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Molecular-Genetic Analyses Reveal Cryptic Species of Trematodes in the Intertidal Gastropod, Batillaria Cumingi (Crosse)*

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Molecular-Genetic Analyses Reveal Cryptic Species of Trematodes in the Intertidal Gastropod, Batillaria Cumingi (Crosse)* International Journal for Parasitology 35 (2005) 793–801 www.parasitology-online.com Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse)* Osamu Miuraa,*, Armand M. Kurisb, Mark E. Torchinc, Ryan F. Hechingerb, Eleca J. Dunhamb, Satoshi Chibaa aDepartment of Ecology and Evolutionary Biology Graduate School of Life Sciences University of Tohoku, Aobayama, Sendai 980-8578, Japan bMarine Science Institute and Department of Ecology Evolution and Marine Biology University of California, Santa Barbara, California, CA 93106, USA cSmithsonian Tropical Research Institute, Apartado 2072, Balboa, Ancon, Republic of Panama Received 29 November 2004; received in revised form 14 February 2005; accepted 22 February 2005 Abstract Cryptic species of the digeneans, Cercaria batillariae (Heterophyidae) and an undescribed philophthalmid, were detected using polymerase chain reaction-based restriction fragment-length polymorphism methodology and sequence analyses. These digeneans were all collected from the same species of gastropod first intermediate host, Batillaria cumingi (ZBatillaria attramentaria). The mitochondrial cytochrome oxidase subunit 1 gene (approximately 800 bp) and nuclear internal transcribed spacer 1 gene (approximately 400 bp) were used for species level discrimination. Restriction fragment-length polymorphism analyses of cytochrome oxidase subunit 1 gene showed that C. batillariae included 10 distinguishable fragment patterns, and the philophthalmid included five patterns. On the basis of subsequent sequence analyses, the restriction fragment length polymorphism patterns of C. batillariae were grouped into eight phylogenetically distinct lineages and those of the philophthalmid into three phylogenetically distinct lineages. There was no evidence of gene flow among the different lineages due to the lack of heterozygosity within the observed internal transcribed spacer 1 gene fragment patterns. This suggests that all of these lineages are different species. Most of these species were widespread, but some exhibited restricted geographic distributions. We discuss the implications of these findings for host specificity of these trematodes. These results demonstrate the utility of genetic analysis to distinguish species of morphologically similar trematodes. Hence, trematode species diversity may often be underestimated when species identifications are limited to morphological features. q 2005 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. Keywords: Cryptic species; Batillaria cumingi; Cercaria batillariae; Restriction fragment-length polymorphism; Cytochrome oxidase subunit 1; Internal transcribed spacer 1 1. Introduction McManus and Bowles, 1996; Hung et al., 1999; Hus- peni, 2000. A molecular genetic analysis of host Cryptic species (or ‘sibling species’) are common in all specificity, continental geography, and recruitment major taxa (Knowlton, 1993). Although such species are dynamics of a larval trematode in a salt marsh snail, PhD genetically distinct from each other, they are morphologi- Dissertation. University of California, Santa Barbara; cally very similar. Parasitic taxa, due to their restricted Macnish et al., 2002; Donald et al., 2004). This is unfortunate morphology, appear to often manifest cryptic species (e.g. since the accurate identification of species is crucial for virtually any ecological or evolutionary investigation. Cryptic parasite species may differ in traits important to * Nucleotide sequence data reported in this paper are available in the host-parasite interactions, such as host susceptibility (e.g. GenBanke, EMBL and DDBJ databases under the accession numbers Reversat et al., 1989), pathogenesis (e.g. Homan and Mank, AY626457-AY262550. * Corresponding author. Tel.: C81 22 217 7813; fax: C81 22 217 7813. 2001; Haque et al., 2003), and epidemiology (e.g. Murrell E-mail address: [email protected] (O. Miura). and Pozio, 2000). 0020-7519/$30.00 q 2005 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.ijpara.2005.02.014 794 O. Miura et al. / International Journal for Parasitology 35 (2005) 793–801 Molecular genetic methods can distinguish otherwise cryptic species (Avise, 2004). Molecular methods are often used to identify species of bacteria and protozoans lacking major distinguishing morphologies (e.g. Perkins, 2000; Jenga et al., 2001). Molecular techniques can also be applied to helminths to enable identification of cryptic species and to reveal their phylogenetic relationships (e.g. Bowles and McManus, 1993; Bowles et al., 1995; Morgan and Blair, 1998; Hung et al., 1999; Huspeni, 2000. A molecular genetic analysis of host specificity, continental geography, and recruitment dynamics of a larval trematode in a salt marsh snail. Ph.D. Dissertation. University of California, Santa Barbara; Bell et al., 2001; Macnish et al., 2002; Olson et al., 2003; Donald et al., 2004). A comprehensive molecular genetic analysis of an assemblage of parasites infecting a single host species over a wide geographic range will help define the role of cryptic species in host-parasite interactions. The rich assemblage of larval trematodes in the Northeast Asian mud snail, Batillaria cumingi (ZBatillaria attramentaria), provides an excellent system to examine parasites within a single host species. This host snail has a broad geographic distribution throughout eastern Asia (Hasegawa, 2000) and Fig. 1. Map of Japan Islands with sample localities. Details of each locality is very common on mud flats of Japan (Adachi and Wada, are shown in Table 1. 1999). Further, B. cumingi has been introduced to the west daytime low tides between September and November 2003. coast of North America (Byers, 1999). This snail is infected Snails were identified following Adachi and Wada (1998). by at least nine morphologically recognized species of Snails were dissected under a stereo-microscope and digenean trematodes (Ito, 1957; Shimura and Ito, 1980; Rybakov and Lukomskaya, 1988; Harada, 1989; Harada and trematode species were identified based on previous work Suguri, 1989; Hechinger, unpublished data). All the on cercariae from B. cumingi (Ito, 1957; Shimura and Ito, described species are in taxa that use shorebirds as final 1980; Harada, 1989; Harada and Suguri, 1989; Hechinger, hosts and a variety of invertebrates and fishes as second unpublished data). The parasites were fixed with 70% K intermediate hosts. ethanol and stored at 20 8C for molecular analysis. DNA Here, by examining genetic variation in two of trematode of the two most prevalent species, C. batillariae morphospecies, we identify a previously unrecognized Table 1 substantial diversity of cryptic species of trematodes Collection localities and numbers of individual parasites used in restriction infecting a single host snail species. We also examine the fragment-length polymorphism and sequence analyses of the cytochrome phylogenetic relationships between the cryptic species oxidase subunit 1 and internal transcribed spacer 1 genes. Numbers to the groups and report on their geographic distributions in left of the slash are individuals of Cercaria batillariae and the numbers to Japan. One of the species we studied is the larval heterophyid, the right are individuals of the philophthalmid Cercaria batillariae Shimura and Ito, 1980. Members of the Site Name RFLP RFLP Sequence Heterophyidae use fishes as second intermediate hosts (CO1) (ITS1) analysis (CO1 (Yamaguti, 1975; Schell, 1985). The other species is an and ITS1) unnamed philophthalmid. Species of the Philophthalmidae 1 Toga Bay 17/0 – 4/0 (such as Cloacitrema spp. and Parorchis spp.) typically 2 Yamada Bay 12/1 12/1 10/1 3 Nagazura Bay 10/0 – 5/0 encyst on hard substrates. For both species that we studied, 4 Mangoku Bay 39/0 39/0 5/0 the life cycle is completed via trophic transmission of second 5 Matsushima Bay 28/0 – 4/0 intermediate hosts by bird final hosts. 6 Torinoumi 37/0 37/0 6/0 7 Matsukawa Bay 36/0 36/0 8/0 8 Obitsu River 18/6 – 5/2 9 Shiogawa 0/5 – 0/2 2. Materials and methods 10 Kumode River 44/1 44/1 11/1 11 Tanabe Bay 36/0 – 3/0 2.1. Study sites and sample collection 12 Ibo River 8/34 8/34 2/5 13 Kasuga River 5/22 5/22 5/6 Samples of B. cumingi were collected from 15 muddy 14 Hiroshima Bay 61/23 61/23 14/4 15 Ariakekai 3/2 – 2/2 shore and estuary sites in Japan (Fig. 1 and Table 1)on O. Miura et al. / International Journal for Parasitology 35 (2005) 793–801 795 (Heterophyidae) and the undescribed philophthalmid, was Five micro litre of the unpurified PCR products were isolated using a modification of the procedure described in digested for 10 h by the four-base cutting restriction Doyle and Doyle (1987). We recognized the philophthalmid enzyme, endonuclease Mse 1 (New England Biolabs). as a morphospecies using characters of the rediae and The restricted fragments were separated using electro- cercariae (such as the presence of profuse dark cystogenous phoresis in 4% Tris-acetate EDTA (TAE) agarose gels at glands). The larval trematodes from a single snail are 50 V for 4 h. Bands were visualized by staining with assumed to be the genetically identical products resulting ethidium bromide. Genotypes were identified based on the from the asexual reproduction of an individual trematode. A fragment patterns and scored individually for each DNA few rediae were separated from host snail tissue and region. homogenized in a solution of 300 ml of 2!hexadecyl- trimethylammonium
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