Abstract
The accumulation of information on the geographical distribution range, genetic structure, and host utilization of the symbiont is important for studying how the symbiont spreads its distribution. Pseudocladophora conchopheria is a green alga that grows on the shells of intertidal gastropods distributed in the Japanese Archipelago, the Ryukyu Archipelago, and the southern part of Korean Peninsula. However, we discovered algae similar to P. conchopheria on the shells of gastropods from Vietnam. Therefore, species identification of the algae and the host gastropods was performed based on morphological observations and molecular genetic methods. As a result, the morphological characteristics of the algae were consistent with those of P. conchopheria, and the morphological characteristics of the host gastropods were consistent with those of Lunella granulata. Molecular genetic methods further supported these results of morphological identification. Interestingly, their algae were more closely related to P. conchopheria attached to L. correensis from the Sea of Japan rather than those attached to L. granulata from the Ryukyu Archipelago. These results suggest that P. conchopheria has expanded its distribution by utilizing multiple hosts and are explained on a wider scale than previous findings.
References
Boedeker C, O’Kelly CJ, Star W, Leliaert F (2012) Molecular phylogeny and taxonomy of the Aegagropila clade (Cladophorales, Ulvophyceae), including the description of Aegagropilopsis gen. nov. and Pseudocladophora gen. nov. J Phycol 48:808–825
Bridle JR, Buckley J, Bodsworth EJ, Thomas CD (2014) Evolution on the move: specialization on widespread resources associated with rapid range expansion in response to climate change. Proc Biol Sci 281:20131800
Cheng J, Sha Z-L (2017) Cryptic diversity in the Japanese mantis shrimp Oratosquilla oratoria (Crustacea: Squillidae): allopatric diversification, secondary contact and hybridization. Sci Rep 7:1972
Clark NJ, Clegg SM, Sam K, Goulding W, Koane B, Wellset K (2018) Climate, host phylogeny and the connectivity of host communities govern regional parasite assembly. Divers Distrib 24:13–23
Cornwell BH, Hernández L (2021) Genetic structure in the endosymbiont Breviolum “muscatinei” is correlated with geographical location, environment and host species. Proc Biol Sci 288:20202896
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoeket R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299
Gmelin JF (1791) Vermes. In: Gmelin JF (Ed.) Caroli a Linnaei Systema Naturae per Regna Tria Naturae, Ed. 13. Tome 1(6). Beer GE, Lipsiae [Leipzig]. pp. 3021-3910. Systema Naturae. Linneaeus (ed.). Ed. 13. 1: pars. 6.
Griekspoor A, Groothuis T (2006) 4Peaks. https://nucleobytes.com. Accessed 1 Apr 2024
Hanyuda T, Wakana I, Arai S, Miyaji K, Watano Y, Ueda K (2002) Phylogenetic relationships within Cladophorales (Ulvophyceae, Chlorophyta) inferred from 18S rRNA gene sequences, with sepecial reference to Aegagropila linnaei. J Phycol 38:564–571
Hanyuda T, Kawai H (2018) Genetic examination of the type specimen of Ulva australis suggests that it was introduced to Australia. Phycological Res 66:238–241
Hanyuda T, Hansen GI, Kawai H (2018) Genetic identification of macroalgal species on Japanese tsunami marine debris and genetic comparisons with their wild populations. Mar Pollut Bull 132:74–81
Hawes NA, Taylor DI, Schiel DR (2017) Transport of drifting fucoid algae: nearshore transport and potential for long distance dispersal. J Exp Mar Bio Ecol 490:34–41
Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5-9
Kagawa O, Chiba S (2019) Snails wearing green heatproof suits: the benefits of algae growing on the shells of an intertidal gastropod. J Zool 307:256–263
Kagawa O, Uchida S, Yamazaki D, Osawa Y, Ito S, Chiba S, The green-costumed snail’s citizen researchers (2020) Citizen science via social media revealed conditions of symbiosis between a marine gastropod and an epibiotic alga. Sci Rep 10:19647
Kagawa O, Hirota SK, Saito T, Uchida S, Watanabe H, Miyazoe R, Yamaguchi T, Matsuno T, Araki K, Wakasugi H, Suzuki S, Kobayashi G, Miyazaki H, Suyama Y, Hanyuda T, Chiba S (2023) Host-shift speciation proceeded with gene flow in algae covering shells. Am Nat 202:721–732
Kalyaanamoorthy S, Minh BQ, Wong TKF, Haeseler AV, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589
Krasnov BR, Poulin R, Shenbrot GI, Mouillot D, Khokhlova IS (2005) Host specificity and geographic range in haematophagous ectoparasites. Oikos 108:449–456
Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116
Lischke CE (1869) Diagnosen neuer Meeres-Konchylien von Japan. Malakozoologische Blätter. 16: 105-109.
Matsuyama K, Aruga Y, Tanaka J (1999) Ecological and morphological studies of Cladophora conchopheria Sakai (Ulvophyceae, Cladophoraceae). J Jap Bot 74:136–141
Meseguer AS, Coeur d’acier A, Genson G, Jousselin E (2015) Unravelling the historical biogeography and diversification dynamics of a highly diverse conifer-feeding aphid genus. J Biogeogr 42:1482–1492
Mestre A, Poulin R, Hortal J (2020) A niche perspective on the range expansion of symbionts. Biol Rev Camb Philos Soc 95:491–516
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, Haeseler AV, Lanfear R (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 37:1530–1534
Miura O, Torchin ME, Bermingham E, Jacobs DK, Hechinger RF (2012) Flying shells: historical dispersal of marine snails across Central America. Proc Biol Sci 279:1061–1067
Nakano T, Takahashi K, Ozawa T (2007) Description of an endangered new species of Lunella (Gastropoda: Turbinidae) from the Ogasawara Islands, Japan. Venus 66:1–10
Okutani T (2017) Marine mollusks in Japan (the, 2nd edn). Tokai University Press, Japan
Poulin R, Krasnov BR, Mouillot D, Thieltges DW (2011) The comparative ecology and biogeography of parasites. Philos Trans R Soc Lond B Biol Sci 366:2379–2390
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904
Récluz C (1853) Description de coquilles nouvelles (Genres Turbo, Triton et Mitra). Journal de Conchyliologie. 4: 245-249.
Reeve LA (1846-1847) Monograph of the genus Buccinum. In: Conchologia Iconica, or, illustrations of the shells of molluscous animals, vol. 3, pl. 1-14 and unpaginated text. L. Reeve & Co., London.
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542
Saito T, Tatani M, Odaya Y, Chiba S (2023) Direct evidence for intercontinental dispersal of a snail via a bird. Ecography 10:e06771
Sakai Y (1964) The species of Cladophora from Japan and its vicinity. Scientific papers of the Institute of Algological Research, Faculty of Science, Hokkaido University, vol 5, pp 1–104
Sowerby GB II (1855) Monograph of the genus Cerithium, Adanson. In Sowerby GB II (ed.), Thesaurus conchyliorum, or monographs of genera of shells. Vol. 2 (16): 847–899. London, privately published.
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577
Tanabe AS (2008) Phylogears version 2–2.0.2016.09.06. http://www.fifthdimension.jp. Accessed 1 Apr 2024
Tanabe AS (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol Ecol Resour 11:914–921
Tonk L, Sampayo EM, Weeks S, Magno-Canto M, Hoegh-Guldberg O (2013) Host-specific interactions with environmental factors shape the distribution of symbiodinium across the Great Barrier Reef. PLoS ONE 8:e68533
van den Hoek C (1987) The possible significance of long-range dispersal for the biogeography of seaweeds. Helgoländer Meeresuntersuchungen 41:261–272
Van Oppen MJ, Olsen JL, Stam WT (1993) Evidence for independent acquisition of group I introns in green algae. Mol Biol Evol 10:1317–1326
Villesen P (2007) FaBox: an online toolbox for fasta sequences. Mol Ecol Notes 7:965–968
Wang XY, Sakai Y (1986) Life history of Cladohora opaca and Cl. conchopheria (Chlorophyta). The Japanese Journal of Phycology 34:209–215
Wang J, Tsang LM, Dong Y-W (2015) Causations of phylogeographic barrier of some rocky shore species along the Chinese coastline. BMC Evol Biol 15:114
Warburton EM, Kohler SL, Vonhof MJ (2016) Patterns of parasite community dissimilarity: the significant role of land use and lack of distance-decay in a bat-helminth system. Oikos 125:374–385
Whittaker RJ, Fernández-Palacios JM, Matthews TJ, Borregaard MK, Triantis KA (2017) Island biogeography: taking the long view of nature’s laboratories. Science 357:eaam8326
Williams S, Apte D, Ozawa T, Kaligis F (2011) Speciation and dispersal along continental coastlines and island arcs in the Indo-West Pacific turbinid gastropod genus Lunella. Evolution 65:1752–1771
Yamada M, Wada K, Ohno T (2003) Observations on the alga Cladophora conchopheria on shells of the intertidal gastropod Turbo coronatus coreensis. Benthos Res 58:1–6
Acknowledgements
We thank Shun Ito, Takahiro Hirano, Takumi Saito, and Masanori Tatani for the research advice and support. We would like to thank Inaba Laboratory at the Shimoda Marine Research Center, University of Tsukuba, and Chiba Laboratory at Tohoku University for providing us with the support. We also gratefully acknowledge the editors of Marine Biodiversity and the anonymous reviewers.
Funding
This study was financially supported by a Sasakawa Scientific Research Grant (2020–5046) from the Japan Science Society, and JSPS KAKENHI (JP17H04611, JP20J14469, JP22J00433 and JP21K15161).
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All applicable international, national, and/or institutional guidelines for the use of animals were followed by the authors.
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All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable. The study is compliant with CBD and Nagoya protocols.
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The sequence data obtained are registered and available in GenBank of NCBI (accession numbers; OR844530- OR844531 and OR863900-OR863902).
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OK and DY conceived this study. DY and DVT carried out field surveys and purchased the gastropods. TH presented the molecular identification method. SC provided the experimental environment, including reagents and equipment. OK conducted the morphological observations, genetic experiments, and genetic analyses and wrote the first draft of this paper. All authors revised the paper.
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Kagawa, O., Van Tu, D., Hanyuda, T. et al. Southernmost record of an epibiotic alga Pseudocladophora conchopheria (Sakai) Boedeker & Leliaert (Cladophorales, Ulvophyceae) with insights into the geographical dispersal and host utilization. Mar. Biodivers. 54, 47 (2024). https://doi.org/10.1007/s12526-024-01437-5
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DOI: https://doi.org/10.1007/s12526-024-01437-5