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      Rapid increase in snake dietary diversity and complexity following the end-Cretaceous mass extinction

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      PLoS Biology
      Public Library of Science

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          Abstract

          The Cenozoic marked a period of dramatic ecological opportunity in Earth history due to the extinction of non-avian dinosaurs as well as to long-term physiographic changes that created new biogeographic theaters and new habitats. Snakes underwent massive ecological diversification during this period, repeatedly evolving novel dietary adaptations and prey preferences. The evolutionary tempo and mode of these trophic ecological changes remain virtually unknown, especially compared with co-radiating lineages of birds and mammals that are simultaneously predators and prey of snakes. Here, we assemble a dataset on snake diets (34,060 observations on the diets of 882 species) to investigate the history and dynamics of the multidimensional trophic niche during the global radiation of snakes. Our results show that per-lineage dietary niche breadths remained remarkably constant even as snakes diversified to occupy disparate outposts of dietary ecospace. Rapid increases in dietary diversity and complexity occurred in the early Cenozoic, and the overall rate of ecospace expansion has slowed through time, suggesting a potential response to ecological opportunity in the wake of the end-Cretaceous mass extinction. Explosive bursts of trophic innovation followed colonization of the Nearctic and Neotropical realms by a group of snakes that today comprises a majority of living snake diversity. Our results indicate that repeated transformational shifts in dietary ecology are important drivers of adaptive radiation in snakes and provide a framework for analyzing and visualizing the evolution of complex ecological phenotypes on phylogenetic trees.

          Abstract

          The Cenozoic marked a period of dramatic ecological opportunity in Earth history due to the extinction of non-avian dinosaurs and long-term physiographic changes. This phylogenetic natural history study offers new insights into the evolution of snake ecological diversity after the end-Cretaceous mass extinction, as they took advantage of these new opportunities.

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          Trends, rhythms, and aberrations in global climate 65 Ma to present.

          Since 65 million years ago (Ma), Earth's climate has undergone a significant and complex evolution, the finer details of which are now coming to light through investigations of deep-sea sediment cores. This evolution includes gradual trends of warming and cooling driven by tectonic processes on time scales of 10(5) to 10(7) years, rhythmic or periodic cycles driven by orbital processes with 10(4)- to 10(6)-year cyclicity, and rare rapid aberrant shifts and extreme climate transients with durations of 10(3) to 10(5) years. Here, recent progress in defining the evolution of global climate over the Cenozoic Era is reviewed. We focus primarily on the periodic and anomalous components of variability over the early portion of this era, as constrained by the latest generation of deep-sea isotope records. We also consider how this improved perspective has led to the recognition of previously unforeseen mechanisms for altering climate.
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            The global diversity of birds in space and time.

            Current global patterns of biodiversity result from processes that operate over both space and time and thus require an integrated macroecological and macroevolutionary perspective. Molecular time trees have advanced our understanding of the tempo and mode of diversification and have identified remarkable adaptive radiations across the tree of life. However, incomplete joint phylogenetic and geographic sampling has limited broad-scale inference. Thus, the relative prevalence of rapid radiations and the importance of their geographic settings in shaping global biodiversity patterns remain unclear. Here we present, analyse and map the first complete dated phylogeny of all 9,993 extant species of birds, a widely studied group showing many unique adaptations. We find that birds have undergone a strong increase in diversification rate from about 50 million years ago to the near present. This acceleration is due to a number of significant rate increases, both within songbirds and within other young and mostly temperate radiations including the waterfowl, gulls and woodpeckers. Importantly, species characterized with very high past diversification rates are interspersed throughout the avian tree and across geographic space. Geographically, the major differences in diversification rates are hemispheric rather than latitudinal, with bird assemblages in Asia, North America and southern South America containing a disproportionate number of species from recent rapid radiations. The contribution of rapidly radiating lineages to both temporal diversification dynamics and spatial distributions of species diversity illustrates the benefits of an inclusive geographical and taxonomical perspective. Overall, whereas constituent clades may exhibit slowdowns, the adaptive zone into which modern birds have diversified since the Cretaceous may still offer opportunities for diversification.
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              The placental mammal ancestor and the post-K-Pg radiation of placentals.

              To discover interordinal relationships of living and fossil placental mammals and the time of origin of placentals relative to the Cretaceous-Paleogene (K-Pg) boundary, we scored 4541 phenomic characters de novo for 86 fossil and living species. Combining these data with molecular sequences, we obtained a phylogenetic tree that, when calibrated with fossils, shows that crown clade Placentalia and placental orders originated after the K-Pg boundary. Many nodes discovered using molecular data are upheld, but phenomic signals overturn molecular signals to show Sundatheria (Dermoptera + Scandentia) as the sister taxon of Primates, a close link between Proboscidea (elephants) and Sirenia (sea cows), and the monophyly of echolocating Chiroptera (bats). Our tree suggests that Placentalia first split into Xenarthra and Epitheria; extinct New World species are the oldest members of Afrotheria.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: ResourcesRole: VisualizationRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                14 October 2021
                October 2021
                14 October 2021
                : 19
                : 10
                : e3001414
                Affiliations
                [001] Museum of Zoology and Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, United States of America
                Universidade de São Paulo, BRAZIL
                Author notes

                The authors have declared that no competing interests exist.

                [¤]

                Current address: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, United States of America

                Author information
                https://orcid.org/0000-0003-0729-6687
                https://orcid.org/0000-0002-7499-8251
                Article
                PBIOLOGY-D-21-01458
                10.1371/journal.pbio.3001414
                8516226
                34648487
                3f2228e0-a1de-4174-be97-8eb2e8a996dc
                © 2021 Grundler, Rabosky

                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.

                History
                : 4 June 2021
                : 16 September 2021
                Page count
                Figures: 4, Tables: 0, Pages: 20
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000008, David and Lucile Packard Foundation;
                Award Recipient :
                Funded by: National Science Foundation (US)
                Award ID: DGE 1841052
                Award Recipient :
                This research was supported by a Graduate Research Fellowship (DGE 1841052) from the National Science Foundation to M.C.G. and by a fellowship from the David and Lucile Packard Foundation to D.L.R. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Short Reports
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Reptiles
                Squamates
                Snakes
                Biology and Life Sciences
                Zoology
                Animals
                Vertebrates
                Amniotes
                Reptiles
                Squamates
                Snakes
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Biology and Life Sciences
                Nutrition
                Diet
                Medicine and Health Sciences
                Nutrition
                Diet
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
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                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Computer and Information Sciences
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                Taxonomy
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                Biology and Life Sciences
                Evolutionary Biology
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                Biology and Life Sciences
                Ecology
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                Ecology and Environmental Sciences
                Ecology
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                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
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                Biology and Life Sciences
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                Custom metadata
                All data and analysis files are available from the Zenodo data repository (doi: 10.5281/zenodo.4446064).

                Life sciences
                Life sciences

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