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      Density-Dependent Cladogenesis in Birds

      research-article

      1 , * , 2

      PLoS Biology

      Public Library of Science

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          Abstract

          A characteristic signature of adaptive radiation is a slowing of the rate of speciation toward the present. On the basis of molecular phylogenies, studies of single clades have frequently found evidence for a slowdown in diversification rate and have interpreted this as evidence for density dependent speciation. However, we demonstrated via simulation that large clades are expected to show stronger slowdowns than small clades, even if the probability of speciation and extinction remains constant through time. This is a consequence of exponential growth: clades, which, by chance, diversify at above the average rate early in their history, will tend to be large. They will also tend to regress back to the average diversification rate later on, and therefore show a slowdown. We conducted a meta-analysis of the distribution of speciation events through time, focusing on sequence-based phylogenies for 45 clades of birds. Thirteen of the 23 clades (57%) that include more than 20 species show significant slowdowns. The high frequency of slowdowns observed in large clades is even more extreme than expected under a purely stochastic constant-rate model, but is consistent with the adaptive radiation model. Taken together, our data strongly support a model of density-dependent speciation in birds, whereby speciation slows as ecological opportunities and geographical space place limits on clade growth.

          Author Summary

          It is probable that the number of species that a given region can support is limited; however, it is unclear whether the limit is approached sufficiently in nature such that the rate at which new species form slows down. Using the pattern of phylogenetic branching, a technique that estimates evolutionary relationships based on molecular data, we demonstrate that in large clades of birds, there is a decrease in the per-lineage probability of speciation as the number of species in the clade increase. We also show that this pattern can arise even if speciation and extinction occur randomly through time. This is because large clades are likely, by chance, to have rapidly speciated early in their history, and will relax back to the average speciation rate later on. We account for this effect, and we still find evidence that, as a clade grows to large size, the per-lineage probability of speciation declines. These results strongly suggest that speciation rates are slowed as environments fill up with competitors.

          Abstract

          Molecular evidence provides strong evidence that speciation rates slow down through time.

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          Most cited references54

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          Ecology and the origin of species.

          The ecological hypothesis of speciation is that reproductive isolation evolves ultimately as a consequence of divergent natural selection on traits between environments. Ecological speciation is general and might occur in allopatry or sympatry, involve many agents of natural selection, and result from a combination of adaptive processes. The main difficulty of the ecological hypothesis has been the scarcity of examples from nature, but several potential cases have recently emerged. I review the mechanisms that give rise to new species by divergent selection, compare ecological speciation with its alternatives, summarize recent tests in nature, and highlight areas requiring research.
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            The ecology of adaptive radiation

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              Testing macro-evolutionary models using incomplete molecular phylogenies.

              Phylogenies reconstructed from gene sequences can be used to investigate the tempo and mode of species diversification. Here we develop and use new statistical methods to infer past patterns of speciation and extinction from molecular phylogenies. Specifically, we test the null hypothesis that per-lineage speciation and extinction rates have remained constant through time. Rejection of this hypothesis may provide evidence for evolutionary events such as adaptive radiations or key adaptations. In contrast to previous approaches, our methods are robust to incomplete taxon sampling and are conservative with respect to extinction. Using simulation we investigate, first, the adverse effects of failing to take incomplete sampling into account and, second, the power and reliability of our tests. When applied to published phylogenies our tests suggest that, in some cases, speciation rates have decreased through time.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                pbio
                plbi
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                March 2008
                25 March 2008
                : 6
                : 3
                Affiliations
                [1 ] Natural Environment Research Council Centre for Population Biology and Division of Biology, Imperial College London, Ascot, Berkshire, United Kingdom
                [2 ] Department of Ecology and Evolution, University of Chicago, Chicago, Illinois, United States of America
                University of Edinburgh, United Kingdom
                Author notes
                * To whom correspondence should be addressed. E-mail: albert.phillimore@ 123456imperial.ac.uk
                Article
                07-PLBI-RA-3332R3 plbi-06-03-19
                10.1371/journal.pbio.0060071
                2270327
                18366256
                8e9ff975-dac3-45a1-a382-fe729a3d1ae4
                Copyright: © 2008 Phillimore and Price. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 7
                Categories
                Research Article
                Ecology
                Evolutionary Biology
                Custom metadata
                Phillimore AB, Price TD (2008) Density-dependent cladogenesis in birds. PLoS Biol 6(3): e71. doi: 10.1371/journal.pbio.0060071

                Life sciences

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