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The genetic structure of the marine flatworm Stylochoplana pusilla (Rhabditophora: Polycladida) and its use of intertidal snails

Published online by Cambridge University Press:  15 July 2020

Daishi Yamazaki Open the ORCID record for Daishi Yamazaki [Opens in a new window] ,
Tomoki Aota  and
Satoshi Chiba
Daishi Yamazaki*
Affiliation:
Center for Northeast Asian Studies, Tohoku University, 41 Kawauchi, Aoba-ku, Sendai, Miyagi, 980-8576, Japan
Tomoki Aota
Affiliation:
Department of Ecology and Evolutionary Biology, Graduate School of Life Science, Tohoku University, Aobayama, Aoba-ku, Sendai, Miyagi980-8578, Japan
Satoshi Chiba
Affiliation:
Center for Northeast Asian Studies, Tohoku University, 41 Kawauchi, Aoba-ku, Sendai, Miyagi, 980-8576, Japan Department of Ecology and Evolutionary Biology, Graduate School of Life Science, Tohoku University, Aobayama, Aoba-ku, Sendai, Miyagi980-8578, Japan
*
Author for correspondence: Daishi Yamazaki, E-mail: zaki.daishi@gmail.com
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Abstract

Although marine phylogeographers have accumulated knowledge of the evolutionary history of various invertebrates, there is a large bias among the taxa regarding genetic data. The order Polycladida is a typical example for which little genetic information at population level is available. Here, we focused on the polyclad flatworm Stylochoplana pusilla, distributed in the Japanese Pacific coastal area. Stylochoplana pusilla is known to have commensal relationships with certain intertidal snails, using snails (mainly Monodonta confusa) as a refugee house. During low tide, S. pusilla hides in the mantle cavity of snails to protect themselves from desiccation and predation. Here, we investigated the genetic structure of S. pusilla using a mitochondrial Cytochrome Oxidase I marker and the species diversity of snails used by it. We found that S. pusilla has high genetic diversity of its populations. While S. pusilla showed a significant genetic differentiation among populations, it was relatively low. In addition, we also showed that S. pusilla used several intertidal snail species which inhabit various coastal environments. The present study suggests S. pusilla has sufficient dispersal ability to connect among its local populations. Also, the range of available snails for S. pusilla may help the connectivity among local populations. We provide important knowledge about this invertebrate taxon with a unique ecology, which has been insufficiently studied.

Keywords

Cytochrome Oxidase Igenetic structuremarine flatwormPolycladidaRhabditophora
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 100 , Issue 5 , August 2020 , pp. 713 - 717
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

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References

Aguado, MT, Noreña, C, Alcaraz, L, Marquina, D, Brusa, F, Damborenea, C, Almon, B, Bleidorn, C and Grande, C (2017) Phylogeny of Polycladida (Platyhelminthes) based on mtDNA data. Organisms Diversity and Evolution 17, 767–778.CrossRefGoogle Scholar
Bahia, J and Schrödl, M (2016) Pseudobiceros wirtzi sp. nov. (Polycladida: Cotylea) from Senegal with revision of valid species of the genus. Zootaxa 4097, 101–117.CrossRefGoogle ScholarPubMed
Bahia, J, Padula, V, Correia, MD and Sovierzoski, HH (2015) First records of the order Polycladida (Platyhelminthes, Rhabditophora) from reef ecosystems of Alagoas State, north-eastern Brazil, with the description of Thysanozoon alagoensis sp. nov. Journal of the Marine Biological Association of the United Kingdom 95, 1–14.CrossRefGoogle Scholar
Bahia, J, Padula, V and Schrödl, M (2017) Polycladida phylogeny and evolution: integrating evidence from 28S rDNA and morphology. Organism Diversity and Evolution 17, 653–678.Google Scholar
Crandall, ED, Riginos, C, Bird, CE, Liggins, L, Treml, E, Beger, M, Barber, PH, Connolly, SR, Cowman, PF, DiBattista, JD and Eble, JA (2019) Contributing members of the Diversity of the Indo-Pacific Network. The molecular biogeography of the Indo-Pacific: testing hypotheses with multispecies genetic patterns. Global Ecology and Biogeography 28, 943–960.Google Scholar
Deguchi, R, Sasaki, H, Iwata, K and Echizen, M (2009) Reproduction and life cycle of the polyclad flatworm. Bulletin Miyagi University Education 44, 53–61.Google Scholar
Dillon, RT and Robinson, JD (2009) The snails the dinosaurs saw: are the pleurocerid populations of the Older Appalachians a relict of the Paleozoic era? Journal of the North American Benthological Society 28, 1–11.CrossRefGoogle Scholar
Dittmann, IL, Cuadrado, D, Aguado, MT et al. (2019) Polyclad phylogeny persists to be problematic. Organisms Diversity and Evolution 19, 585–608.Google Scholar
Doignon, G, Artois, T and Deheyn, D (2003) Discoplana malagasensis sp. nov., a new turbellarian (Platyhelminthes: Polycladida: Leptoplanidae) symbiotic in a ophiuroid (Echinodermata), with a cladistic analysis of the Discoplana/Euplana species. Zoological Science 20, 357–369.CrossRefGoogle Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle ScholarPubMed
Excoffier, L and Lischer, HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.CrossRefGoogle ScholarPubMed
Excoffier, L, Smouse, PE and Quattro, JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.Google ScholarPubMed
Faubel, A, Sluys, R and Reid, DG (2007) A new genus and species of polyclad flatworm found in the mantle cavities of gastropod molluscs in the high-intertidal zone of the Pacific coast of Central America. Journal of the Marine Biological Association of the United Kingdom 87, 429–434.Google Scholar
Fujiwara, Y, Urabe, J and Takeda, S (2014) Host preference of a symbiotic flatworm in relation to the ecology of littoral snails. Marine Biology 161, 1873–1882.CrossRefGoogle Scholar
Fujiwara, Y, Iwata, T, Urabe, J and Takeda, S (2016) Life history traits and ecological conditions influencing the symbiotic relationship between the flatworm Stylochoplana pusilla and host snail Monodonta labio. Journal of the Marine Biological Association of the United Kingdom 96, 667–672.Google Scholar
Griekspoor, A and Groothuis, T (2005) 4peaks. Ver. 1.7.1. http://nucleo-bytes.com/4peaks/.Google Scholar
Hirase, S, Ikeda, M, Kanno, M and Kijima, A (2012) Phylogeography of the intertidal goby Chaenogobius annularis associated with paleoenvironmental changes around the Japanese Archipelago. Marine Ecology Progress Series 450, 167–179.CrossRefGoogle Scholar
Kato, K (1933) On Stylochoplana pusilla Bock. Doubutugaku Zasshi 45, 487–490.Google Scholar
Kato, K (1935) Stylochoplana parasitica sp. nov., a polyclad parasitic in the pallial groove of the chiton. Annotationes zoologicae Japonenses 15, 123–129.Google Scholar
Kato, K (1965) Stylochoplana pusilla Bock. In Okada, K (ed.), New Illustrated Encyclopedia of the Fauna of Japan, vol. 1. Tokyo: Hokuryukan Co., p. 324.Google Scholar
Keyse, J, Crandall, ED, Toonen, RJ, Meyer, CP, Treml, EA and Riginos, C (2014) The scope of published population genetic data for Indo-Pacific marine fauna and future research opportunities in the region. Bulletin of Marine Science 90, 47–78.CrossRefGoogle Scholar
Kojima, S, Segawa, R and Hayashi, I (1997) Genetic differentiation among populations of the Japanese turban shell Turbo (Batillus) cornutus corresponding to warm current. Marine Ecology Progress Series 150, 149–155.CrossRefGoogle Scholar
Leigh, JW and Bryant, D (2015) PopART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.CrossRefGoogle Scholar
Li, S, Jovelin, R, Yoshiga, T, Tanaka, R and Cutter, AC (2014) Specialist versus generalist life histories and nucleotide diversity in Caenorhabditis nematodes. Proceedings of the Royal Society B: Biological Sciences 281, 1777.Google ScholarPubMed
Litvaitis, MK, Bolaños, DM and Quiroga, SY (2010) When names are wrong and colours deceive: unravelling the Pseudoceros bicolor species complex (Turbellaria: Polycladida). Journal of Natural History 44, 13–14.CrossRefGoogle Scholar
Litvaitis, MK, Bolaños, DM and Quiroga, YS (2019) Systematic congruence in Polycladida (Platyhelminthes, Rhabditophora): are DNA and morphology telling the same story? Zoological Journal of the Linnean Society 186, 865–891.CrossRefGoogle Scholar
Lytwyn, MW and McDermott, JI (1976) Incidence, reproduction and feeding of Stylochus zebra, a polyclad turbellarian symbiont of hermit crabs. Marine Biology 38, 365–372.CrossRefGoogle Scholar
Martín-Durán, JM and Egger, B (2012) Developmental diversity in free-living flatworms. EvoDevo 3, 1–22.CrossRefGoogle ScholarPubMed
Newman, L and Cannon, L (2003) Marine Flatworms: The World of Polyclads. Collingwood: CSIRO.CrossRefGoogle Scholar
Oya, Y and Kajihara, H (2017) Description of a new Notocomplana species (Platyhelminthes: Acotylea), new combination and new records of Polycladida from the northeastern Sea of Japan, with a comparison of two different barcoding markers. Zootaxa 4282, 526–542.CrossRefGoogle Scholar
Oya, Y and Kajihara, H (2019) A new bathyal species of Cestoplana (Polycladida: Cotylea) from the West Pacific Ocean. Marine Biodiversity 49, 905–911.CrossRefGoogle Scholar
Quiroga, SY, Bolaños, DM and Litvaitis, MK (2006) First description of deep-sea polyclad flatworms from the North Pacific: Anocellidus n. Gen. profundus n. sp. (Anocelidae, n. Fam.) and Oligocladus Voightae n. sp. (Euryleptidae). Zootaxa 1317, 1–19.CrossRefGoogle Scholar
Sasaki, T (2017) Superfamily Trochoidea. In Okutani, T (ed.), Marine Mollusks in Japan, 2nd Edn. Tokyo: Tokai University Press, pp. 747–765.Google Scholar
Takenouchi, K (1985) An analysis of shell character and distribution of the intertidal trochid, Monodonta labio (Linné) (Gastropoda: Prosobranchia). Venus 44, 110–122.Google Scholar
Thompson, JD, Higgins, DG and Gibson, TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Tsunashima, T, Hagiya, M, Yamada, R, Koito, T, Tsuyuki, N, Izawa, S, Kosoba, K, Itoi, S and Sugita, H (2017) A molecular framework for the taxonomy and systematics of Japanese marine turbellarian flatworms (Platyhelminthes, Polycladida). Aquatic Biology 26, 159–167.CrossRefGoogle Scholar
Tsuyuki, A, Oya, Y and Kajihara, H (2019) A new species of Prosthiostomum (Platyhelminthes: Polycladida) from Shirahama, Japan. Species Diversity 24, 137–143.CrossRefGoogle Scholar
Yamazaki, D, Miura, O, Ikeda, M, Kijima, A, Van Tu, D, Sasaki, T and Chiba, S (2017) Genetic diversification of intertidal gastropoda in an archipelago: the effects of islands, oceanic currents and ecology. Marine Biology 164, 184.CrossRefGoogle Scholar
Yamazaki, D, Hirano, T, Uchida, S, Miura, O and Chiba, S (2019) Relationship between contrasting morphotypes and the phylogeny of the marine gastropoda genus Tegula in East Asia. Journal of Molluscan Studies 84, 24–34.CrossRefGoogle Scholar
Williams, JD and McDermott, JJ (2004) Hermit crab biocoenoses: a worldwide review of the diversity and natural history of hermit crab associates. Journal of Experimental Marine Biology and Ecology 305, 1–128.CrossRefGoogle Scholar
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