Discord between morphological and phylogenetic species boundaries: incomplete lineage sorting and recombination results in fuzzy species boundaries in an asexual fungal pathogen

Persistent Link:
http://hdl.handle.net/10150/610386
Title:
Discord between morphological and phylogenetic species boundaries: incomplete lineage sorting and recombination results in fuzzy species boundaries in an asexual fungal pathogen
Author:
Stewart, Jane; Timmer, Lavern; Lawrence, Christopher; Pryor, Barry; Peever, Tobin
Affiliation:
Department of Plant Pathology, Washington State University, Pullman, WA, USA; Citrus Research and Education Center, University of Florida, Lake Alfred, FL, USA; Virginia Bioinformatics Institute, Blacksburg, VA, USA; Division of Plant Pathology and Microbiology, School of Plant Sciences, University of Arizona, Tucson, AZ, USA; Current address: Department of Plant Pathology, University of Georgia, Athens, Georgia
Issue Date:
2014
Publisher:
BioMed Central
Citation:
Stewart et al. BMC Evolutionary Biology 2014, 14:38 http://www.biomedcentral.com/1471-2148/14/38
Journal:
BMC Evolutionary Biology
Rights:
© 2014 Stewart et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0)
Collection Information:
This item is part of the UA Faculty Publications collection. For more information this item or other items in the UA Campus Repository, contact the University of Arizona Libraries at repository@u.library.arizona.edu.
Abstract:
BACKGROUND:Traditional morphological and biological species concepts are difficult to apply to closely related, asexual taxa because of the lack of an active sexual phase and paucity of morphological characters. Phylogenetic species concepts such as genealogical concordance phylogenetic species recognition (GCPSR) have been extensively used; however, methods that incorporate gene tree uncertainty into species recognition may more accurately and objectively delineate species. Using a worldwide sample of Alternaria alternata sensu lato, causal agent of citrus brown spot, the evolutionary histories of four nuclear loci including an endo-polygalacturonase gene, two anonymous loci, and one microsatellite flanking region were estimated using the coalescent. Species boundaries were estimated using several approaches including those that incorporate uncertainty in gene genealogies when lineage sorting and non-reciprocal monophyly of gene trees is common.RESULTS:Coalescent analyses revealed three phylogenetic lineages strongly influenced by incomplete lineage sorting and recombination. Divergence of the citrus 2 lineage from the citrus 1 and citrus 3 lineages was supported at most loci. A consensus of species tree estimation methods supported two species of Alternaria causing citrus brown spot worldwide. Based on substitution rates at the endo-polygalacturonase locus, divergence of the citrus 2 and the 1 and 3 lineages was estimated to have occurred at least 5, 400 years before present, predating the human-mediated movement of citrus and associated pathogens out of SE Asia.CONCLUSIONS:The number of Alternaria species identified as causing brown spot of citrus worldwide using morphological criteria has been overestimated. Little support was found for most of these morphospecies using quantitative species recognition approaches. Correct species delimitation of plant-pathogenic fungi is critical for understanding the evolution of pathogenicity, introductions of pathogens to new areas, and for regulating the movement of pathogens to enforce quarantines. This research shows that multilocus phylogenetic methods that allow for recombination and incomplete lineage sorting can be useful for the quantitative delimitation of asexual species that are morphologically indistinguishable. Two phylogenetic species of Alternaria were identified as causing citrus brown spot worldwide. Further research is needed to determine how these species were introduced worldwide, how they differ phenotypically and how these species are maintained.
EISSN:
1471-2148
DOI:
10.1186/1471-2148-14-38
Keywords:
Coalescent; Species delimitation; Species tree; Gene tree
Version:
Final published version
Additional Links:
http://www.biomedcentral.com/1471-2148/14/38

Full metadata record

DC FieldValue Language
dc.contributor.authorStewart, Janeen
dc.contributor.authorTimmer, Lavernen
dc.contributor.authorLawrence, Christopheren
dc.contributor.authorPryor, Barryen
dc.contributor.authorPeever, Tobinen
dc.date.accessioned2016-05-20T09:05:39Z-
dc.date.available2016-05-20T09:05:39Z-
dc.date.issued2014en
dc.identifier.citationStewart et al. BMC Evolutionary Biology 2014, 14:38 http://www.biomedcentral.com/1471-2148/14/38en
dc.identifier.doi10.1186/1471-2148-14-38en
dc.identifier.urihttp://hdl.handle.net/10150/610386-
dc.description.abstractBACKGROUND:Traditional morphological and biological species concepts are difficult to apply to closely related, asexual taxa because of the lack of an active sexual phase and paucity of morphological characters. Phylogenetic species concepts such as genealogical concordance phylogenetic species recognition (GCPSR) have been extensively useden
dc.description.abstracthowever, methods that incorporate gene tree uncertainty into species recognition may more accurately and objectively delineate species. Using a worldwide sample of Alternaria alternata sensu lato, causal agent of citrus brown spot, the evolutionary histories of four nuclear loci including an endo-polygalacturonase gene, two anonymous loci, and one microsatellite flanking region were estimated using the coalescent. Species boundaries were estimated using several approaches including those that incorporate uncertainty in gene genealogies when lineage sorting and non-reciprocal monophyly of gene trees is common.RESULTS:Coalescent analyses revealed three phylogenetic lineages strongly influenced by incomplete lineage sorting and recombination. Divergence of the citrus 2 lineage from the citrus 1 and citrus 3 lineages was supported at most loci. A consensus of species tree estimation methods supported two species of Alternaria causing citrus brown spot worldwide. Based on substitution rates at the endo-polygalacturonase locus, divergence of the citrus 2 and the 1 and 3 lineages was estimated to have occurred at least 5, 400 years before present, predating the human-mediated movement of citrus and associated pathogens out of SE Asia.CONCLUSIONS:The number of Alternaria species identified as causing brown spot of citrus worldwide using morphological criteria has been overestimated. Little support was found for most of these morphospecies using quantitative species recognition approaches. Correct species delimitation of plant-pathogenic fungi is critical for understanding the evolution of pathogenicity, introductions of pathogens to new areas, and for regulating the movement of pathogens to enforce quarantines. This research shows that multilocus phylogenetic methods that allow for recombination and incomplete lineage sorting can be useful for the quantitative delimitation of asexual species that are morphologically indistinguishable. Two phylogenetic species of Alternaria were identified as causing citrus brown spot worldwide. Further research is needed to determine how these species were introduced worldwide, how they differ phenotypically and how these species are maintained.en
dc.language.isoenen
dc.publisherBioMed Centralen
dc.relation.urlhttp://www.biomedcentral.com/1471-2148/14/38en
dc.rights© 2014 Stewart et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0)en
dc.subjectCoalescenten
dc.subjectSpecies delimitationen
dc.subjectSpecies treeen
dc.subjectGene treeen
dc.titleDiscord between morphological and phylogenetic species boundaries: incomplete lineage sorting and recombination results in fuzzy species boundaries in an asexual fungal pathogenen
dc.typeArticleen
dc.identifier.eissn1471-2148en
dc.contributor.departmentDepartment of Plant Pathology, Washington State University, Pullman, WA, USAen
dc.contributor.departmentCitrus Research and Education Center, University of Florida, Lake Alfred, FL, USAen
dc.contributor.departmentVirginia Bioinformatics Institute, Blacksburg, VA, USAen
dc.contributor.departmentDivision of Plant Pathology and Microbiology, School of Plant Sciences, University of Arizona, Tucson, AZ, USAen
dc.contributor.departmentCurrent address: Department of Plant Pathology, University of Georgia, Athens, Georgiaen
dc.identifier.journalBMC Evolutionary Biologyen
dc.description.collectioninformationThis item is part of the UA Faculty Publications collection. For more information this item or other items in the UA Campus Repository, contact the University of Arizona Libraries at repository@u.library.arizona.edu.en
dc.eprint.versionFinal published versionen
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