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      Mycophagous rove beetles highlight diverse mushrooms in the Cretaceous

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          Abstract

          Agaricomycetes, or mushrooms, are familiar, conspicuous and morphologically diverse Fungi. Most Agaricomycete fruiting bodies are ephemeral, and their fossil record is limited. Here we report diverse gilled mushrooms (Agaricales) and mycophagous rove beetles (Staphylinidae) from mid-Cretaceous Burmese amber, the latter belonging to Oxyporinae, modern members of which exhibit an obligate association with soft-textured mushrooms. The discovery of four mushroom forms, most with a complete intact cap containing distinct gills and a stalk, suggests evolutionary stasis of body form for ∼99 Myr and highlights the palaeodiversity of Agaricomycetes. The mouthparts of early oxyporines, including enlarged mandibles and greatly enlarged apical labial palpomeres with dense specialized sensory organs, match those of modern taxa and suggest that they had a mushroom feeding biology. Diverse and morphologically specialized oxyporines from the Early Cretaceous suggests the existence of diverse Agaricomycetes and a specialized trophic interaction and ecological community structure by this early date.

          Abstract

          Agarics (gilled mushrooms) are rarely preserved as fossils, which has obscured their evolutionary history. Here, the authors describe new forms of agarics as well as new species of rove beetles with morphological specializations for mushroom feeding discovered in 99-million-year-old Burmese amber.

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          Most cited references 38

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          The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils?

          The use of nucleotide and amino acid sequences allows improved understanding of the timing of evolutionary events of life on earth. Molecular estimates of divergence times are, however, controversial and are generally much more ancient than suggested by the fossil record. The limited number of genes and species explored and pervasive variations in evolutionary rates are the most likely sources of such discrepancies. Here we compared concatenated amino acid sequences of 129 proteins from 36 eukaryotes to determine the divergence times of several major clades, including animals, fungi, plants, and various protists. Due to significant variations in their evolutionary rates, and to handle the uncertainty of the fossil record, we used a Bayesian relaxed molecular clock simultaneously calibrated by six paleontological constraints. We show that, according to 95% credibility intervals, the eukaryotic kingdoms diversified 950-1,259 million years ago (Mya), animals diverged from choanoflagellates 761-957 Mya, and the debated age of the split between protostomes and deuterostomes occurred 642-761 Mya. The divergence times appeared to be robust with respect to prior assumptions and paleontological calibrations. Interestingly, these relaxed clock time estimates are much more recent than those obtained under the assumption of a global molecular clock, yet bilaterian diversification appears to be approximately 100 million years more ancient than the Cambrian boundary.
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            Dating divergences in the Fungal Tree of Life: review and new analyses.

            The collection of papers in this issue of Mycologia documents considerable improvements in taxon sampling and phylogenetic resolution regarding the Fungal Tree of Life. The new data will stimulate new attempts to date divergences and correlate events in fungal evolution with those of other organisms. Here, we review the history of dating fungal divergences by nucleic acid variation and then use a dataset of 50 genes for 25 selected fungi, plants and animals to investigate divergence times in kingdom Fungi. In particular, we test the choice of fossil calibration points on dating divergences in fungi. At the scale of our analysis, substitution rates varied without showing significant within-lineage correlation, so we used the Langley-Fitch method in the R8S package of computer programs to estimate node ages. Different calibration points had a dramatic effect on estimated divergence dates. The estimate for the age of the Ascomycota/Basidiomycota split was 1808000000 y ago when calibrated assuming that mammals and birds diverged 300000000 y ago, 1489000000 y ago when calibrated assuming that the 400000000 y old fungal fossil Paleopyrenomycites devonicus represents Sordariomycetes and approximately 400000000 y ago when calibrated assuming 206000000 y ago for the plant eudicot/monocot divergence. An advantage of a date of approximately 400000000 y ago for the Ascomycota/Basidiomycota divergence is that the radiation of fungi associated with land plants would not greatly precede the earliest land plant fossils. Acceptance of approximately 400000000 y ago for the Ascomycota/Basidiomycota split would require that P. devonicus be considered a deeply branching Ascomycota. To improve on current estimates of divergence times, mycologists will require calibration points from within groups of fungi that share similar substitution rates. The most useful calibration is likely to depend on the discovery and description of continuous records of fossil fungi, or their spores, that show recognizable shifts in morphology.
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              Fungi evolved right on track.

              Dating of fungal divergences with molecular clocks thus far has yielded highly inconsistent results. The origin of fungi was estimated at between 660 million and up to 2.15 billion y ago, and the divergence of the two major lineages of higher fungi, Ascomycota and Basidiomycota, at between 390 million y and up to 1.5 billion y ago. Assuming that these inconsistencies stem from various causes, we reassessed the systematic placement of the most important fungal fossil, Paleopyrenomycites, and recalibrated internally unconstrained, published molecular clock trees by applying uniform calibration points. As a result the origin of fungi was re-estimated at between 760 million and 1.06 billion y ago and the origin of the Ascomycota at 500-650 million y ago. These dates are much more consistent than previous estimates, even if based on the same phylogenies and molecular clock trees, and they are also much better in line with the fossil record of fungi and plants and the ecological interdependence between filamentous fungi and land plants. Our results do not provide evidence to suggest the existence of ancient protolichens as an alternative to explain the ecology of early terrestrial fungi in the absence of land plants.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                16 March 2017
                2017
                : 8
                Affiliations
                [1 ]Key Laboratory of Economic Stratigraphy and Palaeogeography, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences , Nanjing 210008, China
                [2 ]State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences , Nanjing 210008, China
                [3 ]Landcare Research, New Zealand Arthropod Collection , Private Bag 92170, Auckland, New Zealand
                [4 ]Department of Biology , Clark University , Worcester, Massachusetts 01610, USA
                [5 ]Lingpoge Amber Museum , Shanghai 201108, China
                Author notes
                Article
                ncomms14894
                10.1038/ncomms14894
                5357310
                28300055
                Copyright © 2017, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

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