Abstract
Parasites exhibit high diversity in various ecosystems. Habitat selection has played an important role in the diversification of parasites by facilitating intra-host speciation and repeated shifts to a single host species by multiple parasite taxa. In this study, we investigated habitat selection in two gastropod species, Melanella cf. acicula and Peasistilifer nitidula (Caenogastropoda: Vanikoroidea: Eulimidae), that are parasitic on the black sea cucumber Holothuria atra in southwestern Japan. The number and position of parasites were observed for 335 hosts; in total, 89 individuals of M. cf. acicula and 194 of P. nitidula were found. Melanella cf. acicula exhibited strong habitat selection, with 70 individuals (78.7%) attached around the host’s mouth, whereas P. nitidula had relatively low infection site specificity. This suggests that the two parasite species have different feeding habits. Molecular phylogenetic analysis verified their non-monophyletic relationship, indicating that they likely made independent host shifts to H. atra. The observed difference in habitat preference, as well as the abundance of suitable habitats, may have contributed to the repeated host shifts and sympatric distribution of M. cf. acicula and P. nitidula. Our phylogenetic analysis also revealed the non-monophyly of eulimids parasitising holothuroids, as in asteroid and ophiuroid parasitic taxa.
Similar content being viewed by others
Data availability
The datasets generated and analysed during the current study are available from the corresponding author on reasonable request.
References
Bouchet, P. & J. Lützen, 1980. Deux Gastéropodes parasites d’ne Holothurie Élasipode. Bulletin du Muséum National d’Histoire Naturelle, Paris 4(2): 59–75.
Castresana, J., 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334.
Crossland, M. R., J. D. Collins & R. A. Alford, 1993. Host selection and distribution of Hypermastus placentae (Eulimidae), an ectoparasitic gastropod on the sand dollar Arachnoides placenta (Echinoidea). Australian Journal of Marine and Freshwater Research 44: 835–844. https://doi.org/10.1071/MF9930835.
Darriba, D., G. L. Taboada, R. Doallo & D. Posada, 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. https://doi.org/10.1038/nmeth.2109.
Dgebuadze, P. Y., V. P. Voronin, E. S. Mekhova, S. N. Pekkoeva & S. A. Murzina, 2022. First data on lipids and fatty acids composition in the tropical parasitic system between molluscs and echinoderms. Symbiosis 87: 281–291. https://doi.org/10.1007/s13199-022-00876-7
Emelianov, I., 2007. How adaptive is parasite species diversity? International Journal for Parasitology 37: 851–860. https://doi.org/10.1016/j.ijpara.2007.04.010.
Euzet, L. & C. Combes, 1998. The selection of habitats among the monogenea. International Journal for Parasitology 28: 1645–1652. https://doi.org/10.1016/S0020-7519(98)00062-9.
Folmer, O., M. Black, W. Hoeh, R. Luts & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.
Goto, R., 2010. First record of the genus Megadenus Rosén, 1910 (Gastropoda: Eulimidae), endoparasites of sea cucumbers, from Japan. Venus 69: 80–83. https://doi.org/10.18941/venus.69.1-2_80.
Goto, R., T. Takano, D. J. Eernisse, M. Kato & Y. Kano, 2021. Snails riding mantis shrimps: ectoparasites evolved from ancestors living as commensals on the host’s burrow wall. Molecular Phylogenetics and Evolution 163: 107122. https://doi.org/10.1016/j.ympev.2021.107122.
Hamamoto, K., T. Soliman, A. Poliseno, I. Fernandez-Silva & J. D. Reimer, 2021. Higher genetic diversity of the common sea cucumber Holothuria (Halodeima) atra in marine protected areas of the central and southern Ryukyu Islands. Frontiers in Conservation Science 2: 736633. https://doi.org/10.3389/fcosc.2021.736633.
Hay, E. M., R. Poulin & F. Jorge, 2020. Macroevolutionary dynamics of parasite diversification: a reality check. Journal of Evolutionary Biology 33: 1758–1769. https://doi.org/10.1111/jeb.13714.
Hori, S. & M. Matsuda, 2017. Family Eulimidae. In Okutani, T. (ed), Marine Mollusks in Japan, the Second Edition. Tokai University Press, Hiratsuka: 142–151, 823–832.
Hothorn, T., K. Hornik, M. A. van de Wiel & A. Zeileis, 2008. Implementing a class of permutation tests: the coin package. Journal of Statistical Software 28: 1–23. https://doi.org/10.18637/jss.v028.i08.
Huyse, T., R. Poulin & A. Théron, 2005. Speciation in parasites: a population genetics approach. Trends in Parasitology 21: 469–475. https://doi.org/10.1016/j.pt.2005.08.009.
Johnson, K. P., S. M. Shreve & V. S. Smith, 2012. Repeated adaptive divergence of microhabitat specialization in avian feather lice. BMC Biology 10: 52. https://doi.org/10.1186/1741-7007-10-52.
Kano, Y., 2008. Vetigastropod phylogeny and a new concept of Seguenzioidea: independent evolution of copulatory organs in the deep-sea habitats. Zoologica Scripta 37: 1–21. https://doi.org/10.1111/j.1463-6409.2007.00316.x.
Katoh, K. & D. M. Standley, 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010.
Littlewood, D. T. J., M. Curini-Galletti & A. Herniou, 2000. The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution 16: 449–466. https://doi.org/10.1006/mpev.2000.0802.
Lockyer, A. E., P. D. Olson, P. Østergaard, D. Rollinson, D. A. Johnston, S. W. Attwood, V. R. Southgate, P. Horak, S. D. Snyder, T. H. Le, T. Agatsuma, D. P. McManus, A. C. Carmichael, S. Naem & D. T. J. Littlewood, 2003. The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126: 203–224. https://doi.org/10.1017/S0031182002002792.
Matsuda, H., T. Hamano & K. Nagasawa, 2010. Spatial distribution patterns of the parasitic gastropod Hypermastus tokunagai (Eulimidae) in populations of its echinoid host Scaphechinus mirabilis (Scutellidae). Venus 69: 59–70. https://doi.org/10.18941/venus.69.1-2_59.
Matsuda, H., T. Hamano & K. Nagasawa, 2013. Growth and reproductive cycle of Hypermastus tokunagai (Caenogastropoda: Eulimidae), an ectoparasite of the sand dollar Scaphechinus mirabilis (Clypeasteroida: Scutellidae) in the Seto Inland Sea, Japan. Journal of the Marine Biological Association of the United Kingdom 93: 1041–1051. https://doi.org/10.1017/S0025315412001269.
Mladineo, I., N. J. Bott, B. F. Nowak & B. A. Block, 2010. Multilocus phylogenetic analyses reveal that habitat selection drives the speciation of Didymozoidae (Digenea) parasitizing Pacific and Atlantic bluefin tunas. Parasitology 137: 1013–1025. https://doi.org/10.1017/S0031182009991703.
Morton, B., 1976. Selective site segregation in Balcis shaplandi and Mucronalia fulvescens (Mollusca: Gastropoda: Aglossa) parasitic upon Archaster typicus (Echinodermata: Asteroidea). Malacological Review 9: 55–61.
Morton, B., 1979. The population dynamics and expression of sexuality in Balcis shaplandi and Mucronalia fulvescens (Mollusca: Gastropoda: Aglossa) parasitic upon Archaster typicus (Echinodermata: Asteroidea). Malacologia 18: 327–346.
Palumbi, S., A. Martin, S. Romano, W. O. McMillan, L. Stice & G. Grabowski, 1991. The Simple Fool’s Guide to PCR, Version 2.0. Department of Zoology and Kewalo Marine Laboratory, University of Hawaii, Honolulu.
Purcell, S. W., Y. Samyn & C. Conand, 2012. Commercially Important Sea Cucumbers of the World, Food and Agriculture Organization of the United Nations, Rome.
Rahmouni, C., M. P. M. Vanhove, S. Koblmüller & A. Šimková, 2022. Molecular phylogeny and speciation patterns in host-specific monogeneans (Cichlidogyrus, Dactylogyridae) parasitizing cichlid fishes (Cichliformes, Cichlidae) in Lake Tanganyika. International Journal for Parasitology 52: 359–375. https://doi.org/10.1016/j.ijpara.2021.12.004.
R Core Team, 2022. R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna.
Ronquist, F. & J. P. Huelsenbeck, 2003. MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. https://doi.org/10.1093/bioinformatics/btg180.
Ronquist, F., M. Teslenko, P. van der Mark, D. L. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M. A. Suchard & J. P. Huelsenbeck, 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029.
Seidlová, L., M. Benovics & A. Šimková, 2022. Gill monogeneans of neotropical cichlid fish: diversity, phylogenetic relationships, and host-parasite cophylogenetic associations. International Journal for Parasitology 52: 603–615. https://doi.org/10.1016/j.ijpara.2022.05.001.
Šimková, A., S. Morand, E. Jobet, M. Gelnar & O. Verneau, 2004. Molecular phylogeny of congeneric monogenean parasites (Dactylogyrus): a case of intrahost speciation. Evolution 58: 1001–1018. https://doi.org/10.1111/j.0014-3820.2004.tb00434.x.
Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313. https://doi.org/10.1093/bioinformatics/btu033.
Tamura, K., G. Stecher & S. Kumar, 2021. MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38: 3022–3027. https://doi.org/10.1093/molbev/msab120.
Takano, T. & Y. Kano, 2014. Molecular phylogenetic investigations of the relationships of the echinoderm-parasite family Eulimidae within Hypsogastropoda (Mollusca). Molecular Phylogenetics and Evolution 79: 258–269. https://doi.org/10.1016/j.ympev.2014.06.021.
Takano, T., A. Warén & Y. Kano, 2017. Megadenus atrae n. sp., an endoparasitic eulimid gastropod (Mollusca) from the black sea cucumber Holothuria atra Jaeger (Aspidochirotida: Holothuriidae) in the Indo-West Pacific. Systematic Parasitology 94: 699–709. https://doi.org/10.1007/s11230-017-9731-7.
Takano, T. & R. Goto, 2021. Molecular and morphological systematics of the crinoid-parasitic snail genus Goodingia (Mollusca: Caenogastropoda: Eulimidae) with new insights into intrafamilial phylogenetic relationships. Marine Biodiversity 51: 5. https://doi.org/10.1007/s12526-020-01141-0.
Takano, T., Y. Kano, T. Mogi & M. Okanishi, 2023. Fusceulimoides kohtsukai gen. et sp. nov., a minute eulimid gastropod parasitic on the little brittle star Ophiactis savignyi in central Japan. Zoological Science 40: 64–69. https://doi.org/10.2108/zs220050.
Warén, A., 1980. Descriptions of new taxa of Eulimidae (Mollusca, Prosobranchia), with notes on some previously described genera. Zoologica Scripta 9: 283–306. https://doi.org/10.1111/j.1463-6409.1980.tb00668.x.
Warén, A., 1981. Revision of the genera Apicalia A. Adams and Stilapex Iredale and description of two new genera (Mollusca: Prosobranchia: Eulimidae). Zoologica Scripta 10: 133–154. https://doi.org/10.1111/j.1463-6409.1981.tb00491.x.
Warén, A., 1983. A generic revision of the family Eulimidae (Gastropoda, Prosobranchia). Journal of Molluscan Studies, Supplement 13: 1–96. https://doi.org/10.1093/mollus/49.Supplement_13.1.
Weinstein, S. B. & A. M. Kuris, 2016. Independent origins of parasitism in Animalia. Biology Letters 12: 20160324. https://doi.org/10.1098/rsbl.2016.0324.
Will, I., 2009. Host preference, detection, and dependence: the ectoparasitic gastropods Melanella acicula and Peasistilifer nitidula (Eulimidae) on holothurian hosts. UC Berkeley Student Research Papers, Berkeley. Accessed online on 4 July 2023 at https://escholarship.org/uc/item/1ft6r4hf.
Williams, S. T., D. G. Reid & D. T. J. Littlewood, 2003. A molecular phylogeny of the Littorininae (Gastropoda: Littorinidae): unequal evolutionary rates, morphological parallelism, and biogeography of the Southern Ocean. Molecular Phylogenetics and Evolution 28: 60–86. https://doi.org/10.1016/S1055-7903(03)00038-1.
Windsor, D. A., 1998. Most of the species on Earth are parasites. International Journal for Parasitology 28: 1939–1941. https://doi.org/10.1016/S0020-7519(98)00153-2.
WoRMS, 2023. Melanella acicula (A. Gould, 1849). Accessed online on 4 July 2023 at https://www.marinespecies.org/aphia.php?p=taxdetails&id=537004.
Acknowledgements
We thank H. Fukumori (Tohoku University) for his help with fieldwork. Invaluable comments were provided by two anonymous reviewers for the improvement of the manuscript.
Funding
This work was supported by a grant from the Research Institute of Marine Invertebrates (KO2022-05) and by a JSPS KAKENHI grant (23K14257) to TT.
Author information
Authors and Affiliations
Contributions
TT conducted field surveys and molecular analysis and prepared the manuscript. MH and KI conducted field surveys, revised drafts, and gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare none.
Additional information
Handling editor: Manuel Lopes-Lima
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Takano, T., Hasegawa-Takano, M. & Inoue, K. Habitat selection in two species of Eulimidae (Mollusca: Gastropoda) parasitic on the black sea cucumber Holothuria atra. Hydrobiologia 851, 1779–1788 (2024). https://doi.org/10.1007/s10750-023-05417-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-023-05417-x