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      Worldwide paleodistribution of capillariid parasites: Paleoparasitology, current status of phylogeny and taxonomic perspectives

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          Abstract

          Introduction

          Paleoparasitology, the study of parasites in the past, brings the knowledge of where and when they occurred in preterit populations. Some groups of parasites, as capillariids, have a complex and controversial systematic, hindering the paleoparasitological diagnosis. In this article, we synthesized the occurrence of capillariids in both the New and the Old World in ancient times, and discussed the difficulty of the diagnosis of species and the strategies for identification. The present review also shows the current status of the phylogeny in capillariids and indicates the necessity to try new approaches for a better understanding of capillariid paleodistribution.

          Methods

          For the systematic review, a predefined guideline defined by PRISMA was used. The articles collected were identified, screened, and included in the review following criteria for eligibility. The current status of the phylogeny of capillariids was accessed using MUSCLE, Bioedit v.7.0.5 and MEGA v. 7.0.21 programs.

          Results

          The review discussed 38 articles that presented information about capillariids in past populations. Most of capillariid eggs found in the New and Old World were not identified. However, Calodium hepaticum eggs were the most identified, as some from Eucoleus genus. It was observed that sites from the New World had a better chance for capillariid egg identification, due to previous knowledge of its host, when compared to the Old World. In the 18S rDNA phylogenetic analyses, two datasets were constructed, one including sequences from 7 Moravec’s genera, where 3 genus-specific clusters, with high bootstrap values, could be observed for Capillaria (ML = 99%, NJ = 96%), Eucoleus (ML / NJ = 100%) and Paratrichosoma (ML / NJ = 100%). A fourth cluster of 18S rDNA dataset I revealed lack of definition of Pearsonema and Aonchotheca genera. The 18S rDNA dataset II comprised 8 Moravec’s genera and defined 3 clusters, 2 genus-specific for Eucoleus (ML = 99%, NJ = 100%) and Capillaria (ML / NJ = 98%). The third 18S rDNA dataset II cluster included 6 genera and exhibited, once again, Pearsonema and Aonchotheca poor discrimination. The cox1 gene data consist of 4 Moravec’s genera, and in spite of grouping some species-specific clusters, did not show genera-specific definition.

          Conclusions

          Despite the numerous archaeological findings, both in the New and the Old Worlds, the identification of capillariid species based on the morphology and morphometry of eggs remains imprecise, often resulting in a generic diagnosis of a group or morphotype of capillariid. Capillariid is one of the most diverse group of helminths recovered in archaeological sites. The phylogenetic trees produced in this study showed limited genetic information available, unresolved genera and incongruence with the classical taxonomy. The elucidation of the paleodistribution of capillariids can give insights of the ancient host-parasite associations but also in modern sceneries.

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          Most cited references45

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          Programmatic access to bioinformatics tools from EMBL-EBI update: 2017

          Abstract Since 2009 the EMBL-EBI provides free and unrestricted access to several bioinformatics tools via the user's browser as well as programmatically via Web Services APIs. Programmatic access to these tools, which is fundamental to bioinformatics, is increasingly important as more high-throughput data is generated, e.g. from proteomics and metagenomic experiments. Access is available using both the SOAP and RESTful approaches and their usage is reviewed regularly in order to ensure that the best, supported tools are available to all users. We present here an update describing the latest enhancement to the Job Dispatcher APIs as well as the governance under it.
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            Coprolite deposits reveal the diet and ecology of the extinct New Zealand megaherbivore moa (Aves, Dinornithiformes)

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              A Megafauna’s Microfauna: Gastrointestinal Parasites of New Zealand’s Extinct Moa (Aves: Dinornithiformes)

              We perform the first multidisciplinary study of parasites from an extinct megafaunal clade using coprolites from the New Zealand moa (Aves: Dinornithiformes). Ancient DNA and microscopic analyses of 84 coprolites deposited by four moa species (South Island giant moa, Dinornis robustus; little bush moa, Anomalopteryx didiformis; heavy-footed moa, Pachyornis elephantopus; and upland moa, Megalapteryx didinus) reveal an array of gastrointestinal parasites including coccidians (Cryptosporidium and members of the suborder Eimeriorina), nematodes (Heterakoidea, Trichostrongylidae, Trichinellidae) and a trematode (Echinostomida). Parasite eggs were most prevalent and diverse in coprolites from lowland sites, where multiple sympatric moa species occurred and host density was therefore probably higher. Morphological and phylogenetic evidence supports a possible vicariant Gondwanan origin for some of the moa parasites. The discovery of apparently host-specific parasite taxa suggests paleoparasitological studies of megafauna coprolites may provide useful case-studies of coextinction.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: SupervisionRole: ValidationRole: Writing – review & editing
                Role: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: 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
                30 April 2019
                2019
                : 14
                : 4
                : e0216150
                Affiliations
                [1 ] Laboratório de Helmintologia Romero Lascasas Porto, Faculdade de Ciências Médicas, Universidade do Estado do Rio de Janeiro (FCM/UERJ), Rio de Janeiro, Rio de Janeiro, Brazil
                [2 ] Laboratório de Biologia de Tripanosomatídeos, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz (IOC/FIOCRUZ), Rio de Janeiro, Rio de Janeiro, Brazil
                [3 ] University of Bourgogne Franche-Comte, CNRS UMR 6249 Chrono-environment, Besançon, France
                Onderstepoort Veterinary Institute, SOUTH AFRICA
                Author notes

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

                Author information
                http://orcid.org/0000-0002-9788-9533
                Article
                PONE-D-18-29971
                10.1371/journal.pone.0216150
                6490956
                31039193
                6abb7ced-5107-4e73-a56a-90bbb3a72265
                © 2019 Borba 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
                : 9 November 2018
                : 15 April 2019
                Page count
                Figures: 6, Tables: 2, Pages: 19
                Funding
                Funded by: Fundação de Amparo a Pesquisa do Rio de Janeiro
                Award ID: 26/202.945/2016
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 307932/2014-1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 312934/2017-3
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;
                Award ID: 23038000059/2015-61
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;
                Award ID: 23038000059/2015-61
                Award Recipient :
                Funded by: Comité français d’évaluation de la coopération universitaire et scientifique avec le Brésil
                Award ID: 33387UA
                Award Recipient :
                Funded by: Comité français d’évaluation de la coopération universitaire et scientifique avec le Brésil (FR)
                Award ID: 33387UA
                Award Recipient :
                Funded by: Comité français d’évaluation de la coopération universitaire et scientifique avec le Brésil
                Award ID: 33387UA
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 470724/2014-5
                Award Recipient :
                We declare that all the funding or sources of support received during this specific study are presented. This study was supported by grants-in-aid and fellowship from Fundação de Amparo à Pesquisa do Rio de Janeiro ( http://www.faperj.br/) (AMI, grant number 26/202.945/2016); fellowships from Conselho Nacional de Desenvolvimento Científico e Tecnológico ( http://www.cnpq.br/) (AMI, grant number 307932/2014-1 and 312934/2017-3) (JRMS, grant number 470724/2014-5); grants-in-aid and fellowships from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior ( http://www.capes.gov.br/) (AMI and VHB, grant number 23038000059/2015-61) and grants-in-aid and fellowships from the Comité français d’évaluation de la coopération universitaire et scientifique avec le Brésil, COFECUB research and cooperation program ( https://www.campusfrance.org/fr/cofecub) (AMI, ML and VHB, grant number 33387UA). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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