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      Species boundaries in plant pathogenic fungi: a Colletotrichum case study

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          Abstract

          Background

          Accurate delimitation of plant pathogenic fungi is critical for the establishment of quarantine regulations, screening for genetic resistance to plant pathogens, and the study of ecosystem function. Concatenation analysis of multi-locus DNA sequence data represents a powerful and commonly used approach to recognizing evolutionary independent lineages in fungi. It is however possible to mask the discordance between individual gene trees, thus the speciation events might be erroneously estimated if one simply recognizes well supported clades as distinct species without implementing a careful examination of species boundary. To investigate this phenomenon, we studied Colletotrichum siamense s. lat., which is a cosmopolitan pathogen causing serious diseases on many economically important plant hosts. Presently there are significant disagreements among mycologists as to what constitutes a species in C. siamense s. lat., with the number of accepted species ranging from one to seven.

          Results

          In this study, multiple approaches were used to test the null hypothesis “ C. siamense is a species complex”, using a global strain collection. Results of molecular analyses based on the Genealogical Concordance Phylogenetic Species Recognition (GCPSR) and coalescent methods (e.g. Generalized Mixed Yule-coalescent and Poisson Tree Processes) do not support the recognition of any independent evolutionary lineages within C. siamense s. lat. as distinct species, thus rejecting the null hypothesis. This conclusion is reinforced by the recognition of genetic recombination, cross fertility, and the comparison of ecological and morphological characters. Our results indicate that reproductive isolation, geographic and host plant barriers to gene flow are absent in C. siamense s. lat.

          Conclusions

          This discovery emphasized the importance of a polyphasic approach when describing novel species in morphologically conserved genera of plant pathogenic fungi.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12862-016-0649-5) contains supplementary material, which is available to authorized users.

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          Most cited references79

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          Cryptic species as a window on diversity and conservation.

          The taxonomic challenge posed by cryptic species (two or more distinct species classified as a single species) has been recognized for nearly 300 years, but the advent of relatively inexpensive and rapid DNA sequencing has given biologists a new tool for detecting and differentiating morphologically similar species. Here, we synthesize the literature on cryptic and sibling species and discuss trends in their discovery. However, a lack of systematic studies leaves many questions open, such as whether cryptic species are more common in particular habitats, latitudes or taxonomic groups. The discovery of cryptic species is likely to be non-random with regard to taxon and biome and, hence, could have profound implications for evolutionary theory, biogeography and conservation planning.
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            Phylogenetic species recognition and species concepts in fungi.

            The operational species concept, i.e., the one used to recognize species, is contrasted to the theoretical species concept. A phylogenetic approach to recognize fungal species based on concordance of multiple gene genealogies is compared to those based on morphology and reproductive behavior. Examples where Phylogenetic Species Recognition has been applied to fungi are reviewed and concerns regarding Phylogenetic Species Recognition are discussed.
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              Bayesian species delimitation using multilocus sequence data.

              In the absence of recent admixture between species, bipartitions of individuals in gene trees that are shared across loci can potentially be used to infer the presence of two or more species. This approach to species delimitation via molecular sequence data has been constrained by the fact that genealogies for individual loci are often poorly resolved and that ancestral lineage sorting, hybridization, and other population genetic processes can lead to discordant gene trees. Here we use a Bayesian modeling approach to generate the posterior probabilities of species assignments taking account of uncertainties due to unknown gene trees and the ancestral coalescent process. For tractability, we rely on a user-specified guide tree to avoid integrating over all possible species delimitations. The statistical performance of the method is examined using simulations, and the method is illustrated by analyzing sequence data from rotifers, fence lizards, and human populations.
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                Author and article information

                Contributors
                liufang@im.ac.cn
                WangMei910527@163.com
                ulrike.damm@senckenberg.de
                p.crous@cbs.knaw.nl
                +86-10-64806139 , cail@im.ac.cn
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                14 April 2016
                14 April 2016
                2016
                : 16
                : 81
                Affiliations
                [ ]State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101 China
                [ ]Microbiology, Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands
                [ ]Senckenberg Museum of Natural History Görlitz, PF 300 154, 02806 Görlitz, Germany
                [ ]CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands
                [ ]Department of Microbiology and Plant Pathology, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria, 0002 South Africa
                Article
                649
                10.1186/s12862-016-0649-5
                4832473
                27080690
                5e44b858-0e4b-4c7d-baab-5927b2a04d4c
                © Liu et al. 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 14 December 2015
                : 31 March 2016
                Funding
                Funded by: External Cooperation Program of the Chinese Academy of Sciences
                Award ID: GJHZ1310
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: NSFC 31400017
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2016

                Evolutionary Biology
                coalescent,gcpsr,mating test,phylogeny,species delimitation
                Evolutionary Biology
                coalescent, gcpsr, mating test, phylogeny, species delimitation

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