Skip to main content
SpringerLink
Log in

Cryptic speciation in the cosmopolitan Epiphanes senta complex (Monogononta, Rotifera) with the description of new species

  • Advances in Rotifer Research
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Many rotifers are considered to be cosmopolitan species including Epiphanes senta, which has been reported from all continents including Antarctica. To determine the potential for cryptic speciation in this species, we examined morphology, mating behavior and genetic divergence in three populations: (1) a tropical alpine lake on Mauna Kea (HI, USA), (2) temporary rock pools of the Chihuahuan Desert (TX, USA), and (3) floodplain habitats of the Oder River (Germany). Morphological differences among these populations are restricted to the surface structure of diapausing eggs and the shape of the rami. In crossmating experiments, German males never fertilized females from the Texan population. Texan males mated with hatching females from the German population. However, juvenile mortality among these fertilized females reached 40% and was significantly higher than juvenile mortality after intrapopulational mating (2%). Surviving females did not produce viable diapausing eggs. Hawaiian males readily mated with newborn Texan females, which produced viable offspring. They also copulated with females from the German population, but these females never produced diapausing eggs. Genetic distance among the three populations was considerable, ranging from 10.9 to 12.5% for 648 bp of the mitochondrial cox1 gene. Morphological, reproductive, and genetic differentiation among the studied populations demonstrates E. senta is actually a species complex. Three new species within the E. senta species complex are described.

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

  • Avise, J. C. & D. E. Walker, 1999. Species realities and numbers in sexual invertebrates: Perspectives from an asexually transmitted genome. Proceedings of the National Academy of Sciences of the United States of America 96: 992–995.

    Article  PubMed  CAS  Google Scholar 

  • Ciros-Pérez, J., A. Gómez & M. Serra, 2001a. On the taxonomy of three sympatric sibling species of the Brachionus plicatilis (Rotifera) complex from Spain, with the description of B. ibericus n.sp. Journal of Plankton Research 23: 1311–1328.

    Article  Google Scholar 

  • Ciros-Pérez, J., A. Gómez & M. Serra, 2001b. Resource competition between sympatric sibling rotifer species. Limnology and Oceanography 46: 1511–1523.

    Article  Google Scholar 

  • de Beauchamp, P., 1965. Classe des Rotifères. In Grassé, P. P. (ed.), Traité de Zoologie—Metazoaires, Vol. 4(3), Némathelminthes (Nématodes, Gordiacés), Rotifères, Gastrotriches, Kinorhynques. Masson, Paris, 1225–1379.

  • DeRidder, M. & H. Segers, 1997. Rotifera Monogononta in six zoogeographical regions after publications between 1960–1992. In Van Goethem J. (ed) Studiedocumenten van het Koninklijk Belgisch Instituut voor Natuurwetenschappen). Koninklijk Belgisch Instituut voor Natuurweten-schappen, Brussels, 481 pp.

    Google Scholar 

  • Derry, A. M., P. D. N. Hebert & E. E. Prepas, 2003. Evolution of rotifers in saline and subsaline lakes: A molecular phylogenetic approach. Limnology and Oceanography 48: 675–685.

    Article  CAS  Google Scholar 

  • Dodson, S. I., A. K. Grishanin, K. Gross & G. A. Wyngaard, 2003. Morphological analysis of some cryptic species in the Acanthocyclops vernalis species complex from North America. Hydrobiologia 500: 131–143.

    Article  Google Scholar 

  • Ehrenberg, C. G., 1838. Die Infusionsthierchen als voll-kommene Organismen. Ein Blick in das tiefere organische Leben der Natur. L. Voβ, Leipzig, 547 pp.

  • Folmer, O., M. Black, W. Hoch, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit 1 from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.

    PubMed  CAS  Google Scholar 

  • Gilbert, J. J. & T. Schröder, 2003. The ciliate epibiont Epistylis pygmaeum: Selection for zooplankton hosts, reproduction and effect on two rotifers. Freshwater Biology 48: 878–893.

    Article  Google Scholar 

  • Gilbert, J. J. & E. J. Walsh, 2005. Brachionus calyciflorus is a species complex: Mating behavior and genetic differentiation among four geographically isolated strains. Hydrobiologia 546: 257–265.

    Article  CAS  Google Scholar 

  • Gómez, A., 2005. Molecular ecology of rotifers: From population differentiation to speciation. Hydrobiologia 546: 83–99.

    Article  CAS  Google Scholar 

  • Gómez, A., M. Serra, G. R. Carvalho & D. H. Lunt, 2002. Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera). Evolution 56: 1431–1444.

    PubMed  Google Scholar 

  • Hebert, P. D. N., S. Ratnasingham & J. R. de Waard, 2003. Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, Series B—Biology Letters 270: S96–S99.

    Article  CAS  Google Scholar 

  • Jersabek, C., 2003. Freshwater Rotifera (Monogononta) from Hawai’i—a preliminary checklist. In Evenhuis, N.L. & L.G. Eldredge (eds), Records of the Hawaii Biological Survey. (Bishop Museum Occasional Papers; 74). Bishop Museum Press, Honolulu, 46–72.

  • José De Paggi, S. & W. Koste, 1984. Checklist of the rotifers recorded from Antarctic and Subantarctic areas. Senckenbergiana Biologica 65: 169–178.

    Google Scholar 

  • Kim, K., A. A. Kotov & D. J. Taylor, 2006. Hormonal induction of undescribed males resolves cryptic species of cladocerans. Proceedings of the Royal Society of London, Series B 273: 141–147.

    Article  Google Scholar 

  • Knowlton, N., 2000. Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420: 73–90.

    Article  CAS  Google Scholar 

  • Koste, W., 1978. Rotatoria—die Rädertiere Mitteleuropas, 2nd ed., Vols. 1 and 2. Bornträger, Berlin, 673 pp.

  • Laws, E. A. & A. H. Woodcock, 1981. Hypereutrophication of an Hawaiian alpine lake. Pacific Science 35: 257–261.

    CAS  Google Scholar 

  • Lee, C. E., 2000. Global phylogeography of a cryptic copepod species complex and reproductive isolation between genetically proximate ‘populations’. Evolution 54: 2014–2027.

    Article  PubMed  CAS  Google Scholar 

  • Lee, C. E. & B. W. Frost, 2002. Morphological stasis in the Eurytemora affinis species complex (Copepoda: Temoridae). Hydrobiologia 480: 111–128.

    Article  CAS  Google Scholar 

  • Müller, O. F., 1773. Vermium terrestrium et fluviatilium, seu animalium infusorium, helminthicorum et testaceorum, non marinorum, succincta historia. Heineck et Faber, Havniae & Lipsiae, 135 pp.

  • Meier, R. & R. Willmann, 2000. The Hennigian species concept. In Wheeler Q. D. & R. Meier (eds) Species Concepts and Phylogenetic Theory: A Debate. Columbia University Press, New York, 30–43.

    Google Scholar 

  • Mishler, B. D. & E. C. Theriot, 2000. The phylogenetic species concept (sensu Mishler and Theriot): Monophyly, apomorphy, and phylogenetic species concepts. In Wheeler Q. D. & R. Meier (eds) Species Concepts and Phylogenetic Theory: A Debate. Columbia University Press, New York, 44–54.

    Google Scholar 

  • Ortells, R., A. Gómez & M. Serra, 2003. Coexistence of cryptic rotifer species: Ecological and genetic characterization of Brachionus plicatilis. Freshwater Biology 48: 2194–2202.

    Article  Google Scholar 

  • Padial, J. M. & I. De La Riva, 2006. Taxonomic inflation and the stability of species lists: The peril of ostrich’s behavior. Systematic Biology 55: 859–867.

    Article  PubMed  Google Scholar 

  • Penton, E. H., P. D. N. Hebert & T. J. Crease, 2004. Mitochrondrial DNA variation in North American populations of Daphnia obtusa: Continentalism or cryptic endemism? Molecular Ecology 13: 97–107.

    Article  PubMed  CAS  Google Scholar 

  • Plate, L., 1885. Beiträge zur Naturgeschichte der Rotatorien. Jenaische Zeitschrift für Naturwissenschaft 19 (N.F. 12): 1–120.

    Google Scholar 

  • Ruttner-Kolisko, A., 1974. Plankton rotifers. In Elster, H.J. & W. Ohle (eds), Die Binnengewässer, Vol. 26.1, supplement. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, 1–146.

  • SAS Institute, 2001. JMP Statistical Software Package, Version 4.0.4.. SAS Institute, Inc., Cary, NC.

    Google Scholar 

  • Schröder, T., 2001. Colonising strategies and diapause of planktonic rotifers (Monogononta, Rotifera) during aquatic and terrestrial phases in a floodplain (Lower Oder Valley, Germany). International Review of Hydrobiology 86: 635–660.

    Article  Google Scholar 

  • Schröder, T., 2003. Precopulatory mate guarding and mating behaviour in the rotifer Epiphanes senta (Monogononta, Rotifera). Proceedings of the Royal Society of London, Series B 270: 1965–1970.

    Article  Google Scholar 

  • Schröder, T., 2005. Diapause in monogonont rotifers. Hydrobiologia 546: 291–306.

    Article  Google Scholar 

  • Schröder, T. & J. J. Gilbert, 2004. Transgenerational plasticity for sexual reproduction and diapause in the life cycle of monogonont rotifers: Intraclonal, intraspecific and interspecific variation in the response to crowding. Functional Ecology 18: 458–466.

    Article  Google Scholar 

  • Stemberger, R. S., 1981. A general approach to the culture of planktonic rotifers. Canadian Journal of Fisheries and Aquatic Sciences 38: 721–724.

    Article  Google Scholar 

  • Swofford, D. L., 2002. PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods), Vers. 4.0. Sinauer Assoc., Sunderland, MA.

    Google Scholar 

  • Taylor, D. J. & P. D. N. Hebert, 1992. Daphnia galeata mendotae as a cryptic species complex with interspecific hybrids. Limnology and Oceanography 37: 658–665.

    Article  Google Scholar 

  • Thomas, J. A., J. J. Welch, M. Woolfit & L. Bromham, 2006. There is no universal molecular clock for invertebrates, but rate variation does not scale with body size. Proceedings of the National Academy of Sciences of the United States of America 103: 7366–7371.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, J. D., D. G. Higgins & T. J. Gibson, 1994. Clustal W: Improving the sensitivity of progressive multiple sequence alignment through weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680.

    Article  PubMed  CAS  Google Scholar 

  • Wallace, R. L. & T. W. Snell, 2001. Rotifera. In Thorp J. H. & A. P. Covich (eds) Ecology and Classification of North American Freshwater Invertebrates, 2nd ed. Academic Press, San Diego, 195–254.

    Google Scholar 

  • Weider, L. W., 1993. Niche breadth and life history variation in a hybrid Daphnia complex. Ecology 74: 935–943.

    Article  Google Scholar 

  • Wesenberg-Lund, C., 1930. Contributions to the Biology of the Rotifera, Vol. II. The Periodicity and Sexual Periods. A.F. Hoest & soen, Kopenhagen, 230 pp.

  • Wheeler, Q. D. & N. I. Platnick, 2000a. The phylogenetic species concept (sensu Wheeler and Platnick). In Wheeler Q. D. & R. Meier (eds) Species Concepts and Phylogenetic Theory: A Debate. Columbia University Press, New York, 55–69.

    Google Scholar 

  • Wheeler, Q. D. & N. I. Platnick, 2000b. A defense of the phylogenetic species concept (sensu Wheeler and Platnick). In Wheeler Q. D. & R. Meier (eds) Species Concepts and Phylogenetic Theory: A Debate. Columbia University Press, New York, 185–197.

    Google Scholar 

Download references

Acknowledgments

We thank the staff at Hueco Tanks State Historical Site (Permit #07-02), Jochen Beschnitt of the Lower Oder Valley National Park, and Betsy Gagne of the Department of Land and Natural Resources (Hawaii) for their cooperation and permission to sample. Christian Jersabek provided valuable information about the population in Hawaii. We thank Robert L. Wallace, Hendrik Segers and an anonymous reviewer for their comments which helped to improve the manuscript. This material is based upon work supported by the National Science Foundation under Grant No. 0516032 and No. 9628568 (E. Walsh) and by the Gallagher Fellowship (T. Schröder). The SEM facility at UTEP is funded by NSF DRM 0521650.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Texas at El Paso, 500 W. University Ave, El Paso, TX, 79968, USA

    Thomas Schröder & Elizabeth J. Walsh

  2. Academy of Natural Sciences in Philadelphia, 1900 Benjamin Franklin Parkway, Philadelphia, PA, 19103, USA

    Thomas Schröder

Authors
  1. Thomas Schröder
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elizabeth J. Walsh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas Schröder.

Additional information

Guest editors: S. S. S. Sarma, R. D. Gulati, R. L. Wallace, S. Nandini, H. J. Dumont & R. Rico-Martínez

Advances in Rotifer Research

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schröder, T., Walsh, E.J. Cryptic speciation in the cosmopolitan Epiphanes senta complex (Monogononta, Rotifera) with the description of new species. Hydrobiologia 593, 129–140 (2007). https://doi.org/10.1007/s10750-007-9066-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-007-9066-5

Keywords

Search

Navigation