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      Phylogeography and genetics of the globally invasive snail Physa acuta Draparnaud 1805, and its potential to serve as an intermediate host to larval digenetic trematodes

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          Abstract

          Background

          Physa acuta is a globally invasive freshwater snail native to North America. Prior studies have led to conflicting views of how P. acuta populations are connected and genetic diversity is partitioned globally. This study aims to characterize phylogeographic and population genetic structure within the native range of P. acuta, elucidate its invasion history and assess global patterns of genetic diversity. Further, using meta-analytic methods, we test the ‘Enemy-Release hypothesis’ within the P. acuta – digenetic trematode system. The ‘Enemy-Release hypothesis’ refers to the loss of native parasites following establishment of their host within an invasive range. Population genetic data is combined with surveys of trematode infections to map range-wide trematode species richness associated with P. acuta, and to identify relevant host-population parameters important in modeling host-parasite invasion.

          Results

          Phylogenetic analyses using mtDNA uncovered two major clades (A & B). Clade A occurs globally while clade B was only recovered from the Western USA. All invasive populations sampled grouped within Clade A, where multiple independent source populations were identified from across North America. Significant population genetic structure was found within the native range of P. acuta, with some evidence for contemporary geographic barriers between western and eastern populations. Mito-nuclear discordance was found suggesting historical isolation with secondary contact between the two mitochondrial clades. Trematode species richness was found to differ significantly between native and invasive populations, in concordance with the ‘Enemy-Release hypothesis’. Further, our data suggests a positive relationship between nucleotide diversity of invasive populations and trematode prevalence and richness.

          Conclusions

          This study includes a wider geographic sampling of P. acuta within its native range that provides insight into phylogeographic and population genetic structure, range-wide genetic diversity and estimation of the invasion history. Meta-analysis of P. acuta – trematode surveys globally is consistent with the ‘Enemy-Release hypothesis’. Additionally, results from this study suggest that host demographic parameters, namely genetic diversity as a proxy for population size, may play an essential role in how parasite communities assemble within invasive host populations. This knowledge can be used to begin to construct a framework to model host-parasite invasion dynamics over time.

          Electronic supplementary material

          The online version of this article (10.1186/s12862-018-1208-z) contains supplementary material, which is available to authorized users.

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          Most cited references79

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Reconstructing routes of invasion using genetic data: why, how and so what?

            Detailed knowledge about the geographical pathways followed by propagules from their source to the invading populations--referred to here as routes of invasion-provides information about the history of the invasion process and the origin and genetic composition of the invading populations. The reconstruction of invasion routes is required for defining and testing different hypotheses concerning the environmental and evolutionary factors responsible for biological invasions. In practical terms, it facilitates the design of strategies for controlling or preventing invasions. Most of our knowledge about the introduction routes of invasive species is derived from historical and observational data, which are often sparse, incomplete and, sometimes, misleading. In this context, population genetics has proved a useful approach for reconstructing routes of introduction, highlighting the complexity and the often counterintuitive nature of the true story. This approach has proved particularly useful since the recent development of new model-based methods, such as approximate Bayesian computation, making it possible to make quantitative inferences in the complex evolutionary scenarios typically encountered in invasive species. In this review, we summarize some of the fundamental aspects of routes of invasion, explain why the reconstruction of these routes is useful for addressing both practical and theoretical questions, and comment on the various reconstruction methods available. Finally, we consider the main insights obtained to date from studies of invasion routes. © 2010 Blackwell Publishing Ltd.
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              Parasite spillback: a neglected concept in invasion ecology?

              While there is good evidence linking animal introductions to impacts on native communities via disease emergence, our understanding of how such impacts occur is incomplete. Invasion ecologists have focused on the disease risks to native communities through "spillover" of infectious agents introduced with nonindigenous hosts, while overlooking a potentially more common mechanism of impact, that of "parasite spillback." We hypothesize that parasite spillback could occur when a nonindigenous species is a competent host for a native parasite, with the presence of the additional host increasing disease impacts in native species. Despite its lack of formalization in all recent reviews of the role of parasites in species introductions, aspects of the invasion process actually favor parasite spillback over spillover. We specifically review the animal-parasite literature and show that native species (arthropods, parasitoids, protozoa, and helminths) account for 67% of the parasite fauna of nonindigenous animals from a range of taxonomic groups. We show that nonindigenous species can be highly competent hosts for such parasites and provide evidence that infection by native parasites does spillback from nonindigenous species to native host species, with effects at both the host individual and population scale. We conclude by calling for greater recognition of parasite spillback as a potential threat to native species, discuss possible reasons for its neglect by invasion ecologists, and identify future research directions.
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                Author and article information

                Contributors
                gendron@unm.edu
                esloker@unm.edu
                sbrant@unm.edu
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                3 July 2018
                3 July 2018
                2018
                : 18
                : 103
                Affiliations
                ISNI 0000 0001 2188 8502, GRID grid.266832.b, Department of Biology, Museum of Southwestern Biology Parasite Division, Center for Evolutionary and Theoretical Immunology, , University of New Mexico, ; 167 Castetter MSCO3 2020, Albuquerque, NM 87131 USA
                Author information
                http://orcid.org/0000-0001-5987-9484
                Article
                1208
                10.1186/s12862-018-1208-z
                6029401
                29969987
                46852093-061b-4b24-a592-f1c5f02f2e38
                © The Author(s). 2018

                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
                : 31 August 2017
                : 5 June 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DEB 1021427
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: R37 AI101438
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2018

                Evolutionary Biology
                invasion genetics,physa,physidae,mitochondrial marker,trematode,parasite invasion,parasite richness,enemy-release

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