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      Implications of lemuriform extinctions for the Malagasy flora

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          Significance

          Madagascar is a conservation priority because of its unique and threatened biodiversity. Lemurs, by acting as seed dispersers, are essential to maintaining healthy and diverse forests on the island. However, in the past few thousand years, at least 17 lemur species, many of which were inferred seed dispersers, have gone extinct. We outline the substantial impact that these extinctions have likely had on Malagasy forests by comparing the gape sizes and diets of living and extinct lemurs to identify large-seeded Malagasy plants that appear to be without extant animal dispersers. Additionally, we identify living lemurs that are endangered yet occupy unique and essential dispersal niches. This information can inform conservation initiatives targeting the protection and restoration of these vulnerable ecosystems.

          Abstract

          Madagascar’s lemurs display a diverse array of feeding strategies with complex relationships to seed dispersal mechanisms in Malagasy plants. Although these relationships have been explored previously on a case-by-case basis, we present here the first comprehensive analysis of lemuriform feeding, to our knowledge, and its hypothesized effects on seed dispersal and the long-term survival of Malagasy plant lineages. We used a molecular phylogenetic framework to examine the mode and tempo of diet evolution, and to quantify the associated morphological space occupied by Madagascar’s lemurs, both extinct and extant. Using statistical models and morphometric analyses, we demonstrate that the extinction of large-bodied lemurs resulted in a significant reduction in functional morphological space associated with seed dispersal ability. These reductions carry potentially far-reaching consequences for Malagasy ecosystems, and we highlight large-seeded Malagasy plants that appear to be without extant animal dispersers. We also identify living lemurs that are endangered yet occupy unique and essential dispersal niches defined by our morphometric analyses.

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          Most cited references 33

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          Phylogenetic signal and linear regression on species data

           Liam Revell (2010)
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            Size-correction and principal components for interspecific comparative studies.

            Phylogenetic methods for the analysis of species data are widely used in evolutionary studies. However, preliminary data transformations and data reduction procedures (such as a size-correction and principal components analysis, PCA) are often performed without first correcting for nonindependence among the observations for species. In the present short comment and attached R and MATLAB code, I provide an overview of statistically correct procedures for phylogenetic size-correction and PCA. I also show that ignoring phylogeny in preliminary transformations can result in significantly elevated variance and type I error in our statistical estimators, even if subsequent analysis of the transformed data is performed using phylogenetic methods. This means that ignoring phylogeny during preliminary data transformations can possibly lead to spurious results in phylogenetic statistical analyses of species data.
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              Stochastic mapping of morphological characters.

              Many questions in evolutionary biology are best addressed by comparing traits in different species. Often such studies involve mapping characters on phylogenetic trees. Mapping characters on trees allows the nature, number, and timing of the transformations to be identified. The parsimony method is the only method available for mapping morphological characters on phylogenies. Although the parsimony method often makes reasonable reconstructions of the history of a character, it has a number of limitations. These limitations include the inability to consider more than a single change along a branch on a tree and the uncoupling of evolutionary time from amount of character change. We extended a method described by Nielsen (2002, Syst. Biol. 51:729-739) to the mapping of morphological characters under continuous-time Markov models and demonstrate here the utility of the method for mapping characters on trees and for identifying character correlation.
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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
                3 May 2016
                11 April 2016
                : 113
                : 18
                : 5041-5046
                Affiliations
                aDepartment of Ecology and Evolutionary Biology, Yale University , New Haven, CT 06520;
                b North Carolina Museum of Natural Sciences , Raleigh, NC 27601;
                cInstitute of Systematic Botany, New York Botanical Garden , Bronx, NY 10458;
                dDepartment of Anthropology, Pennsylvania State University , University Park, PA 16802;
                eDepartment of Biology, Pennsylvania State University , University Park, PA 16802;
                fDepartment of Biology, Duke University , Durham, NC 27708;
                gDepartment of Anthropology, Yale University , New Haven, CT 06520;
                hDepartment of Anthropology, Hunter College , New York, NY 10065;
                iDepartment of Anthropology, The Graduate Center, City University of New York , New York, NY 10065;
                j The New York Consortium in Evolutionary Primatology , New York, NY 10065
                Author notes
                1To whom correspondence should be addressed. Email: sarah.federman@ 123456yale.edu .

                Edited by Rodolfo Dirzo, Stanford University, Stanford, CA, and approved March 10, 2016 (received for review December 4, 2015)

                Author contributions: S.F. and A.L.B. designed research; S.F., A. Dornburg, D.C.D., A. Downie, G.H.P., and A.L.B. performed research; S.F. and A. Dornburg analyzed data; and S.F., A. Dornburg, D.C.D., A. Downie, G.H.P., A.D.Y., E.J.S., A.F.R., M.J.D., and A.L.B. wrote the paper.

                Article
                PMC4983841 PMC4983841 4983841 201523825
                10.1073/pnas.1523825113
                4983841
                27071108
                11f6ba4a-0b3c-4d5b-a630-b1e5bcfcda5b
                Page count
                Pages: 6
                Funding
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: DGE-1122492
                Categories
                Biological Sciences
                Evolution

                anachronism, extinction, lemurs, Madagascar, seed dispersal

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