, 27, 70–82.CrossRefGoogle Scholar
  73. Štorchová, Z., Landová, E., & Frynta, D. (2010). Why some tits store food and others do not: evaluation of ecological factors. Journal of Ethology, 28, 207–219.CrossRefGoogle Scholar
  74. Tamura, K., Peterson, D., Peterson, N., et al. (2011). MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.PubMedCrossRefGoogle Scholar
  75. Tietze, D. T., Martens, J., Sun, Y.-H., et al. (2011). Song evolution in the Coal Tit (Parus ater). Journal of Avian Biology, 42, 214–230.CrossRefGoogle Scholar
  76. Voelker, G., & Outlaw, R. K. (2008). Establishing a perimeter position: speciation around the Indian Ocean Basin. Journal of Evolutionary Biology, 21, 1779–1788.PubMedCrossRefGoogle Scholar
  77. Voelker, G., Rohwer, S., Outlaw, D. C., et al. (2009). Repeated trans-Atlantic dispersal catalysed a global songbird radiation. Global Ecology and Biogeography, 18, 41–49.CrossRefGoogle Scholar
  78. Weir, J. T., Bermingham, E., & Schluter, D. (2009). The Great American Biotic Interchange in birds. Proceedings of the National Academy of Sciences of the United States of America, 106, 21737–21742.PubMedCrossRefGoogle Scholar
  79. Wolters, H. E. (1980). Die Vogelarten der Erde. Eine systematische Liste mit Verbreitungsangaben sowie deutschen und englischen Namen. Pt. 5. Hamburg and Berlin: Parey.Google Scholar
  80. Yu, Y., Harris, A. J., & He, X. J. (2010). S-DIVA (Statistical Dispersal-Vicariance Analysis): a tool for inferring biogeographic histories. Molecular Phylogenetics and Evolution, 56, 848–850.PubMedCrossRefGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2012

Authors and Affiliations

  1. 1.Department of Ecology and EvolutionThe University of ChicagoChicagoUSA
  2. 2.Institut für Ökologie, Evolution und DiversitätGoethe-Universität Frankfurt am MainFrankfurt am MainGermany
  3. 3.Wildlife Genetics Laboratory, AaranyakGuwahatiIndia

Personalised recommendations