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      Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot

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          Significance

          Why do so many species occur in mountains? A popular but little-tested hypothesis is that tectonic uplift creates environmental conditions (new habitats, dispersal barriers, etc.) that increase the rate at which resident species divide and evolve to form new ones. In China’s Hengduan Mountains region, a biodiversity hotspot uplifted over the last 8 million years, this rate does in fact show a significant increase during that time, relative to the rate for adjacent older mountains, and to the rate of species immigration. The Hengduan Mountains flora is thus made up disproportionately of species that evolved within the region during its uplift, supporting the original hypothesis and helping to explain the prevalence of mountains as global biodiversity hotspots.

          Abstract

          A common hypothesis for the rich biodiversity found in mountains is uplift-driven diversification—that orogeny creates conditions favoring rapid in situ speciation of resident lineages. We tested this hypothesis in the context of the Qinghai–Tibetan Plateau (QTP) and adjoining mountain ranges, using the phylogenetic and geographic histories of multiple groups of plants to infer the tempo (rate) and mode (colonization versus in situ diversification) of biotic assembly through time and across regions. We focused on the Hengduan Mountains region, which in comparison with the QTP and Himalayas was uplifted more recently (since the late Miocene) and is smaller in area and richer in species. Time-calibrated phylogenetic analyses show that about 8 million y ago the rate of in situ diversification increased in the Hengduan Mountains, significantly exceeding that in the geologically older QTP and Himalayas. By contrast, in the QTP and Himalayas during the same period the rate of in situ diversification remained relatively flat, with colonization dominating lineage accumulation. The Hengduan Mountains flora was thus assembled disproportionately by recent in situ diversification, temporally congruent with independent estimates of orogeny. This study shows quantitative evidence for uplift-driven diversification in this region, and more generally, tests the hypothesis by comparing the rate and mode of biotic assembly jointly across time and space. It thus complements the more prevalent method of examining endemic radiations individually and could be used as a template to augment such studies in other biodiversity hotspots.

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          Most cited references51

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          Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire.

          The relative importance of local ecological and larger-scale historical processes in causing differences in species richness across the globe remains keenly debated. To gain insight into these questions, we investigated the assembly of plant diversity in the Cerrado in South America, the world's most species-rich tropical savanna. Time-calibrated phylogenies suggest that Cerrado lineages started to diversify less than 10 Mya, with most lineages diversifying at 4 Mya or less, coinciding with the rise to dominance of flammable C4 grasses and expansion of the savanna biome worldwide. These plant phylogenies show that Cerrado lineages are strongly associated with adaptations to fire and have sister groups in largely fire-free nearby wet forest, seasonally dry forest, subtropical grassland, or wetland vegetation. These findings imply that the Cerrado formed in situ via recent and frequent adaptive shifts to resist fire, rather than via dispersal of lineages already adapted to fire. The location of the Cerrado surrounded by a diverse array of species-rich biomes, and the apparently modest adaptive barrier posed by fire, are likely to have contributed to its striking species richness. These findings add to growing evidence that the origins and historical assembly of species-rich biomes have been idiosyncratic, driven in large part by unique features of regional- and continental-scale geohistory and that different historical processes can lead to similar levels of modern species richness.
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            A likelihood framework for inferring the evolution of geographic range on phylogenetic trees.

            At a time when historical biogeography appears to be again expanding its scope after a period of focusing primarily on discerning area relationships using cladograms, new inference methods are needed to bring more kinds of data to bear on questions about the geographic history of lineages. Here we describe a likelihood framework for inferring the evolution of geographic range on phylogenies that models lineage dispersal and local extinction in a set of discrete areas as stochastic events in continuous time. Unlike existing methods for estimating ancestral areas, such as dispersal-vicariance analysis, this approach incorporates information on the timing of both lineage divergences and the availability of connections between areas (dispersal routes). Monte Carlo methods are used to estimate branch-specific transition probabilities for geographic ranges, enabling the likelihood of the data (observed species distributions) to be evaluated for a given phylogeny and parameterized paleogeographic model. We demonstrate how the method can be used to address two biogeographic questions: What were the ancestral geographic ranges on a phylogenetic tree? How were those ancestral ranges affected by speciation and inherited by the daughter lineages at cladogenesis events? For illustration we use hypothetical examples and an analysis of a Northern Hemisphere plant clade (Cercis), comparing and contrasting inferences to those obtained from dispersal-vicariance analysis. Although the particular model we implement is somewhat simplistic, the framework itself is flexible and could readily be modified to incorporate additional sources of information and also be extended to address other aspects of historical biogeography.
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              Palaeo-altimetry of the late Eocene to Miocene Lunpola basin, central Tibet.

              The elevation history of the Tibetan plateau provides direct insight into the tectonic processes associated with continent-continent collisions. Here we present oxygen-isotope-based estimates of the palaeo-altimetry of late Eocene and younger deposits of the Lunpola basin in the centre of the plateau, which indicate that the surface of Tibet has been at an elevation of more than 4 kilometres for at least the past 35 million years. We conclude that crustal, but not mantle, thickening models, combined with plate-kinematic solutions of India-Asia convergence, are compatible with palaeo-elevation estimates across the Tibetan plateau.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                25 April 2017
                3 April 2017
                3 April 2017
                : 114
                : 17
                : E3444-E3451
                Affiliations
                [1] aLife Sciences Section, Integrative Research Center, The Field Museum , Chicago, IL 60605;
                [2] bKey Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences , Yunnan 666303, China;
                [3] c National Institute of Ecology , 1210 Geumgang-ro, Maseo-myeon, Seocheon-gun, Chungcheongnam-do, South Korea
                Author notes
                2To whom correspondence should be addressed. Email: rree@ 123456fieldmuseum.org .

                Edited by Scott V. Edwards, Harvard University, Cambridge, MA, and approved February 27, 2017 (received for review September 26, 2016)

                Author contributions: Y.X. and R.H.R. designed research, performed research, analyzed data, and wrote the paper.

                1Y.X. and R.H.R. contributed equally to this work.

                Article
                PMC5410793 PMC5410793 5410793 201616063
                10.1073/pnas.1616063114
                5410793
                28373546
                c78b3962-df2a-446b-a95b-bc6863f0f337

                Freely available online through the PNAS open access option.

                History
                Page count
                Pages: 8
                Funding
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: DEB-1119098
                Funded by: Swiss National Science Foundation (Schweizerische Nationalfonds) 501100001711
                Award ID: P300P3_158528
                Categories
                PNAS Plus
                Biological Sciences
                Evolution
                From the Cover
                PNAS Plus

                speciation,dispersal,molecular clocks,vascular plants,biogeography

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