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Bidirectional Introgressive Hybridization between a Cattle and Human Schistosome Species

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      Abstract

      Schistosomiasis is a disease of great medical and veterinary importance in tropical and subtropical regions, caused by parasitic flatworms of the genus Schistosoma (subclass Digenea). Following major water development schemes in the 1980s, schistosomiasis has become an important parasitic disease of children living in the Senegal River Basin (SRB). During molecular parasitological surveys, nuclear and mitochondrial markers revealed unexpected natural interactions between a bovine and human Schistosoma species: S. bovis and S. haematobium, respectively. Hybrid schistosomes recovered from the urine and faeces of children and the intermediate snail hosts of both parental species, Bulinus truncatus and B. globosus, presented a nuclear ITS rRNA sequence identical to S. haematobium, while the partial mitochondrial cox1 sequence was identified as S. bovis. Molecular data suggest that the hybrids are not 1st generation and are a result of parental and/or hybrid backcrosses, indicating a stable hybrid zone. Larval stages with the reverse genetic profile were also found and are suggested to be F1 progeny. The data provide indisputable evidence for the occurrence of bidirectional introgressive hybridization between a bovine and a human Schistosoma species. Hybrid species have been found infecting B. truncatus, a snail species that is now very abundant throughout the SRB. The recent increase in urinary schistosomiasis in the villages along the SRB could therefore be a direct effect of the increased transmission through B. truncatus. Hybridization between schistosomes under laboratory conditions has been shown to result in heterosis (higher fecundity, faster maturation time, wider intermediate host spectrum), having important implications on disease prevalence, pathology and treatment. If this new hybrid exhibits the same hybrid vigour, it could develop into an emerging pathogen, necessitating further control strategies in zones where both parental species overlap.

      Author Summary

      Schistosome blood flukes cause significant disease in humans and their livestock in tropical and subtropical regions of the world. They have a two host-life cycle with a sexual stage within the mammalian host and are transmitted through water contact. Understanding the biology of these dioecious parasites is essential for developing strategies for control of schistosomiasis. Hybridization between schistosome species can occur, but in most cases host specificity and ecology are thought to maintain species barriers. Here, we report on the emergence of a new hybrid strain of schistosome found in northern Senegalese children, resulting from introgressive hybridization between a bovine and human parasite. This situation may have arisen due to the increased number of water contact sites commonly used by both cattle and people linked to recent major water development projects. Our findings have come to light due to optimized sampling and genotyping techniques of individual schistosome larval stages. Gene exchange following hybridization can lead to phenotypic innovations that can ultimately lead to the emergence of new diseases. The impact on disease epidemiology is only now unfolding, and it is essential to monitor the situation closely and move swiftly to control this rapidly evolving situation.

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      Most cited references 29

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      Hybridization as an invasion of the genome.

       James Mallet (2005)
      Hybridization between species is commonplace in plants, but is often seen as unnatural and unusual in animals. Here, I survey studies of natural interspecific hybridization in plants and a variety of animals. At least 25% of plant species and 10% of animal species, mostly the youngest species, are involved in hybridization and potential introgression with other species. Species in nature are often incompletely isolated for millions of years after their formation. Therefore, much evolution of eventual reproductive isolation can occur while nascent species are in gene-flow contact, in sympatry or parapatry, long after divergence begins. Although the relative importance of geographic isolation and gene flow in the origin of species is still unknown, many key processes involved in speciation, such as 'reinforcement' of post-mating isolation by the evolution of assortative mating, will have ample opportunity to occur in the presence of continuing gene flow. Today, DNA sequence data and other molecular methods are beginning to show that limited invasions of the genome are widespread, with potentially important consequences in evolutionary biology, speciation, biodiversity, and conservation.
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        Hybridization and adaptive radiation.

         Ole Seehausen (2004)
        Whether interspecific hybridization is important as a mechanism that generates biological diversity is a matter of controversy. Whereas some authors focus on the potential of hybridization as a source of genetic variation, functional novelty and new species, others argue against any important role, because reduced fitness would typically render hybrids an evolutionary dead end. By drawing on recent developments in the genetics and ecology of hybridization and on principles of ecological speciation theory, I develop a concept that reconciles these views and adds a new twist to this debate. Because hybridization is common when populations invade new environments and potentially elevates rates of response to selection, it predisposes colonizing populations to rapid adaptive diversification under disruptive or divergent selection. I discuss predictions and suggest tests of this hybrid swarm theory of adaptive radiation and review published molecular phylogenies of adaptive radiations in light of the theory.
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          Natural hybridization and the evolution of domesticated, pest and disease organisms.

          The role of natural hybridization in the evolutionary history of numerous species is well recognized. The impact of introgressive hybridization and hybrid speciation has been documented especially in plant and animal assemblages. However, there remain certain areas of investigation for which natural hybridization and its consequences remain under-studied and under-appreciated. One such area involves the evolution of organisms that positively or negatively affect human populations. In this review, I highlight exemplars of how natural hybridization has contributed to the evolution of (i) domesticated plants and animals; (ii) pests; (iii) human disease vectors; and (iv) human pathogens. I focus on the effects from genetic exchange that may lead to the acquisition of novel phenotypes and thus increase the beneficial or detrimental (to human populations) aspects of the various taxa.
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            Author and article information

            Affiliations
            [1 ]Institute of Tropical Medicine, Department of Parasitology, Antwerpen, Belgium
            [2 ]Laboratory of Animal Diversity and Systematics, Katholieke Universiteit Leuven, Leuven, Belgium
            [3 ]Wolfson Wellcome Biomedical Laboratories, Department of Zoology, The Natural History Museum, London, United Kingdom
            [4 ]Institut Sénégalais de Recherches Agricoles (ISRA), Bel Air, Dakar, Sénégal
            Case Western Reserve University, United States of America
            Author notes

            Conceived and designed the experiments: TH BLW JRS. Performed the experiments: TH BLW SG OTD. Analyzed the data: TH BLW JRS. Contributed reagents/materials/analysis tools: TH KP DR. Wrote the paper: TH BLW DR. Designed the multiplex PCR protocol and performed the fieldwork for the KUL part of the study: TH. Performed most part of the field work relating to CONTRAST: BLW. Played a role in the planning and organization of aspects of the field and laboratory work relating to CONTRAST: JRS. Coordinated the fieldwork relating to CONTRAST: OTD. Coordinated the fieldwork in Senegal and is in charge of the Senegalese field team; trained the field team and provided all material and working space in Senegal; provided useful suggestions for the manuscript: KP. Is in charge of the CONTRAST program in Senegal: DR.

            Contributors
            Role: Editor
            Journal
            PLoS Pathog
            plos
            plospath
            PLoS Pathogens
            Public Library of Science (San Francisco, USA )
            1553-7366
            1553-7374
            September 2009
            September 2009
            4 September 2009
            : 5
            : 9
            2731855
            19730700
            09-PLPA-RA-0922R2
            10.1371/journal.ppat.1000571
            (Editor)
            Huyse 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.
            Counts
            Pages: 9
            Categories
            Research Article
            Ecology/Evolutionary Ecology
            Infectious Diseases/Epidemiology and Control of Infectious Diseases
            Infectious Diseases/Helminth Infections
            Infectious Diseases/Neglected Tropical Diseases

            Infectious disease & Microbiology

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