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      Evolution of ectomycorrhizas as a driver of diversification and biogeographic patterns in the model mycorrhizal mushroom genus Laccaria

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          Summary

          • A systematic and evolutionary ecology study of the model ectomycorrhizal (ECM) genus Laccaria was performed using herbarium material and field collections from over 30 countries covering its known geographic range.

          • A four‐gene (nr ITS, 28S, RPB2, EF1α) nucleotide sequence dataset consisting of 232 Laccaria specimens was analyzed phylogenetically. The resulting Global Laccaria dataset was used for molecular dating and estimating diversification rates in the genus. Stable isotope analysis of carbon and nitrogen was used to evaluate the origin of Laccaria's ECM ecology.

          • In all, 116 Laccaria molecular species were identified, resulting in a near 50% increase in its known diversity, including the new species described herein: Laccaria ambigua. Molecular dating indicates that the most recent common ancestor to Laccaria existed in the early Paleocene (56–66 million yr ago), probably in Australasia. At this time, Laccaria split into two lineages: one represented by the new species L. ambigua, and the other reflecting a large shift in diversification that resulted in the remainder of Laccaria. L. ambigua shows a different isotopic profile than all other Laccaria species.

          • Isotopes and diversification results suggest that the evolution of the ECM ecology was a key innovation in the evolution of Laccaria. Diversification shifts associated with Laccaria's dispersal to the northern hemisphere are attributed to adaptations to new ecological niches.

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          Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales).

          P. Matheny (2005)
          Approximately 3000 bp across 84 taxa have been analyzed for variable regions of RPB1, RPB2, and nLSU-rDNA to infer phylogenetic relationships in the large ectomycorrhizal mushroom genus Inocybe (Agaricales; Basidiomycota). This study represents the first effort to combine variable regions of RPB1 and RPB2 with nLSU-rDNA for low-level phylogenetic studies in mushroom-forming fungi. Combination of the three loci increases non-parametric bootstrap support, Bayesian posterior probabilities, and resolution for numerous clades compared to separate gene analyses. These data suggest the evolution of at least five major lineages in Inocybe-the Inocybe clade, the Mallocybe clade, the Auritella clade, the Inosperma clade, and the Pseudosperma clade. Additionally, many clades nested within each major lineage are strongly supported. These results also suggest the family Crepiodataceae sensu stricto is sister to Inocybe. Recognition of Inocybe at the family level, the Inocybaceae, is recommended.
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            Model inadequacy and mistaken inferences of trait-dependent speciation.

            Species richness varies widely across the tree of life, and there is great interest in identifying ecological, geographic, and other factors that affect rates of species proliferation. Recent methods for explicitly modeling the relationships among character states, speciation rates, and extinction rates on phylogenetic trees- BiSSE, QuaSSE, GeoSSE, and related models-have been widely used to test hypotheses about character state-dependent diversification rates. Here, we document the disconcerting ease with which neutral traits are inferred to have statistically significant associations with speciation rate. We first demonstrate this unfortunate effect for a known model assumption violation: shifts in speciation rate associated with a character not included in the model. We further show that for many empirical phylogenies, characters simulated in the absence of state-dependent diversification exhibit an even higher Type I error rate, indicating that the method is susceptible to additional, unknown model inadequacies. For traits that evolve slowly, the root cause appears to be a statistical framework that does not require replicated shifts in character state and diversification. However, spurious associations between character state and speciation rate arise even for traits that lack phylogenetic signal, suggesting that phylogenetic pseudoreplication alone cannot fully explain the problem. The surprising severity of this phenomenon suggests that many trait-diversification relationships reported in the literature may not be real. More generally, we highlight the need for diagnosing and understanding the consequences of model inadequacy in phylogenetic comparative methods.
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              Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies.

              Species traits may influence rates of speciation and extinction, affecting both the patterns of diversification among lineages and the distribution of traits among species. Existing likelihood approaches for detecting differential diversification require complete phylogenies; that is, every extant species must be present in a well-resolved phylogeny. We developed 2 likelihood methods that can be used to infer the effect of a trait on speciation and extinction without complete phylogenetic information, generalizing the recent binary-state speciation and extinction method. Our approaches can be used where a phylogeny can be reasonably assumed to be a random sample of extant species or where all extant species are included but some are assigned only to terminal unresolved clades. We explored the effects of decreasing phylogenetic resolution on the ability of our approach to detect differential diversification within a Bayesian framework using simulated phylogenies. Differential diversification caused by an asymmetry in speciation rates was nearly as well detected with only 50% of extant species phylogenetically resolved as with complete phylogenetic knowledge. We demonstrate our unresolved clade method with an analysis of sexual dimorphism and diversification in shorebirds (Charadriiformes). Our methods allow for the direct estimation of the effect of a trait on speciation and extinction rates using incompletely resolved phylogenies.
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                Author and article information

                Contributors
                awilson@chicagobotanic.org , Andrew.wilson@botanicgardens.org
                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                07 November 2016
                March 2017
                : 213
                : 4 ( doiID: 10.1111/nph.2017.213.issue-4 )
                : 1862-1873
                Affiliations
                [ 1 ] Chicago Botanic GardenPlant Science and Conservation 1000 Lake Cook Road Glencoe IL 60022USA
                [ 2 ] Sam Mitchel Herbarium of FungiDenver Botanic Gardens 909 York Street Denver CO 80206USA
                [ 3 ] Department of BotanyNational Museum of Nature and Science Tsukuba Ibaraki 305‐0005Japan
                Author notes
                [*] [* ] Author for correspondence:

                Andrew W. Wilson

                Tel: +1 508 754 8531

                Emails: awilson@ 123456chicagobotanic.org ; Andrew.wilson@ 123456botanicgardens.org

                Article
                NPH14270 2016-22292
                10.1111/nph.14270
                5324586
                28164331
                dcfa1055-c11e-4b04-905a-6e886bd267fe
                © 2016 The Authors. New Phytologist © 2016 New Phytologist Trust

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 21 June 2016
                : 15 September 2016
                Page count
                Figures: 2, Tables: 1, Pages: 12, Words: 9895
                Funding
                Funded by: National Science Foundation
                Award ID: DEB‐0445216
                Funded by: Institute for Fermentation, Osaka, Japan
                Categories
                Full Paper
                Research
                Full Papers
                Custom metadata
                2.0
                nph14270
                March 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.0.7 mode:remove_FC converted:24.02.2017

                Plant science & Botany
                biogeography,diversification,ectomycorrhiza,evolutionary ecology,molecular dating,new species,stable isotopes,systematic evolution

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