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      Parasite spillover: indirect effects of invasive Burmese pythons

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          Abstract

          Identification of the origin of parasites of nonindigenous species ( NIS) can be complex. NIS may introduce parasites from their native range and acquire parasites from within their invaded range. Determination of whether parasites are non‐native or native can be complicated when parasite genera occur within both the NIS’ native range and its introduced range. We explored potential for spillover and spillback of lung parasites infecting Burmese pythons ( Python bivittatus) in their invasive range (Florida). We collected 498 indigenous snakes of 26 species and 805 Burmese pythons during 2004–2016 and examined them for lung parasites. We used morphology to identify three genera of pentastome parasites, Raillietiella, a cosmopolitan form, and Porocephalus and Kiricephalus, both New World forms. We sequenced these parasites at one mitochondrial and one nuclear locus and showed that each genus is represented by a single species, R. orientalis, P. crotali, and K. coarctatus. Pythons are host to R. orientalis and P. crotali, but not K. coarctatus; native snakes are host to all three species. Sequence data show that pythons introduced R. orientalis to North America, where this parasite now infects native snakes. Additionally, our data suggest that pythons are competent hosts to P. crotali, a widespread parasite native to North and South America that was previously hypothesized to infect only viperid snakes. Our results indicate invasive Burmese pythons have affected parasite‐host dynamics of native snakes in ways that are consistent with parasite spillover and demonstrate the potential for indirect effects during invasions. Additionally, we show that pythons have acquired a parasite native to their introduced range, which is the initial condition necessary for parasite spillback.

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          The evolutionary impact of invasive species.

          Since the Age of Exploration began, there has been a drastic breaching of biogeographic barriers that previously had isolated the continental biotas for millions of years. We explore the nature of these recent biotic exchanges and their consequences on evolutionary processes. The direct evidence of evolutionary consequences of the biotic rearrangements is of variable quality, but the results of trajectories are becoming clear as the number of studies increases. There are examples of invasive species altering the evolutionary pathway of native species by competitive exclusion, niche displacement, hybridization, introgression, predation, and ultimately extinction. Invaders themselves evolve in response to their interactions with natives, as well as in response to the new abiotic environment. Flexibility in behavior, and mutualistic interactions, can aid in the success of invaders in their new environment.
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            Introduced species and their missing parasites.

            Damage caused by introduced species results from the high population densities and large body sizes that they attain in their new location. Escape from the effects of natural enemies is a frequent explanation given for the success of introduced species. Because some parasites can reduce host density and decrease body size, an invader that leaves parasites behind and encounters few new parasites can experience a demographic release and become a pest. To test whether introduced species are less parasitized, we have compared the parasites of exotic species in their native and introduced ranges, using 26 host species of molluscs, crustaceans, fishes, birds, mammals, amphibians and reptiles. Here we report that the number of parasite species found in native populations is twice that found in exotic populations. In addition, introduced populations are less heavily parasitized (in terms of percentage infected) than are native populations. Reduced parasitization of introduced species has several causes, including reduced probability of the introduction of parasites with exotic species (or early extinction after host establishment), absence of other required hosts in the new location, and the host-specific limitations of native parasites adapting to new hosts.
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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
                melissamiller@auburn.edu
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                10 December 2017
                January 2018
                : 8
                : 2 ( doiID: 10.1002/ece3.2018.8.issue-2 )
                : 830-840
                Affiliations
                [ 1 ] Department of Biological Sciences Auburn University Auburn AL USA
                [ 2 ] HelmWest Laboratory Missoula MT USA
                [ 3 ] Everglades National Park National Park Service Homestead FL USA
                [ 4 ] Fort Collins Science Center U.S. Geological Survey Fort Collins CO USA
                [ 5 ] Department of Wildlife Ecology and Conservation Ft. Lauderdale Research and Education Center University of Florida Ft. Lauderdale FL USA
                [ 6 ] Department of Wildlife Ecology and Conservation University of Florida Gainesville FL USA
                Author notes
                [*] [* ] Correspondence

                Melissa A. Miller, Department of Biological Sciences, Auburn University, Auburn, AL, USA.

                Email: melissamiller@ 123456auburn.edu

                Author information
                http://orcid.org/0000-0002-6743-6808
                http://orcid.org/0000-0003-1900-5648
                Article
                ECE33557
                10.1002/ece3.3557
                5773325
                29375757
                02f00a73-a370-4eff-963a-1885e54b1dbb
                © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 17 May 2017
                : 28 September 2017
                : 08 October 2017
                Page count
                Figures: 7, Tables: 0, Pages: 11, Words: 7586
                Funding
                Funded by: Auburn University
                Funded by: American Society of Ichthyologists and Herpetologists Gaige Award
                Funded by: Auburn University Dissertation Fellowship
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece33557
                January 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.3.1 mode:remove_FC converted:18.01.2018

                Evolutionary Biology
                biological invasion,everglades,parasite spillback,parasite spillover,pentastome,raillietiella bicaudata,raillietiella orientalis

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