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      Fasciola Species Introgression: Just a Fluke or Something More?

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          Abstract

          The threats posed by a range of viral and bacterial zoonotic diseases inevitably receive renewed attention in the wake of global pandemic events due to their overt and devastating impacts on human health and the economy. Parasitic zoonoses, however, many of which affect millions of people each day, are frequently ignored. In the case of fasciolosis, caused by infection with Fasciola hepatica or Fasciola gigantica, this oversight has allowed for the expansion of areas of parasite sympatry and thus increased the incidence of hybridization and possible introgression between the two species. Here we highlight how an increased demand for animal-derived protein, combined with a lack of appropriate tools for detection of these events, is changing the status quo of these zoonotic parasites.

          Highlights

          • Increased demand for animal-derived protein from Fasciola hepatica-endemic countries has led to a growing number of reports of hybridization between F. hepatica and Fasciola gigantica in Southeast Asia.

          • Hybridization and eventual introgression have been reported in a range of protozoan, helminth, and arthropod parasites and act as important drivers of evolutionary change and adaptation.

          • Introgression between Fasciola spp. remains unproven but has potentially serious human and animal health consequences as seen in other parasites.

          • New tools for the characterization of hybridization and introgression events between Fasciola spp. are needed.

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          Most cited references62

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          Hybridization, introgression, and the nature of species boundaries.

          Species can be defined as populations that are diagnosably distinct, reproductively isolated, cohesive, or exclusive groups of organisms. Boundaries between species in sympatry are maintained by intrinsic barriers to gene exchange; these boundaries may not be uniform in space, in time, or across the genome. Here, we explore the nature of the species boundary, defined as the phenotypes/genes/genome regions that remain differentiated in the face of potential hybridization and introgression. We emphasize that species boundaries are semipermeable, with permeability (gene exchange) being a function of genome region. The early evidence for semipermeable species boundaries came from data on differential introgression in hybrid zones. This "genic view" of species was common in the hybrid zone literature even when few molecular markers were available to characterize genome-wide patterns of variation. Now, molecular tools allow detailed characterization of differentiation between diverging lineages and patterns of variation across natural hybrid zones, but the questions being asked by evolutionary biologists have remained much the same. Recent data (from DNA sequences and genotypes) reinforce earlier conclusions about the semipermeable nature of most species boundaries. However, debate persists over the nature and extent of genome divergence that accompanies speciation.
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            Fascioliasis and other plant-borne trematode zoonoses.

            Fascioliasis and other food-borne trematodiases are included in the list of important helminthiases with a great impact on human development. Six plant-borne trematode species have been found to affect humans: Fasciola hepatica, Fasciola gigantica and Fasciolopsis buski (Fasciolidae), Gastrodiscoides hominis (Gastrodiscidae), Watsonius watsoni and Fischoederius elongatus (Paramphistomidae). Whereas F. hepatica and F. gigantica are hepatic, the other four species are intestinal parasites. The fasciolids and the gastrodiscid cause important zoonoses distributed throughout many countries, while W. watsoni and F. elongatus have been only accidentally detected in humans. Present climate and global changes appear to increasingly affect snail-borne helminthiases, which are strongly dependent on environmental factors. Fascioliasis is a good example of an emerging/re-emerging parasitic disease in many countries as a consequence of many phenomena related to environmental changes as well as man-made modifications. The ability of F. hepatica to spread is related to its capacity to colonise and adapt to new hosts and environments, even at the extreme inhospitality of very high altitude. Moreover, the spread of F. hepatica from its original European range to other continents is related to the geographic expansion of its original European lymnaeid intermediate host species Galba truncatula, the American species Pseudosuccinea columella, and its adaptation to other lymnaeid species authochthonous in the newly colonised areas. Although fasciolopsiasis and gastrodiscoidiasis can be controlled along with other food-borne parasitoses, fasciolopsiasis still remains a public health problem in many endemic areas despite sustained WHO control programmes. Fasciolopsiasis has become a re-emerging infection in recent years and gastrodiscoidiasis, initially supposed to be restricted to Asian countries, is now being reported in African countries.
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              How reticulated are species?

              Many groups of closely related species have reticulate phylogenies. Recent genomic analyses are showing this in many insects and vertebrates, as well as in microbes and plants. In microbes, lateral gene transfer is the dominant process that spoils strictly tree‐like phylogenies, but in multicellular eukaryotes hybridization and introgression among related species is probably more important. Because many species, including the ancestors of ancient major lineages, seem to evolve rapidly in adaptive radiations, some sexual compatibility may exist among them. Introgression and reticulation can thereby affect all parts of the tree of life, not just the recent species at the tips. Our understanding of adaptive evolution, speciation, phylogenetics, and comparative biology must adapt to these mostly recent findings. Introgression has important practical implications as well, not least for the management of genetically modified organisms in pest and disease control.
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                Author and article information

                Journal
                Trends Parasitol
                Trends Parasitol
                Trends in Parasitology
                The Author(s). Published by Elsevier Ltd.
                1471-4922
                1471-5007
                21 October 2020
                21 October 2020
                Affiliations
                [1 ]Laboratory of Veterinary Parasitology, Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, Sydney, Australia
                Author notes
                [* ]Correspondence:
                Article
                S1471-4922(20)30250-6
                10.1016/j.pt.2020.09.008
                7575431
                33097425
                12310382-fa45-4670-bbba-bd3edd8a7819
                © 2020 The Author(s)

                Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.

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                Opinion

                Parasitology
                fasciolosis,hybridization,livestock,next-generation sequencing,southeast asia,zoonosis
                Parasitology
                fasciolosis, hybridization, livestock, next-generation sequencing, southeast asia, zoonosis

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