Advertisement

Hydrobiologia

, Volume 796, Issue 1, pp 19–37 | Cite as

Morphological and taxonomic demarcation of Brachionus asplanchnoidis Charin within the Brachionus plicatilis cryptic species complex (Rotifera, Monogononta)

  • Evangelia MichaloudiEmail author
  • Scott Mills
  • Spiros Papakostas
  • Claus-Peter Stelzer
  • Alexander Triantafyllidis
  • Ilias Kappas
  • Kalliopi Vasileiadou
  • Konstantinos Proios
  • Theodore John Abatzopoulos
ROTIFERA XIV
First Online:

Abstract

Three well-defined groups, consisting of 15 species, have recently been ascribed to organisms historically identified as the Brachionus plicatilis species complex. One of these groups, the large clade, is composed of two named species (Brachionus plicatilis s.s. and Brachionus manjavacas) and two species identifiers (B. ‘Nevada’ and B. ‘Austria’). B. ‘Austria’ has been confirmed to be B. asplanchnoidis. As no type specimen exists for this species, and the original taxonomic description is lacking in detail, we give a detailed account of this species using material from Obere Halbjochlacke in Austria where B. ‘Austria’ was first identified genetically. Our analysis of B. asplanchnoidis populations was of global scope, an approach that revealed a great degree of morphological variability. However, combining aspects of both the dorsal and ventral surfaces clearly discriminated B. asplanchnoidis from the rest of the large-type members. This approach may prove useful in taxonomic studies of other cryptic species with relatively few morphological features. We also observed a geographic pattern of genetic divergence within B. asplanchnoidis. Average uncorrected COI divergences for a 554-bp fragment of the COI gene ranged from 3.9% within species to 17.5% between species of the large clade and indicate deep divisions within the cryptic species complex.

Keywords

Brachionus plicatilis Brachionus asplanchnoidis Brachionus ‘Nevada’ Brachionus ‘Austria’ Brachionus manjavacas Rotifer Morphology Species delimitation 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We would like to thank M. Serra and T.W. Snell for providing individuals and resting eggs from clones they keep in their laboratories; M. Pichler for providing technical assistance; A. Herzig for assisting in the collection of samples from Obere Halbjochlacke and Oberer Stinkersee (Austria), and C. Jersabek for the collection of sediments from which MNCHU clones were extracted and for assistance with the identification of OHJ72. This work was partially supported by an EU research project (ROTIGEN, Q5RS-2002-01302), while SP was supported by the Academy of Finland (Grant Number 258048). We gratefully acknowledge the efforts of two anonymous reviewers and D. Fontaneto whose valuable suggestions were extremely helpful to finally shape the manuscript.

Supplementary material

10750_2016_2924_MOESM1_ESM.pdf (383 kb)
Supplementary material 1 (PDF 383 kb)
10750_2016_2924_MOESM2_ESM.pdf (281 kb)
Supplementary material 2 (PDF 281 kb)

References

  1. Abramoff, M. D., P. J. Magalhaes & S. J. Ram, 2004. Image processing with ImageJ. Biophotonics International 11: 36–42.Google Scholar
  2. Ahlstrom, E. H., 1940. A revision of the rotatorian genera Brachionus and Platyias, with descriptions of one new species and two new varieties. Bulletin of the American Museum of Natural History 77: 143–184.Google Scholar
  3. Brown, J. M., S. M. Hedtke, A. R. Lemmon & E. M. Lemmon, 2010. When trees grow too long: investigating the causes of highly inaccurate bayesian branch-length estimates. Systematic Biology 59: 145–161.CrossRefPubMedGoogle Scholar
  4. Campillo, S., E. M. García-Roger, D. Martínez-Torres & M. Serra, 2005. Morphological stasis of two species belonging to the L-morphotype in the Brachionus plicatilis species complex. Hydrobiologia 546: 181–187.CrossRefGoogle Scholar
  5. Charin, N. N., 1947. O novom vide kolovratki is roda Brachionus. Doklady Akademii Nauk SSSR 56: 107–108.Google Scholar
  6. Ciros-Pérez, J., A. Gómez & M. Serra, 2001. 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.CrossRefGoogle Scholar
  7. Darriba, D., G. L. Taboada, R. Doallo & D. Posada, 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Drummond, A. J., M. A. Suchard, D. Xie & A. Rambaut, 2012. Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 1969–1973.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Edgar, R. C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Ezard, T., T. Fujisawa & T. G. Barraclough, 2014. splits: SPecies’ LImits by Threshold Statistics. R package version 1.0-19/r51. [available on internet at http://R-Forge.R-project.org/projects/splits/].
  11. Folmer, O., M. Black, W. Hoeh, R. Lutz & 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.PubMedGoogle Scholar
  12. Fontaneto, D., 2014. Molecular phylogenies as a tool to understand diversity in rotifers. International Review of Hydrobiology 99: 178–187.CrossRefGoogle Scholar
  13. Fontaneto, D., I. Giordani, G. Melone & M. Serra, 2007. Disentangling the morphological stasis in two rotifer species of the Brachionus plicatilis species complex. Hydrobiologia 583: 297–307.CrossRefGoogle Scholar
  14. Fontaneto, D., M. Kaya, E. A. Herniou & T. G. Barraclough, 2009. Extreme levels of hidden diversity in microscopic animals (Rotifera) revealed by DNA taxonomy. Molecular Phylogenetics and Evolution 53: 182–189.CrossRefPubMedGoogle Scholar
  15. Fu, Y., K. Hirayama & Y. Natsukari, 1991. Morphological differences between two types of the rotifer Brachionus plicatilis O.F. Müller. Journal of Experimental Marine Biology and Ecology 151: 29–41.CrossRefGoogle Scholar
  16. Gómez, A. & G. R. Carvalho, 2000. Sex, parthenogenesis and genetic structure of rotifers: microsatellite analysis of contemporary and resting egg bank populations. Molecular Ecology 9: 203–214.CrossRefPubMedGoogle Scholar
  17. Gómez, A., M. Temprano & M. Serra, 1995. Ecological genetics of a cyclical parthenogen in temporary habitats. Journal of Evolutionary Biology 8: 601–622.CrossRefGoogle Scholar
  18. 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.CrossRefPubMedGoogle Scholar
  19. Horváth, Z. C. F., A. Vad, K. Tóth, E. Zsuga, L. Vörös Boros & R. Ptacnik, 2014. Opposing patterns of zooplankton diversity and functioning along a natural stress gradient: when the going gets tough, the tough get going. Oikos 123: 461–471.CrossRefGoogle Scholar
  20. International Commission on Zoological Nomenclature, 1999. International Code of Zoological Nomenclature, 4th edition, 306 pp.Google Scholar
  21. Itigilova, M. Ts., A. Dulmaa & E Yu Afonina, 2014. Zooplankton of lakes of the Uldza and Kerulen River Valleys of northeastern Mongolia. Inland Water Biology 7: 249–258.CrossRefGoogle Scholar
  22. Jersabek, C. D. & E. Bolortsetseg, 2010. Mongolian rotifers (Rotifera, Monogononta) – a checklist with annotations on global distribution and autecology. Proceeding of the Academy of Natural Sciences of Philadephia 159: 119–168.CrossRefGoogle Scholar
  23. Jersabek, C. D., E. Bolortsetseg & H. L. Taylor, 2010. Mongolian rotifers on microscope slides: instructions to permanent specimen mounts from expedition material. Mongolian Journal of Biological Sciences 8: 51–57.CrossRefGoogle Scholar
  24. Koste, W. & R. J. Shiel, 1980. New Rotifera from Australia. Transactions of the Royal Society of South Australia 104: 133–144.Google Scholar
  25. Kutikova, L.A., 1970. Rotifer Fauna USSR. Fauna USSR. 104. Leningrad: Acad. Nauk. SSSR.Google Scholar
  26. Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.CrossRefPubMedGoogle Scholar
  27. Marshall, D. C., 2010. Cryptic failure of partitioned Bayesian phylogenetic analyses: lost in the land of long trees. Systematic Biology 59: 108–117.CrossRefPubMedGoogle Scholar
  28. Mills, S., J. Arturo Alcántara-Rodríguez, J. Ciros-Pérez, A. Gómez, A. Hagiwara, K. Hinson Galindo, C. D. Jersabek, R. Malekzadeh-Viayeh, F. Leasi, J.-S. Lee, D. B. M. Welch, S. Papakostas, S. Riss, H. Segers, M. Serra, R. Shiel, R. Smolak, T. W. Snell, C.-P. Stelzer, C. Q. Tang, R. L. Wallace, D. Fontaneto & E. J. Walsh, 2016. Fifteen species in one: deciphering the Brachionus plicatilis species complex (Rotifera, Monogononta) through DNA taxonomy. Hydrobiologia (this volume)Google Scholar
  29. Okogwu, O. I., 2010. Seasonal variations of species composition and abundance of zooplankton in Ehoma Lake, a floodplain lake in Nigeria. Revista de Biologia Tropical 58: 171–182.PubMedGoogle Scholar
  30. Oogami, H., 1976. On the morphology of Brachionus plicatilis (in Japanese). Newsletter Izu Branch, Shizuoka Prefectural Fisheries Research Center 18: 2–5.Google Scholar
  31. Ovander, E., N. Iakovenko, V. Trokhymets, Yu Gromova, O. Pashkova & L. Guleikova, 2011. Annotated checklist of monogonont rotifers belonging to the order Ploima (Rotifera: Eurotatoria, Monogonontam Ploima) of Ukraine. Part II. PИБOГOCПOДAPCЬКA HAУКA УКPAÏHИ 3: 46–54.Google Scholar
  32. Papakostas, S., A. Triantafyllidis, I. Kappas & T. J. Abatzopoulos, 2005. The utility of the 16S gene in investigating cryptic speciation within the Brachionus plicatilis species complex. Marine Biology 147: 1129–1139.CrossRefGoogle Scholar
  33. Papakostas, S., A. Triantafyllidis, I. Kappas & T. J. Abatzopoulos, 2009. Clonal composition of Brachionus plicatilis s.s. and B. sp. ‘Austria’ hatchery strains based on microsatellite data. Aquaculture 296: 15–20.CrossRefGoogle Scholar
  34. Papakostas, S., E. Michaloudi, A. Triantafyllidis, I. Kappas & T. J. Abatzopoulos, 2013. Allochronic divergence and clonal succession: two microevolutionary processes sculpturing population structure of Brachionus rotifers. Hydrobiologia 700: 33–45.CrossRefGoogle Scholar
  35. Paradis, E., J. Claude & K. Strimmer, 2004. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290.CrossRefPubMedGoogle Scholar
  36. Pons, J., T. G. Barraclough, J. Gomez-Zurita, A. Cardoso, D. P. Duran, S. Hazell, S. Kamoun, W. D. Sumlin & A. P. Vogler, 2006. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55: 595–609.CrossRefPubMedGoogle Scholar
  37. Proios, K., E. Michaloudi, S. Papakostas, I. Kappas, K. Vasileiadou & T. J. Abatzopoulos, 2014. Updating the description and taxonomic status of Brachionus sessilis Varga, 1951 (Rotifera: Brachionidae) based on detailed morphological analysis and molecular data. Zootaxa. 3873: 345–370.CrossRefPubMedGoogle Scholar
  38. Rambaut, A., M. A. Suchard, D. Xie & A. J. Drummond, 2014. Tracer v1.6 [available on internet at http://beast.bio.ed.ac.uk/Tracer].
  39. Riss, S., W. Arthofer, F. M. Steiner, B. C. Schlick-Steiner, M. Pichler, P. Stadler & C.-P. Stelzer, 2016. Do genome size differences within Brachionus asplanchnoidis (Rotifera, Monogononta) cause reproductive barriers among geographic populations? Hydrobiologia (this volume)Google Scholar
  40. Rong, S., H. Segers & H. J. Dumont, 1998. Distribution of Brachionidae (Rotifera, Monogononta) in Inner Mongolian waters. International Review of Hydrobiology 83: 305–310.CrossRefGoogle Scholar
  41. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Schlick-Steiner, B. C., B. Seifert, C. Stauffer, E. Christian, R. H. Crozier & F. M. Steiner, 2007. Without morphology, cryptic species stay in taxonomic crypsis following discovery. Trends in Ecology and Evolution 22: 391–392.CrossRefPubMedGoogle Scholar
  43. Segers, H., 1995. Nomenclature consequences of some recent studies on Brachionus plicatilis (Rotifera, Brachionidae). Hydrobiologia 313(314): 121–122.CrossRefGoogle Scholar
  44. Segers, H., 2007. Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa 1564: 1–104.Google Scholar
  45. Segers, H., G. Murugan & H. J. Dumont, 1993. On the taxonomy of the Brachionidae: description of Plationus n. gen. (Rotifera, Monogononta). Hydrobiologia 268: 1–8.CrossRefGoogle Scholar
  46. Segers, H., W. De Smet, C. Fischer, D. Fontaneto, E. Michaloudi, R. L. Wallace & C. D. Jersabek, 2012. Towards a list of available names in zoology, partim Phylum Rotifera. Zootaxa 3179: 61–68.Google Scholar
  47. Stamatakis, A., P. Hoover & J. Rougemont, 2008. A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57: 758–771.CrossRefPubMedGoogle Scholar
  48. Stelzer, C. P., S. Riss & P. Stadler, 2011. Genome size evolution at the speciation level: the cryptic species complex Brachionus plicatilis (Rotifera). BMC Evolutionary Biology 11: 90.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Suatoni, E., S. Vicario, S. Rice, T. Snell & A. Caccone, 2006. An analysis of species boundaries and biogeographic patterns in a cryptic species complex: the rotifer – Brachionus plicatilis. Molecular Phylogenetics and Evolution 41: 86–98.CrossRefPubMedGoogle Scholar
  50. Sukumaran, J. & M. T. Holder, 2010. DendroPy: a Python library for phylogenetic computing. Bioinformatics 26: 1569–1571.CrossRefPubMedGoogle Scholar
  51. Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Tang, C. Q., F. Leasi, U. Obertegger, A. Kieneke, T. G. Barraclough & D. Fontaneto, 2012. The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proceedings of the National Academy of Sciences 109: 16208–16212.CrossRefGoogle Scholar
  53. Tóth, A., Z. Horváth, C. F. Vad, K. Zsuga, S. A. Nagy & E. Boros, 2014. Zooplankton of the European soda pans: Fauna and conservation of a unique habitat type. International Review of Hydrobiology 99: 255–276.CrossRefGoogle Scholar
  54. Xiang, X.-L., Y.-L. Xi, X.-L. Wen, G. Zhang, J.-X. Wang & K. Hu, 2011. Patterns and processes in the genetic differentiation of the Brachionus calyciflorus complex, a passively dispersing freshwater zooplankton. Molecular Phylogenetics and Evolution 59: 386–398.CrossRefPubMedGoogle Scholar
  55. Yermolaeva, N. I. & O. S. Burmistrova, 2005. Influence of mineralization on zooplankton of the Lake Chany. Cubupckuŭ Эkoлozuлeckuŭ жypнaл 2: 235–247.Google Scholar
  56. Zagorodnyaya, Y. A., E. A. Batogova & N. V. Shadrin, 2008. Long-term transformation of zooplankton in the hypersaline lake Bakalskoe (Crimea) under salinity fluctuations. MOPCЬКИЙ EКOЛOГIЧHИЙ ЖУPHAЛ 7: 41–50.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Evangelia Michaloudi
    • 1
    Email author
  • Scott Mills
    • 2
  • Spiros Papakostas
    • 3
  • Claus-Peter Stelzer
    • 4
  • Alexander Triantafyllidis
    • 5
  • Ilias Kappas
    • 5
  • Kalliopi Vasileiadou
    • 5
  • Konstantinos Proios
    • 1
  • Theodore John Abatzopoulos
    • 5
  1. 1.Department of ZoologyAristotle University of ThessalonikiThessaloníkiGreece
  2. 2.James Cook UniversityTownsvilleAustralia
  3. 3.Division of Genetics and Physiology, Department of BiologyUniversity of TurkuTurkuFinland
  4. 4.Research Institute for LimnologyUniversity of InnsbruckMondseeAustria
  5. 5.Department of Genetics, Development & Molecular BiologyAristotle University of ThessalonikiThessaloníkiGreece

Personalised recommendations

Cite article

Buy options