Skip to main content
SpringerLink
Log in

Genetic analysis of dicyemid infrapopulations suggests sexual reproduction and host colonization by multiple individuals is common

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

Dicyemida is a group of small-bodied marine parasites infecting cephalopods with many unknown life history details, such as their population structure and diversity, and their relation to sexual and asexual reproductive stages. To reveal (infra)population structure of Dicyema moschatum Whitman, 1883 in its host (Eledone moschata Lamarck, 1798), we isolated microsatellite sequences from a draft genome of D. moschatum and tested the loci for amplification success and genetic diversity. Eight microsatellite loci were selected for an analysis of D. moschatum populations from several octopus individuals sampled at two Mediterranean localities. The majority of microsatellite alleles were shared across the studied range, but several private alleles were also identified. Analysis of population structure identified two to four genetic clusters, mostly concordant with the geographic origin of the samples. Allelic patterns seen in individual dicyemid genotypes revealed that although dicyemids inside one host individual show low genetic variance, they do not represent genetically identical clones. These results suggest that infection is established by several dicyemid larvae within the lifetime of the host and sexual reproduction of dicyemids occurs inside the host.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Anderson, T. J. C., Haubold, B., Williams, J. T., Estrada-Franco, J. G., Richardson, L., Mollinedo, R., Bockarie, M., Mokili, J., Mharakurwa, S., French, N., Whitworth, J., Velez, I. D., Brockman, A. H., Nosten, F., Ferreira, M. U., & Day, K. P. (2000). Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Molecular Biology and Evolution, 17(10), 1467–1482. https://doi.org/10.1093/oxfordjournals.molbev.a026247.

    Article  CAS  PubMed  Google Scholar 

  • Baldwin, R. E., Rew, M. B., Johansson, M. L., Banks, M. A., & Jacobson, K. C. (2011). Population structure of three species of Anisakis nematodes recovered from Pacific Sardines (Sardinops sagax) distributed throughout the California Current System. Journal of Parasitology, 97(4), 545–554. https://doi.org/10.1645/ge-2690.1.

    Article  PubMed  Google Scholar 

  • Bosc, L.A.G. (1817). Pisces accounts. Tome VII. Nouveau Dictionnaire d’Histoire Naturelle, Nouvelle Édition, Paris

  • Catalano, S. R., Whittington, I. D., Donnellan, S. C., & Gillanders, B. M. (2013). Using the giant Australian cuttlefish (Sepia apama) mass breeding aggregation to explore the life cycle of dicyemid parasites. Acta Parasitologica, 58(4), 599–602. https://doi.org/10.2478/s11686-013-0186-y.

    Article  PubMed  Google Scholar 

  • Criscione, C. D., Poulin, R., & Blouin, M. S. (2005). Molecular ecology of parasites: Elucidating ecological and microevolutionary processes. Molecular Ecology, 14(8), 2247–2257. https://doi.org/10.1111/j.1365-294X.2005.02587.x.

    Article  CAS  PubMed  Google Scholar 

  • Criscione, C. D., & Blouin, M. S. (2006). Minimal selfing, few clones, and no among-host genetic structure in a hermaphroditic parasite with asexual larval propagation. Evolution, 60(3), 553–562. https://doi.org/10.1554/05-421.1.

    Article  CAS  PubMed  Google Scholar 

  • Criscione, C. D., Vilas, R., Paniagua, E., & Blouin, M. S. (2011). More than meets the eye: Detecting cryptic microgeographic population structure in a parasite with a complex life cycle. Molecular Ecology, 20(12), 2510–2524. https://doi.org/10.1111/j.1365-294X.2011.05113.x.

    Article  PubMed  Google Scholar 

  • Drábková, M., Jachníková, N., Tyml, T., Sehadová, H., Ditrich, O., Myšková, E., Hypša, V., & Štefka, J. (2019). Population co-divergence in common cuttlefish (Sepia officinalis) and its dicyemid parasite in the Mediterranean Sea. Scientific Reports, 9(1), 1–12. https://doi.org/10.1038/s41598-019-50555-9.

    Article  CAS  Google Scholar 

  • Dunn, A. M., & Smith, J. E. (2001). Microsporidian life cycles and diversity: The relationship between virulence and transmission. Microbes and Infection, 3(5), 381–388.

    Article  CAS  PubMed  Google Scholar 

  • Earl, D. A., & von Holdt, B. M. (2012). STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4(2), 359–361. https://doi.org/10.1007/s12686-011-9548-7.

    Article  Google Scholar 

  • Eshragh, R., & Leander, B. S. (2014). Molecular contributions to species boundaries in dicyemid parasites from eastern Pacific cephalopods. Marine Biology Research, 11(November), 414–422. https://doi.org/10.1080/17451000.2014.943241.

    Article  Google Scholar 

  • Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14(8), 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L. G., Laval, & Schneider, S. (2005). Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.

    CAS  Google Scholar 

  • Falush, D., Stephens, M., & Pritchard, J. K. (2003). Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics, 164, 1567–1587.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3(5), 294–299.

    CAS  PubMed  Google Scholar 

  • Furuya, H., Hochberg, F. G., & Tsuneki, K. (2003). Reproductive traits in dicyemids. Marine Biology, 142(July 2002), 693–706. https://doi.org/10.1007/s00227-002-0991-6.

    Article  Google Scholar 

  • Furuya, H., & Tsuneki, K. (2003). Biology of dicyemid mesozoans. Zoological Science, 20(5), 519–532. https://doi.org/10.2108/zsj.20.519.

    Article  PubMed  Google Scholar 

  • Gray, J. E. (1849). Catalogue of the Mollusca in the collection of the British Museum I: Cephalopoda antepedia. London: British Museum. https://doi.org/10.5962/bhl.title.132909.

    Book  Google Scholar 

  • Hafner, M. S., Sudman, P. D., Villablanca, F. X., Spradling, T. A., Demastes, J. W., & Nadler, S. A. (1994). Disparate rates of molecular evolution in cospeciating hosts and parasites. Science, 265(5175), 1087–1090.

    Article  CAS  PubMed  Google Scholar 

  • Hertig, M. (1936). The Rickettsia, Wolbachia pipientis (gen. et sp.n.) and associated inclusions of the mosquito, Culex pipiens. Parasitology, 28(4), 453–486. https://doi.org/10.1017/S0031182000022666.

    Article  Google Scholar 

  • Hochberg, F. G. (1990). “Diseases of mollusca: cephalopoda: Diseases caused by protistans and metazoans,” in Diseases of marine animals, Vol. III, Cephalopoda to Urochordata, ed. O. Kinne (Hamburg: Biologisches Anstalt Helgoland), 47–227.

  • Hubisz, M. J., Falush, D., Stephens, M., & Pritchard, J. K. (2009). Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources, 9(5), 1322–1332. https://doi.org/10.1111/j.1755-0998.2009.02591.x.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012). Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kopelman, N. M., Mayzel, J., Jakobsson, M., Rosenberg, N. A., & Mayrose, I. (2015). CLUMPAK: A program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources, 15(5), 1179–1191. https://doi.org/10.1111/1755-0998.12387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamarck, J. B. (1798). Extrait d’un memoire sur les genres de la sèche, der Calmar et du Poulpe, vulgairement nomenies Polypes de mer. Bulletin de la Société philomathique de Paris, 2, 129–131.

    Google Scholar 

  • Lapan, E. A., & Morowitz, H. J. (1975). The dicyemid mesozoa as an integrated system for morphogenetic studies. I. Description isolation and maintenance. Journal of Experimental Zoology, 193(2), 147–159. https://doi.org/10.1002/jez.1401930204.

    Article  CAS  PubMed  Google Scholar 

  • Leach, W. E. (1817). Synopsis of the orders, families and genera of the class Cephalopoda. The Zoological Miscellany; being descriptions of new or interesting animals, 3(30), 137–141 available online at http://biodiversitylibrary.org/page/28687004.

  • Lipsitch, M., Nowak, M. A., Ebert, D., & May, R. M. (1995). The population dynamics of vertically and horizontally transmitted parasites. Proceedings of the Royal Society B: Biological Sciences, 260(1359), 321–327. https://doi.org/10.1098/rspb.1995.0099.

    Article  CAS  PubMed  Google Scholar 

  • Lühe, M. (1901). Ueber Hemiuriden. (Ein Beitrag zur Systematik der digenetischen Trematoden). Zoologischer Anzeiger, 24, 394–403–473–488.

    Google Scholar 

  • Marchiafava, E., & Celli, A. (1885). Nouve ricerche sulla infezione malarica. Archivo per le Scienze Mediche, Torino, 9, 311–340.

    Google Scholar 

  • McIntosh, A. (1939). A new allocreadiid trematode, Podocotyle shawi n. sp. from the silver salmon. Journal of the Washington Academy of Sciences, 29, 379–381.

    Google Scholar 

  • Meglécz, E., Pech, N., Gilles, A., Dubut, V., Hingamp, P., Trilles, A., Grenier, R., & Martin, J. F. (2014). QDD version 3.1: A user friendly computer program for microsatellite selection and primer design revisited: Experimental validation of variables determining genotyping success rate. Molecular Ecology Resources, 14(6), 1302–1313. https://doi.org/10.1111/1755-0998.12271.

    Article  CAS  PubMed  Google Scholar 

  • Nouvel, H. (1947). Les dicyémides 1er partie: systématique, générations vermiformes, infusorigène et sexualité. Archives de Biologie, 58, 59–214.

    CAS  PubMed  Google Scholar 

  • Peakall, R., & Smouse, P. (2006). GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6(1), 288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x.

    Article  Google Scholar 

  • Peakall, R., & Smouse, P. E. (2012). GenALEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics, 28(19), 2537–2539. https://doi.org/10.1093/bioinformatics/bts460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945–959.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salem, H., Onchuru, T. O., Bauer, E., & Kaltenpoth, M. (2015). Symbiont transmission entails the risk of parasite infection. Biology Letters, 11(12), 20150840. https://doi.org/10.1098/rsbl.2015.0840.

    Article  PubMed  PubMed Central  Google Scholar 

  • Souidenne, D., Florent, I., Dellinger, M., Romdhane, M. S., Grellier, P., & Furuya, H. (2016). Redescription of Dicyemennea eledones (Wagener, 1857) (Phylum Dicyemida) from Eledone cirrhosa (Lamarck, 1798) (Mollusca: Cephalopoda: Octopoda). Systematic Parasitology, 93(9), 905–915. https://doi.org/10.1007/s11230-016-9659-3.

    Article  PubMed  Google Scholar 

  • Sprehn, C. G., Blum, M. J., Quinn, T. P., & Heins, D. C. (2015). Landscape genetics of Schistocephalus solidus parasites in threespine stickleback (Gasterosteus aculeatus) from Alaska. PLoS One, 10(4), 1–17. https://doi.org/10.1371/journal.pone.0122307.

    Article  CAS  Google Scholar 

  • Štefka, J., Hypša, V., & Scholz, T. (2009). Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: Microsatellite study of Ligula intestinalis (Cestoda). Molecular Ecology, 18(6), 1187–1206. https://doi.org/10.1111/j.1365-294X.2008.04074.x.

    Article  CAS  PubMed  Google Scholar 

  • Stunkard, H. W. (1954). The life history and systematic relations of the mesozoa. The Quarterly Review of Biology, 29(3), 230–244.

    Article  CAS  PubMed  Google Scholar 

  • Taberlet, P., Griffin, S., Goossens, B., Questiau, S., Manceau, V., Escaravage, N., Waits, L. P., & Bouvet, J. (1996). Reliable genotyping from small Dna. Nucleic Acids Research, 24(16), 3189–3194 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC146079/pdf/243189.pdf.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor, M. J., & Hoerauf, A. (1999). Wolbachia bacteria of filarial nematodes. Parasitology Today, 15(11), 437–442.

    Article  CAS  PubMed  Google Scholar 

  • van Beneden, M. E. (1876). Recherches sur le Dicyemides, survivants actuels d’un embranchement des Mésozoaires. Bulletins de l’Académie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique, 41, 1160–1205.

    Google Scholar 

  • von Kölliker, A. (1849). Ueber Dicyema paradoxum, den Schmarotzer der Venenanhänge der Cephalopoden [in German]. Berichte von der Königlichen Zootomischen Anstalt zu Wurzburg, 59–66.

  • Whitman, C. O. (1883). A contribution to the embryology, life history, and classification of the dicyemids. Mittheilungen aus der Zoologischen Station zu Neapel, 4, 1–89.

    Google Scholar 

  • Zhu, Y., Liu, H. Y., Yang, H. Q., Li, Y. D., & Zhang, H. M. (2017). Factors affecting genotyping success in giant panda fecal samples. PeerJ, 2017(5), 1–14. https://doi.org/10.7717/peerj.3358.

    Article  CAS  Google Scholar 

  • Zotta, G. (1912). Sur un flagelle du type Herpetomonas chez Pyrrhocoris apterus. Annales Scientifiques de l’Université de Jassy, 7, 211–223.

    Google Scholar 

Download references

Acknowledgements

The authors are grateful to colleagues who helped with field sampling (mainly Tomáš Tyml) and also to colleagues abroad, namely Graziano Fiorito and Giovanna Ponte, who allowed us to use their facilities at Stazione Zoologica Naples.

Availability of data and material

Dataset produced in this study is available on the following link https://drive.google.com/file/d/1gLuZiwtriHedxyNkIv8bjmWmLBAUUTTF/view?usp=sharing.

Sequences produced in this study are available in Genbank under accession numbers MT703888-MT703900.

Code availability

Not applicable.

Funding

This work was financially supported by grants from the Czech Science Foundation (GACR project nos. 15-08717S and 19-28399X).

Author information

Authors and Affiliations

  1. Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic

    Marie Drábková, Tereza Flegrová, Eva Myšková, Václav Hypša & Jan Štefka

  2. Institute of Parasitology, Biology Centre, CAS, v.v.i., České Budějovice, Czech Republic

    Marie Drábková, Tereza Flegrová & Jan Štefka

Authors
  1. Marie Drábková
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tereza Flegrová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eva Myšková
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Václav Hypša
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jan Štefka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marie Drábková.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(PDF 322 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Drábková, M., Flegrová, T., Myšková, E. et al. Genetic analysis of dicyemid infrapopulations suggests sexual reproduction and host colonization by multiple individuals is common. Org Divers Evol 21, 437–446 (2021). https://doi.org/10.1007/s13127-021-00493-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-021-00493-0

Keywords

Search

Navigation