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      Mega-evolutionary dynamics of the adaptive radiation of birds

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          Abstract

          The origin and expansion of biological diversity is regulated by both developmental trajectories 1, 2 and limits on available ecological niches 37. As lineages diversify an early, often rapid, phase of species and trait proliferation gives way to evolutionary slowdowns as new species pack into ever more densely occupied regions of ecological niche space 6, 8. Small clades such as Darwin’s finches demonstrate that natural selection is the driving force of adaptive radiations, but how microevolutionary processes scale up to shape the expansion of phenotypic diversity over much longer evolutionary timescales is unclear 9. Here we address this problem on a global scale by analysing a novel crowd-sourced dataset of 3D-scanned bill morphology from >2000 species. We find that bill diversity expanded early in extant avian evolutionary history before transitioning to a phase dominated by morphospace packing. However, this early phenotypic diversification is decoupled from temporal variation in evolutionary rate: rates of bill evolution vary among lineages but are comparatively stable through time. We find that rare but major discontinuities in phenotype emerge from rapid increases in rate along single branches, sometimes leading to depauperate clades with unusual bill morphologies. Despite these jumps between groups, the major axes of within-group bill shape evolution are remarkably consistent across birds. We reveal that macroevolutionary processes underlying global-scale adaptive radiations support Darwinian 9 and Simpsonian 4 ideas of microevolution within adaptive zones and accelerated evolution between distinct adaptive peaks.

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          Most cited references 36

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          Tree of Life Reveals Clock-Like Speciation and Diversification

          Genomic data are rapidly resolving the tree of living species calibrated to time, the timetree of life, which will provide a framework for research in diverse fields of science. Previous analyses of taxonomically restricted timetrees have found a decline in the rate of diversification in many groups of organisms, often attributed to ecological interactions among species. Here, we have synthesized a global timetree of life from 2,274 studies representing 50,632 species and examined the pattern and rate of diversification as well as the timing of speciation. We found that species diversity has been mostly expanding overall and in many smaller groups of species, and that the rate of diversification in eukaryotes has been mostly constant. We also identified, and avoided, potential biases that may have influenced previous analyses of diversification including low levels of taxon sampling, small clade size, and the inclusion of stem branches in clade analyses. We found consistency in time-to-speciation among plants and animals, ∼2 My, as measured by intervals of crown and stem species times. Together, this clock-like change at different levels suggests that speciation and diversification are processes dominated by random events and that adaptive change is largely a separate process.
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            Functional traits and niche-based tree community assembly in an Amazonian forest.

            It is debated whether species-level differences in ecological strategy, which play a key role in much of coexistence theory, are important in structuring highly diverse communities. We examined the co-occurrence patterns of over 1100 tree species in a 25-hectare Amazonian forest plot in relation to field-measured functional traits. Using a null model approach, we show that co-occurring trees are often less ecologically similar than a niche-free (neutral) model predicts. Furthermore, we find evidence for processes that simultaneously drive convergence and divergence in key aspects of plant strategy, suggesting that at least two distinct niche-based processes are occurring. Our results show that strategy differentiation among species contributes to the maintenance of diversity in one of the most diverse tropical forests in the world.
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              Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates.

              The uneven distribution of species richness is a fundamental and unexplained pattern of vertebrate biodiversity. Although species richness in groups like mammals, birds, or teleost fishes is often attributed to accelerated cladogenesis, we lack a quantitative conceptual framework for identifying and comparing the exceptional changes of tempo in vertebrate evolutionary history. We develop MEDUSA, a stepwise approach based upon the Akaike information criterion for detecting multiple shifts in birth and death rates on an incompletely resolved phylogeny. We apply MEDUSA incompletely to a diversity tree summarizing both evolutionary relationships and species richness of 44 major clades of jawed vertebrates. We identify 9 major changes in the tempo of gnathostome diversification; the most significant of these lies at the base of a clade that includes most of the coral-reef associated fishes as well as cichlids and perches. Rate increases also underlie several well recognized tetrapod radiations, including most modern birds, lizards and snakes, ostariophysan fishes, and most eutherian mammals. In addition, we find that large sections of the vertebrate tree exhibit nearly equal rates of origination and extinction, providing some of the first evidence from molecular data for the importance of faunal turnover in shaping biodiversity. Together, these results reveal living vertebrate biodiversity to be the product of volatile turnover punctuated by 6 accelerations responsible for >85% of all species as well as 3 slowdowns that have produced "living fossils." In addition, by revealing the timing of the exceptional pulses of vertebrate diversification as well as the clades that experience them, our diversity tree provides a framework for evaluating particular causal hypotheses of vertebrate radiations.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                20 January 2017
                01 February 2017
                16 February 2017
                01 August 2017
                : 542
                : 7641
                : 344-347
                Affiliations
                [1 ]Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK
                [2 ]School of Geosciences, University of South Florida, Tampa, FL 33620, USA
                [3 ]Center for Virtualization and Applied Spatial Technologies, University of South Florida, Tampa, FL 33620, USA
                [4 ]Bird Group, Department of Life Sciences, The Natural History Museum, Tring, Hertfordshire, UK
                Author notes
                [* ]author for correspondence: gavin.thomas@ 123456sheffield.ac.uk
                Article
                EMS70920
                10.1038/nature21074
                5321581
                28146475

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