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Niche filling slows the diversification of Himalayan songbirds

Nature volume 509, pages 222–225 (2014)Cite this article

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Abstract

Speciation generally involves a three-step process—range expansion, range fragmentation and the development of reproductive isolation between spatially separated populations1,2. Speciation relies on cycling through these three steps and each may limit the rate at which new species form1,3. We estimate phylogenetic relationships among all Himalayan songbirds to ask whether the development of reproductive isolation and ecological competition, both factors that limit range expansions4, set an ultimate limit on speciation. Based on a phylogeny for all 358 species distributed along the eastern elevational gradient, here we show that body size and shape differences evolved early in the radiation, with the elevational band occupied by a species evolving later. These results are consistent with competition for niche space limiting species accumulation5. Even the elevation dimension seems to be approaching ecological saturation, because the closest relatives both inside the assemblage and elsewhere in the Himalayas are on average separated by more than five million years, which is longer than it generally takes for reproductive isolation to be completed2,3,6; also, elevational distributions are well explained by resource availability, notably the abundance of arthropods, and not by differences in diversification rates in different elevational zones. Our results imply that speciation rate is ultimately set by niche filling (that is, ecological competition for resources), rather than by the rate of acquisition of reproductive isolation.

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Figure 1: Phylogeny and species distributions.
Figure 2: Morphological evolution.
Figure 3: Phylogenetic and morphological diversity along the elevational gradient.
Figure 4: Species richness and resource abundance.

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References

  1. Mayr, E. & Diamond, J. M. The Birds of Northern Melanesia: Speciation, Ecology, and Biogeography (Oxford Univ. Press, 2001)

    Google Scholar 

  2. Price, T. Speciation in Birds (Roberts, 2008)

    Google Scholar 

  3. Weir, J. T. & Price, T. D. Limits to speciation inferred from times to secondary sympatry and ages of hybridizing species along a latitudinal gradient. Am. Nat. 177, 462–469 (2011)

    Article  PubMed  Google Scholar 

  4. Goldberg, E. E. & Lande, R. Ecological and reproductive character displacement on an environmental gradient. Evolution 60, 1344–1357 (2006)

    PubMed  Google Scholar 

  5. Harvey, P. H. & Rambaut, A. Comparative analyses for adaptive radiations. Phil. Trans. R. Soc. Lond. B 355, 1599–1605 (2000)

    Article  CAS  Google Scholar 

  6. Price, T. D. & Bouvier, M. M. The evolution of F1 postzygotic incompatibilities in birds. Evolution 56, 2083–2089 (2002)

    Article  PubMed  Google Scholar 

  7. Rosenzweig, M. L. Species Diversity in Space and Time (Cambridge Univ. Press, 1995)

    Book  Google Scholar 

  8. Endler, J. A. Geographic Variation, Speciation, and Clines (Princeton Univ. Press, 1977)

    Google Scholar 

  9. Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 (2000)

    Article  Google Scholar 

  10. Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, 2000)

    Google Scholar 

  11. Grant, P. R. & Grant, B. R. How and Why Species Multiply (Princeton Univ. Press, 2008)

    MATH  Google Scholar 

  12. Yoder, J. B. et al. Ecological opportunity and the origin of adaptive radiations. J. Evol. Biol. 23, 1581–1596 (2010)

    Article  CAS  PubMed  Google Scholar 

  13. Johansson, U. S. et al. Build-up of the Himalayan avifauna through immigration: a biogeographical analysis of the Phylloscopus and Seicercus warblers. Evolution 61, 324–333 (2007)

    Article  PubMed  Google Scholar 

  14. Richman, A. D. & Price, T. Evolution of ecological differences in the Old World leaf warblers. Nature 355, 817–821 (1992)

    Article  ADS  CAS  PubMed  Google Scholar 

  15. Ghosh-Harihar, M. & Price, T. D. A test for community saturation along the Himalayan bird diversity gradient, based on within-species geographical variation. J. Anim. Ecol. 628–638 (2014)

  16. Jønsson, K. A., Fabre, P. H., Ricklefs, R. E. & Fjeldså, J. A major global radiation of corvoid birds originated in the proto-Papuan archipelago. Proc. Natl Acad. Sci. USA 108, 2328–2333 (2011)

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  17. Päckert, M. et al. Horizontal and elevational phylogeographic patterns of Himalayan and Southeast Asian forest passerines (Aves: Passeriformes). J. Biogeogr. 39, 556–573 (2012)

    Article  Google Scholar 

  18. Kennedy, J. D. et al. Ecological limits on diversification of the Himalayan core Corvoidea. Evolution 66, 2599–2613 (2012)

    Article  PubMed  Google Scholar 

  19. Price, T. D. The roles of time and ecology in the continental radiation of the Old World leaf warblers (Phylloscopus and Seicercus) . Phil. Trans. R. Soc. Lond. B 365, 1749–1762 (2010)

    Article  Google Scholar 

  20. Wiens, J. J., Parra-Olea, G., Garcia-Paris, M. & Wake, D. B. Phylogenetic history underlies elevational biodiversity patterns in tropical salamanders. Proc. R. Soc. Lond. B 274, 919–928 (2007)

    CAS  Google Scholar 

  21. Price, T. D. et al. Determinants of northerly range limits along the Himalayan bird diversity gradient. Am. Nat. 178, S97–S108 (2011)

    Article  PubMed  Google Scholar 

  22. MacArthur, R. H. Patterns of species diversity. Biol. Rev. Camb. Philos. Soc. 40, 510–533 (1965)

    Article  Google Scholar 

  23. Ricklefs, R. E. Species richness and morphological diversity of passerine birds. Proc. Natl Acad. Sci. USA 109, 14482–14487 (2012)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  24. Rosenzweig, M. L. & Abramsky, Z. in Species Diversity in Ecological Communities (eds Ricklefs, R. E. & Schluter, D. ) 52–65 (Univ. Chicago, 1993)

    Google Scholar 

  25. Rabosky, D. L. & Matute, D. R. Macroevolutionary speciation rates are decoupled from the evolution of intrinsic reproductive isolation in Drosophila and birds. Proc. Natl Acad. Sci. USA 110, 15354–15359 (2013)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  26. Cornell, H. V. Is regional species diversity bounded or unbounded? Biol. Rev. Camb. Phil. Soc. 88, 140–165 (2013)

    Article  Google Scholar 

  27. Ricklefs, R. E. & Bermingham, E. The concept of the taxon cycle in biogeography. Glob. Ecol. Biogeogr. 11, 353–361 (2002)

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E. & Challenger, W. GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129–131 (2008)

    CAS  PubMed  Google Scholar 

  30. Helmus, M. R., Bland, T. J., Williams, C. K. & Ives, A. R. Phylogenetic measures of biodiversity. Am. Nat. 169, E68–E83 (2007)

    Article  PubMed  Google Scholar 

  31. Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012)

    Article  ADS  CAS  PubMed  Google Scholar 

  32. Price, T. Correlated evolution and independent contrasts. Phil. Trans. R. Soc. Lond. B 352, 519–529 (1997)

    Article  ADS  CAS  Google Scholar 

  33. Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005)

    Article  Google Scholar 

  34. Losos, J. B. Adaptive radiation, ecological opportunity, and evolutionary determinism. Am. Nat. 175, 623–639 (2010)

    Article  PubMed  Google Scholar 

  35. Mayr, E. Systematics and the Origin of Species from the Viewpoint of a Zoologist (Columbia Univ. Press, 1942)

    Google Scholar 

  36. Nosil, P. Ecological Speciation (Oxford Univ. Press, 2012)

    Book  Google Scholar 

  37. Price, T., Zee, J., Jamdar, K. & Jamdar, N. Bird species diversity along the Himalayas: a comparison of Himachal Pradesh with Kashmir. J. Bombay Nat. Hist. Soc. 100, 394–409 (2003)

    Google Scholar 

  38. Harvey, P. H., May, R. M. & Nee, S. Phylogenies without fossils. Evolution 48, 523–529 (1994)

    Article  PubMed  Google Scholar 

  39. Phillimore, A. B. & Price, T. D. Density-dependent cladogenesis in birds. PLoS Biol. 6, 483–489 (2008)

    Article  CAS  Google Scholar 

  40. Phillimore, A. B. & Price, T. D. in Speciation and Patterns of Diversity (eds Butlin, R. K., Bridle, J. & Schluter, D. ) 240–256 (Cambridge Univ. Press, 2009)

    Google Scholar 

  41. Weir, J. T. Divergent patterns of species accumulation in lowland and highland neotropical birds. Evolution 60, 842–855 (2006)

    Article  PubMed  Google Scholar 

  42. Etienne, R. S. & Rosindell, J. Prolonging the past counteracts the pull of the present: protracted speciation can explain observed slowdowns in diversification. Syst. Biol. 61, 204–213 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  43. Pybus, O. G. & Harvey, P. H. Testing macro-evolutionary models using incomplete molecular phylogenies. Proc. R. Soc. Lond. B 267, 2267–2272 (2000)

    Article  CAS  Google Scholar 

  44. McPeek, M. A. The ecological dynamics of clade diversification and community assembly. Am. Nat. 172, E270–E284 (2008)

    Article  PubMed  Google Scholar 

  45. Rabosky, D. L. Diversity-dependence, ecological speciation, and the role of competition in macroevolution. Annu. Rev. Ecol. Evol. Syst. 44, 481–502 (2013)

    Article  Google Scholar 

  46. Ricklefs, R. E. Community diversity: relative roles of local and regional processes. Science 235, 167–171 (1987)

    Article  ADS  CAS  PubMed  Google Scholar 

  47. Coyne, J. A. & Price, T. D. Little evidence for sympatric speciation in island birds. Evolution 54, 2166–2171 (2000)

    Article  CAS  PubMed  Google Scholar 

  48. Gill, F. B. Ecology and evolution of sympatric Mascarene white-eyes, Zosterops borbonica and Zosterops olivacea . Auk 88, 35–60 (1971)

    Article  Google Scholar 

  49. Badgley, C. et al. Ecological changes in Miocene mammalian record show impact of prolonged climatic forcing. Proc. Natl Acad. Sci. USA 105, 12145–12149 (2008)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  50. Revell, L. J. Size-correction and principal components for interspecific comparative studies. Evolution 63, 3258–3268 (2009)

    Article  PubMed  Google Scholar 

  51. Beaulieu, J. M., Jhwueng, D. C., Boettiger, C. & O'Meara, B. C. Modeling stabilizing selection: expanding the Ornstein-Uhlenbeck model of adaptive evolution. Evolution 66, 2369–2383 (2012)

    Article  PubMed  Google Scholar 

  52. Butler, M. A. & King, A. A. Phylogenetic comparative analysis: a modeling approach for adaptive evolution. Am. Nat. 164, 683–695 (2004)

    Article  PubMed  Google Scholar 

  53. Ricklefs, R. E. Cladogenesis and morphological diversification in passerine birds. Nature 430, 338–341 (2004)

    Article  ADS  CAS  PubMed  Google Scholar 

  54. Blomberg, S. P., Garland, T. & Ives, A. R. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745 (2003)

    Article  PubMed  Google Scholar 

  55. Kembel, S. W. et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010)

    Article  CAS  PubMed  Google Scholar 

  56. Mahler, D. L., Revell, L. J., Glor, R. E. & Losos, J. B. Ecological opportunity and the rate of morphological evolution in the diversification of Greater Antillean Anoles. Evolution 64, 2731–2745 (2010)

    Article  PubMed  Google Scholar 

  57. Rasmussen, P. C. & Anderton, J. C. Birds of South Asia: the Ripley Guide (Lynx, 2005)

    Google Scholar 

  58. Weir, J. T. & Schluter, D. The latitudinal gradient in recent speciation and extinction rates of birds and mammals. Science 315, 1574–1576 (2007)

    Article  ADS  CAS  PubMed  Google Scholar 

  59. Dong, F., Li, S. H. & Yang, X. J. Molecular systematics and diversification of the Asian scimitar babblers (Timaliidae, Aves) based on mitochondrial and nuclear DNA sequences. Mol. Phylogenet. Evol. 57, 1268–1275 (2010)

    Article  CAS  PubMed  Google Scholar 

  60. Groth, J. G. & Barrowclough, G. F. Basal divergences in birds and the phylogenetic utility of the nuclear RAG-1 gene. Mol. Phylogenet. Evol. 12, 115–123 (1999)

    Article  CAS  PubMed  Google Scholar 

  61. Nylander, J. A. A., Ronquist, F., Huelsenbeck, J. P. & Nieves-Aldrey, J. L. Bayesian phylogenetic analysis of combined data. Syst. Biol. 53, 47–67 (2004)

    Article  PubMed  Google Scholar 

  62. Swofford, D. L. PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods) Version 4 (Sinauer, 2003)

    Google Scholar 

  63. Ayres, D. L. et al. BEAGLE: an application programming interface and high-performance computing library for statistical phylogenetics. Syst. Biol. 61, 170–173 (2012)

    Article  PubMed  Google Scholar 

  64. Linder, H. P., Hardy, C. R. & Rutschmann, F. Taxon sampling effects in molecular clock dating: an example from the African Restionaceae. Mol. Phylogenet. Evol. 35, 569–582 (2005)

    Article  CAS  PubMed  Google Scholar 

  65. Rambaut, A. & Drummond, A. J. Tracer v1.4. http://beast.bio.ed.ac.uk/ (2007)

  66. Weir, J. T. & Schluter, D. Calibrating the avian molecular clock. Mol. Ecol. 17, 2321–2328 (2008)

    Article  CAS  PubMed  Google Scholar 

  67. Hackett, S. J. et al. A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768 (2008)

    Article  ADS  CAS  PubMed  Google Scholar 

  68. Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004)

    Article  CAS  PubMed  Google Scholar 

  69. Mayr, G. The age of the crown group of passerine birds and its evolutionary significance—molecular calibrations versus the fossil record. Syst. Biodivers. 11, 7–13 (2013)

    Article  Google Scholar 

  70. Hansen, J. et al. Target atmospheric CO2: where should humanity aim? Open Atmos. Sci. J. 2, 217–231 (2008)

    Article  ADS  CAS  Google Scholar 

  71. Kraatz, B. P. & Geisler, J. H. Eocene-Oligocene transition in Central Asia and its effects on mammalian evolution. Geology 38, 111–114 (2010)

    Article  ADS  Google Scholar 

  72. Helmus, M. R. & Ives, A. R. Phylogenetic diversity-area curves. Ecology 93, S31–S43 (2012)

    Article  Google Scholar 

  73. Laliberté, E. & Legendre, P. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91, 299–305 (2010)

    Article  PubMed  Google Scholar 

  74. Laliberté, E. & Shipley, B. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1. 0-11, http://cran.r-project.org/web/packages/FD/index.html (2011)

  75. Acharya, B. K., Sanders, N. J., Vijayan, L. & Chettri, B. Elevational gradients in bird diversity in the eastern Himalaya: an evaluation of distribution patterns and their underlying mechanisms. PLoS ONE 6, e29097 (2011)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  76. Gross, S. & Price, T. Determinants of the northern and southern range limits of a warbler. J. Biogeogr. 27, 869–878 (2000)

    Article  Google Scholar 

  77. Ghosh-Harihar, M. Distribution and abundance of foliage-arthropods across elevational gradients in the east and west Himalayas. Ecol. Res. 28, 125–130 (2013)

    Article  Google Scholar 

  78. Pebesma, E. J. & Bivand, R. S. Classes and methods for spatial data in R. R News 5 http://cran.r-project.org/doc/Rnews/ (2005)

  79. Bivand, R. S., Pebesma, E. J. & Gomez-Rubio, V. Applied Spatial Data Analysis with R. (Springer, 2008)

    MATH  Google Scholar 

  80. Hijmans, R. J. & van Etten, J. Raster: geographic analysis and modeling with raster data. R package version 1. 9-92, http://CRAN.R-project.org (2011)

  81. Schnute, J. T., Boers, N. M. & Haigh, R. PBS Mapping 2: user’s guide. Can. Tech. Rep. Fish. Aquat. Sci. 2549, 126 (2004)

  82. Rahbek, C. The elevational gradient of species richness—a uniform pattern. Ecography 18, 200–205 (1995)

    Article  Google Scholar 

  83. McCain, C. M. Global analysis of bird elevational diversity. Glob. Ecol. Biogeogr. 18, 346–360 (2009)

    Article  Google Scholar 

  84. Terborgh, J. Bird species diversity on an Andean elevational gradient. Ecology 58, 1007–1019 (1977)

    Article  Google Scholar 

  85. Sanders, N. J. & Rahbek, C. The patterns and causes of elevational diversity gradients. Ecography 35, 1–3 (2012)

    Article  Google Scholar 

  86. Grytnes, J. A. & Vetaas, O. R. Species richness and altitude: a comparison between null models and interpolated plant species richness along the Himalayan altitudinal gradient, Nepal. Am. Nat. 159, 294–304 (2002)

    Article  PubMed  Google Scholar 

  87. Hawkins, B. A., Diniz, J. A. F. & Weis, A. E. The mid-domain effect and diversity gradients: is there anything to learn? Am. Nat. 166, E140–E143 (2005)

    Article  PubMed  Google Scholar 

  88. Zapata, F. A., Gaston, K. J. & Chown, S. L. The mid-domain effect revisited. Am. Nat. 166, E144–E148 (2005)

    Article  PubMed  Google Scholar 

  89. Colwell, R. K., Rahbek, C. & Gotelli, N. J. The mid-domain effect: there’s a baby in the bathwater. Am. Nat. 166, E149–E154 (2005)

    Article  Google Scholar 

  90. McCain, C. M. The mid-domain effect applied to elevational gradients: species richness of small mammals in Costa Rica. J. Biogeogr. 31, 19–31 (2004)

    Article  Google Scholar 

  91. Grytnes, J. A., Heegaard, E. & Romdal, T. S. Can the mass effect explain the mid-altitudinal peak in vascular plant species richness? Basic Appl. Ecol. 9, 373–382 (2008)

    Article  Google Scholar 

  92. White, E. P. & Hurlbert, A. H. The combined influence of the local environment and regional enrichment on bird species richness. Am. Nat. 175, E35–E43 (2010)

    Article  PubMed  Google Scholar 

  93. Terborgh, J. W. & Faaborg, J. Saturation of bird communities in the West Indies. Am. Nat. 116, 178–195 (1980)

    Article  Google Scholar 

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Acknowledgements

We thank the government of India and the Chief Wildlife Wardens of the six Indian Himalayan states for permits. We also thank S. Dalvi, K. Jamdar, N. Jamdar, E. Scordato and D. Wheatcroft for help in the field, U. Borthakur and V. Mathur in the laboratory and E. Goldberg, R. Hudson, J. Kennedy, M. McPeek, A. Phillimore, D. Schluter, T. Tyrberg and J. Weir for advice. Tissue and toe pads for this project were provided by J. Cracraft (American Museum of Natural History), N. Rice (Academy of Natural Sciences, Philadelphia), M. Adams (The Natural History Museum, Tring), J. Dumbacher and M. Flannery (California Academy of Sciences), J. Bates and D. Willard (Field Museum of Natural History, Chicago), Herman Mays (Cincinnatti Museum); M. Wink (Institut für Pharmazie und Molekulare Biotechnologie, Heidelberg); R. Brumfeld and D. Dittmann (Lousiana State Museum of Zoology); S. Edwards (Museum of Natural History, Harvard); G. Frisk (Swedish Museum of Natural History, Stockholm); J. Dean and J. Rappole (National Museum of Natural History Smithsonian); S. Birks (Burke Museum, University of Washington); the Zoologisches Forschungmuseum Alexander Koenig, Bonn; J. Bolding Kristensen and J. Fjeldså (Zoological Museum, Copenhagen); the Zoologische Staatssammlung München, Munich; and K. Zyskowski (Yale University). This work was supported in part by grants from the US NSF and the National Geographic Society (TDP), the Jornvall Foundation, a Chinese Academy of Sciences Visiting Professorship (to P.A.), the Swedish Research Council (grants to U.O. and P.A.), the Wenner-Gren Foundation (a grant to U.S.J.), the Feldbausch Foundation of Mainz University (a grant to J.M.) and the German DFG (grants to B.H. and D.T.T., grant number Ti 679/1-1). We thank D. Tautz for making laboratory facilities available in Germany.

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Authors and Affiliations

  1. Department of Ecology and Evolution, University of Chicago, Chicago, 60637, Illinois, USA

    Trevor D. Price, Daniel M. Hooper, Caitlyn D. Buchanan, Ulf S. Johansson & D. Thomas Tietze

  2. Department of Zoology, Swedish Museum of Natural History, Stockholm, 10405, Sweden

    Ulf S. Johansson

  3. Institute of Pharmacy and Molecular Biotechnology, University of Heidelberg, Im Neuenheimer Feld 364, 69120 Heidelberg, Germany ,

    D. Thomas Tietze

  4. Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China ,

    Per Alström

  5. Swedish Species Information Centre, Swedish University of Agricultural Sciences, Box 7007, 75007 Uppsala, Sweden ,

    Per Alström

  6. Department of Biology and Environmental Sciences, Systematics and Biodiversity, University of Gothenburg, Gothenburg, 40530, Sweden

    Urban Olsson

  7. Wildlife Institute of India, PO Box 18, Chandrabani, Dehradun 248001, India ,

    Mousumi Ghosh-Harihar, Farah Ishtiaq, Sandeep K. Gupta, Pratap Singh & Dhananjai Mohan

  8. Institute of Zoology, Johannes Gutenberg University, Mainz, 55099, Germany

    Jochen Martens

  9. Max Planck Institute for Evolutionary Biology, August Thienemannstrasse 2, 24306 Plön, Germany ,

    Bettina Harr

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  1. Trevor D. Price
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Contributions

Study design and fieldwork: T.D.P. and D.M. Logistics: D.M. and P.S. Field collections: D.T.T., D.M.H., U.S.J., P.A., U.O., F.I., J.M., D.M. and T.D.P. Sequencing: D.M.H., U.S.J., D.T.T., U.O., P.A. and B.H. Arthropod censuses: M.G.-H. and T.D.P. Phylogeny construction: D.M.H., with early input from D.T.T. and P.A. Museum measurements: C.D.B., D.M., T.D.P. and U.S.J. Analysis and manuscript preparation: T.D.P., with input from B.H., D.M., D.M.H., D.T.T., P.A., U.S.J. and U.O.

Corresponding author

Correspondence to Trevor D. Price.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 The speciation cycle.

A species distributed across space becomes fragmented as a result of either vicariance (illustrated) or dispersal. After barrier formation, reproductive isolation develops. For the cycle to continue at least one of the species must expand into the other’s range, which requires reproductive isolation, and generally also ecological compatibility.

Extended Data Figure 2 Close relatives of a single Himalayan species, the Oriental white-eye, Zosterops palpebrosus.

Only species for which sequence data are available are included (tree from ref. 31). The range of Z. palpebrosus (light red) overlaps with members of the clade containing the lower 5 species, for example, with Z. japonicus (which is migratory) (light green) in eastern China and Z. atricapilla (red) and Z. montanus (blue) in Indonesia, where Z. palpebrosus is altitudinally segregated from them. Within the Z. palpebrosus clade, all species are allopatric replacements, except for the two species on the Mascarene Islands (bracketed). The timeline is from ref. 31.

Extended Data Figure 3 Plot of lineage versus time and morphological disparity generated in a simple model of ecological controls32.

In this model, new niches appear uniformly through time, and new species arise to fill them, with the criterion that new species are always derived from the ecologically most similar form5,32. For this simulation, the position of a new niche was drawn from a bivariate normal (x, y) with a correlation of 0.5, with 380 niches appearing sequentially and uniformly spaced in time. The result is a linear accumulation of species through time (that is, a downturn on the log scale), and most of the morphological variation accumulating early in the radiation (in the plot, disparity for one variable is shown).

Extended Data Figure 4 Disparity plots for morphology and habitat, with the null Brownian-motion model added.

The large shaded area represents the 95% confidence limit from 100 simulations on 100 trees drawn from the posterior distribution of the Bayesian analysis. The shaded areas around the data plots gives the 95% confidence limits based on phylogenetic uncertainty (based on the same 100 trees as above).

Extended Data Figure 5 Slowdowns in morphological evolution across the tree of the east Himalayan oscines.

a, Maximum likelihood breakpoints (the point in time at which one rate becomes favoured over the other) and changes in rate for two-rate models of morphological evolution. Significance values (*P < 0.01, **P < 0.001) refer to likelihood ratio tests comparing the one- and two-rate Brownian motion models (PC2, P = 0.16). 95% support limits (parentheses) were derived from likelihood profiles averaged across 100 trees sampled from the posterior distribution of Bayesian trees. b, The likelihood profile for evolution of the first shape index (PC1). The likelihood for each (x, y) combination was obtained as the average across 100 trees, then log-transformed for the figure. Numbers are the difference in log-likelihood from the maximum (×100). Only values less than 2 units are shown. The profiles are indicated by symbols (squares for the breakpoint, and circles for the rate difference). c, Relative weights of Ornstein–Uhlenbeck (OU) and Brownian-motion models of morphological evolution at different timelines, based on phylogenetically corrected principal components (revellePCs) (see text). d, Correlations of PC scores with the original (log-transformed) variables.

Extended Data Figure 6 Plot of lineage diversity (on a linear scale) versus time for a phylogeny connecting all species present at 500 m and at 3,000 m.

Eighty-two species are estimated to straddle each of these elevational bands.

Extended Data Figure 7 Morphology at specified elevations.

Grey lines are the convex hull for all species in the study area (points as in Fig. 2). Black lines are the convex hulls for all species whose elevational ranges include the specified band. Blue lines are the convex hulls for all the species censused on 5-hectare grids at those elevations (see the source data, in order of elevation, B2, A3, B1 and G1), and green lines are the convex hulls for all common (>5 pairs per hectare) species on those grids. Number of species is the number of all bird species in that elevational belt, plus (in parentheses) the number of songbirds censused on the grid.

Extended Data Figure 8 Climate data (from http://worldclim.org33).

The top panel shows precipitation mapped on to a topographical map of the study area, showing the locations of the 18 grids. The bottom panels show three predicted climate variables (minimum and maximum temperatures, and precipitation) for the 18 grids. Lines are least-squares regression slopes.

Extended Data Figure 9 Mid-elevation peak plots.

The left panel shows area in 500-m bands between 200 m and 3,700 m in the study area (computed using http://worldclim.org altitude data). The right panel shows the number of oscines in the censused 5-hectare grids and number of oscines in those grids discounted by possible sink species (rare species at the edge of their range).

Extended Data Table 1 Significance in the downturn in the plot of lineage diversification versus time
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Price, T., Hooper, D., Buchanan, C. et al. Niche filling slows the diversification of Himalayan songbirds. Nature 509, 222–225 (2014). https://doi.org/10.1038/nature13272

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