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      From mammals back to birds: Host-switch of the acanthocephalan Corynosoma australe from pinnipeds to the Magellanic penguin Spheniscus magellanicus

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          Abstract

          Trophically-transmitted parasites are regularly exposed to potential new hosts through food web interactions. Successful colonization, or switching, to novel hosts, occur readily when ‘donor’ and ‘target’ hosts are phylogenetically related, whereas switching between distantly related hosts is rare and may result from stochastic factors (i.e. rare favourable mutations). This study investigates a host-switching event between a marine acanthocephalan specific to pinnipeds that is apparently able to reproduce in Magellanic penguins Spheniscus magellanicus from Brazil. Detailed analysis of morphological and morphometrical data from acanthocephalans from penguins indicates that they belong to Corynosoma australe Johnston, 1937. Partial fragments of the 28S rRNA and mitochondrial cox1 genes were amplified from isolates from penguins and two pinniped species (i.e. South American sea lion Otaria flavescens and South American fur seal Arctocephalus australis) to confirm this identification. Infection parameters clearly differ between penguins and the two pinniped species, which were significantly lower in S. magellanicus. The sex ratio of C. australe also differed between penguins and pinnipeds; in S. magellanicus was strongly biased against males, while in pinnipeds it was close to 1:1. Females of C. australe from O. flavescens were smaller than those from S. magellanicus and A. australis. However, fecundity (i.e. the proportion of fully developed eggs) was lower and more variable in females collected from S. magellanicus. At first glance, the occurrence of reproductive individuals of C. australe in Magellanic penguins could be interpreted as an adaptive colonization of a novel avian host through favourable mutations. However, it could also be considered, perhaps more likely, as an example of ecological fitting through the use of a plesimorphic (host) resource, since the ancestors of Corynosoma infected aquatic birds.

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          On Ecological Fitting

          D. Janzen (1985)
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            On ecological fitting, plant-insect associations, herbivore host shifts, and host plant selection

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              Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution.

              Ecological fitting is the process whereby organisms colonize and persist in novel environments, use novel resources or form novel associations with other species as a result of the suites of traits that they carry at the time they encounter the novel condition. This paper has four major aims. First, we review the original concept of ecological fitting and relate it to the concept of exaptation and current ideas on the positive role of phenotypic plasticity in evolution. Second, we propose phenotypic plasticity, correlated trait evolution and phylogenetic conservatism as specific mechanisms behind ecological fitting. Third, we attempt to operationalize the concept of ecological fitting by providing explicit definitions for terms. From these definitions, we propose a simple conceptual model of ecological fitting. Using this model, we demonstrate the differences and similarities between ecological fitting and ecological resource tracking and illustrate the process in the context of species colonizing new areas and forming novel associations with other species. Finally, we discuss how ecological fitting can be both a precursor to evolutionary diversity or maintainer of evolutionary stasis, depending on conditions. We conclude that ecological fitting is an important concept for understanding topics ranging from the assembly of ecological communities and species associations, to biological invasions, to the evolution of biodiversity.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: VisualizationRole: Writing – original draft
                Role: Funding acquisitionRole: Project administrationRole: Writing – review & editing
                Role: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Funding acquisitionRole: Project administrationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                5 October 2017
                2017
                : 12
                : 10
                : e0183809
                Affiliations
                [1 ] Centro de Investigación Aplicada y Transferencia Tecnológica en Recursos Marinos Almirante Storni (CIMAS–CCT CONICET–CENPAT) y Escuela Superior de Ciencias Marinas (ESCiMar), Universidad Nacional del Comahue, San Antonio Oeste, Río Negro, Argentina
                [2 ] Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, Seropédica, Rio de Janeiro, Brazil
                [3 ] Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic
                [4 ] Instituto Cavanilles de Biodiversidad y Biología Evolutiva, Parque Científico, Universidad de Valencia, Paterna, Valencia, Spain
                [5 ] Centro para el Estudio de Sistemas Marinos CESIMAR, CENPAT-CONICET, Puerto Madryn, Chubut, Argentina
                [6 ] Universidad Nacional de la Patagonia San Juan Bosco UNPSJB, Sede Puerto Madryn, Puerto Madryn, Chubut, Argentina
                Institute of Tropical Medicine, JAPAN
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-8177-7959
                Article
                PONE-D-17-15667
                10.1371/journal.pone.0183809
                5628790
                28981550
                aa1e1cf8-73a6-4e28-a9ab-737658f5ef9a
                © 2017 Hernández-Orts et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 24 April 2017
                : 13 August 2017
                Page count
                Figures: 6, Tables: 3, Pages: 23
                Funding
                Funded by: Conselho Nacional de Desenvovimento Científico e Tecnológico (CNPq)
                Award ID: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)
                Award Recipient :
                Funded by: Conselho Nacional de Desenvovimento Científico e Tecnológico (CNPq)
                Award ID: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)
                Award Recipient :
                Funded by: Ministry of Economy and Competitiveness of Spain
                Award ID: CGL2012–39545
                Award Recipient :
                Funded by: Generalitat Valenciana
                Award ID: PROMETEO/2011/040
                Award Recipient :
                Funded by: Czech Academy of Sciences
                Award ID: Postdoctoral fellowship
                Award Recipient :
                This study was partially supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) ( http://cnpq.br/) of Brazil to MB and JLL, the Ministry of Economy and Competitiveness ( http://www.mineco.gob.es/portal/site/mineco/) of Spain through the project CGL2012–39545 to FJA, the Generalitat Valenciana ( http://www.ceice.gva.es/web/ciencia) thought the project PROMETEO/2011/040 to JAR, and by Czech Academy of Sciences ( http://www.avcr.cz/en/) postdoctoral fellowship to SG. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Seabirds
                Penguins
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Biology and Life Sciences
                Population Biology
                Population Metrics
                Sex Ratio
                Earth Sciences
                Geomorphology
                Topography
                Landforms
                Islands
                Biology and Life Sciences
                Population Biology
                Population Metrics
                Fecundity
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Animal Phylogenetics
                Biology and Life Sciences
                Taxonomy
                Evolutionary Systematics
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                Computer and Information Sciences
                Data Management
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Animal Phylogenetics
                Biology and Life Sciences
                Zoology
                Animal Phylogenetics
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Biology and Life Sciences
                Marine Biology
                Marine Ornithology
                Earth Sciences
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                Marine Biology
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                Biology and Life Sciences
                Zoology
                Ornithology
                Marine Ornithology
                Custom metadata
                Voucher material is housed in the National Helminth Collection, Biology Institute, National Autonomous University of Mexico, Mexico City (CNHE 10448) and the Helminthological collection of the Oswaldo Cruz Institute, Rio de Janeiro, Brazil (CHIOC 38874–38877). Sequence data are available from GenBank (MF497330–MF497332 for 28S, MF497333–MF497335 for cox1). Data are supplied in Tables or Additional files.

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