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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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.
The authors declare no competing financial interests.
Extended data figures and tables
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.
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.
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.
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).
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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) doi:10.1038/nature13272
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