Abstract
Bdelloid rotifers are mostly known for two peculiarities, continuous parthenogenetic reproduction and dormancy in response to habitat desiccation, a phenomenon named anhydrobiosis. These uncommon traits earned them the names of ‘evolutionary scandals’ and ‘sleeping beauties’, respectively. Relevant aspects of bdelloid biology have recently been described that connect parthenogenesis to anhydrobiosis and that might account for their evolutionary survival in spite of the conservative reproduction. In the present study, I explore recent literature, in the attempt to disentangle the apparent incongruency between the apomictic reproduction and the presumed long-term evolutionary survival of bdelloid species. Recent results remarkably improved our knowledge of bdelloid population biology, genetics, and molecular biology. The most relevant findings concern (i) acquisition of foreign genes through horizontal transfer, (ii) presence of divergent sequences possibly corresponding to ancient gene duplications and (iii) capacity to escape parasites: events that appear to be connected with dormancy. I also address the results of recent studies on the relationships between bdelloids and other rotifers, including acanthocephalans, in an attempt to highlight similarities and differences that should be clarified to better understand phylogenetic relationship among the Rotifera sensu lato.
Similar content being viewed by others
References
Ahlrichs, W., 1995a. Ultrastruktur und Phylogenie von Seison nebaliae (Grube 1859) und Seison annulatus (Claus 1876). Hypothesen zu phylogenetischen Verwandtschaftsverhältnissen innerhalb der Bilateria. Ph D. Thesis, Georg-August-Universität zu Göttingen: 1–310.
Ahlrichs, W. 1995b. Seison annulatus und Seison nebaliae-Ultrastruktur und Phylogenie. Verh. Deu. Zool. Ges., 88.1.
Amsellem, J. & C. Ricci, 1982. Fine structure of the female genital apparatus in Philodina roseola (Rotifera, Bdelloidea). Zoomorphology 100: 89–105.
Barron, G. L., 2004. Fungal parasites and predators of rotifers, nematodes, and other invertebrates. In Mueller, G. M., G. F. Bills, & M. S. Foster (eds), Biodiversity of Fungi: Inventory and Monitoring Methods. Elsevier, New York: 435–450.
Bock, R., 2010. The give-and-take of DNA: horizontal gene transfer in plants. Trends of Plant Sciences 15: 11–22.
Boto, L., 2014. Horizontal gene transfer in the acquisition of novel traits by metazoans. Proceedings of the Royal Society, London, B Biological Sciences 281: 20132450.
Boström, S., 1995. Populations of Plectus acuminatus Bastian, 1865 and Panagrolaimus magnivulvatus n.sp. (Nematoda) from nunatakks in Dronning Maud Land. East Antarctica. Fundamental & Applied Nematology 18: 25–34.
Boschetti, C., C. Ricci, U. Fascio & C. Sotgia, 2005. The development of a bdelloid egg: a contribution after 100 years. Hydrobiologia 546: 323–331.
Boschetti, C., N. Pouchkina-Stantcheva, P. Hoffmann & A. Tunnacliffe, 2011. Foreign genes and novel hydrophilic protein genes participate in the desiccation response of the bdelloid rotifer Adineta ricciae. Journal of Experimental Biology 214: 59–68.
Boschetti, C., A. Carr, A. Crisp, I. Eyres, Y. Wang-Koh, E. Lubzens, T. G. Barraclough, G. Micklem & A. Tunnacliffe, 2012. Biochemical diversification through foreign gene expression in bdelloid rotifers. PLOS Genetics 8: e1003035. doi:10.1371/journal.pgen.1003035.
Clément, P., 1993. The phylogeny of rotifers: molecular, ultrastructural and behavioural data. Hydrobiologia 255(256): 527–544.
Crisp, A., C. Boschetti, M. Perry, A. Tunnacliffe & G. Micklem, 2015. Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes. Genome Biology 16: 50.
Debortoli, N., X. Li, I. Eyres, D. Fontaneto, B. Hespeels, C. Q. Tang, J. F. Flot & K. Van Doninck, 2016. Genetic exchange among bdelloid rotifers is more likely due to horizontal gene transfer than to meiotic sex. Current Biology 26: 1–10.
De Smet, W. H., G. Melone, D. Fontaneto & F. Leasi, 2015. Marine Rotifera, Fauna d’Italia, Vol. 50. Calderini, Bologna: 252 pp.
Dobers, E., 1915. Über die Biologie der Bdelloidea. Internationalen Revue der gesamten Hydrobiologie und Hydrographie – Biologisches Supplement: 128 pp.
Donner, J., 1965. Ordnung Bdelloidea (Rotatoria, Rädertiere). Akademie Verlag, Berlin: 297 pp.
Eyres, I., C. Boschetti, A. Crisp, T. P. Smith, D. Fontaneto, A. Tunnacliffe & T. G. Barraclough, 2015. Horizontal gene transfer in bdelloid rotifers is ancient, ongoing and more frequent in species from desiccating habitats. BMC Biology 13(90): 1–17.
Ferraguti, M. & G. Melone, 1999. Spermiogenesis in Seison nebaliae (Rotifera, Seisonidea): further evidence of a rotifer-acanthocephalan relationship. Tissue and Cell 31: 428–440.
Flot, J. F., B. Hespeels, X. Li, B. Noel, I. Archipova, E. G. J. Danchin, A. Ejnol, B. Henrissat, R. Koszul, et al., 2013. Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature 500: 453–457.
Fontaneto, D. & T. G. Barraclough, 2015. Do species exist in asexuals? Theory and evidence from bdelloid rotifers. Integrative and Comparative Biology. doi:10.1093/icb/icv024.
Fontaneto, D., W. H. De Smet & C. Ricci, 2006. Rotifers in saltwater environments, re-evaluation of an inconspicuous taxon. Journal of the Marine Biological Association of the United Kingdom 86: 623–656. doi:10.1017/S0025315406013531.
Garey, J. R., T. J. Near, M. R. Nonnemacher & S. A. Nadler, 1996. Molecular evidence for Acanthocephala as a subtaxon of Rotifera. Journal of Molecular Evolution 43: 287–292.
Garey, J. R., A. Schmidt-Rhaesa, T. J. Near & S. A. Nadler, 1998. The evolutionary relationship of rotifers and acanthocephalans. Hydrobiologia 387(388): 83–91.
Gladyshev, E. A. & I. R. Arckhipova, 2010. Genome structure of bdelloid rotifers shaped by asexuality or desiccation? Journal of Heredity 101(suppl 1): 585–593.
Gladyshev, E. A. & M. Meselson, 2008. Extreme resistance of bdelloid rotifers to ionizing radiation. Proceedings of National Academy of Sciences, USA 105: 5139–5144.
Gladyshev, E. A., M. Meselson & I. R. Arkhipova, 2008. Massive horizontal gene transfer in bdelloid rotifers. Science 320: 1210–1213.
Hamilton, W. D., 1975. Gamblers since life began: barnacles, aphids, elms. Quarterly Review of Biology 50: 175–180.
Hespeels, B., M. Knapen, D. Hanot-Mambres, A. C. Heuskin, F. Pineux, S. Lucas, R. Kotzul, K. Van Doninck, et al., 2014. Gateway to genetic exchange? DNA double strand-strand breaks in the bdelloid rotifer Adineta vaga submitted to desiccation. Journal of Evolutionary Biology 27: 1334–1345.
Krisko, A., M. Leroy, M. Radman & M. Meselson, 2012. Extreme anti-oxidant protection against ionizing radiation in bdelloid rotifers. Proceedings of National Academy of Sciences, USA 109: 2354–2357.
Lansing, A. I., 1947. A transmissible, cumulative and reversible factor in aging. Journal of Gerontology 2: 228–239.
Lapinski, J. & A. Tunnacliffe, 2003. Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Letters 553: 387–390.
Lasek-Nesselquist, E., 2012. A mitogenomic re-evaluation of the bdelloid phylogeny and relationships among the Syndermata. PLOS ONE 7(8): e43554. doi:10.1371/journal.pone.0043554.
Lorenzen, S., 1985. Phylogenetic aspects of pseudocoelomate evolution. In Conway Morris, S., J. D. George, R. Gibson & H. M. Platt (eds), The Origins and Relationships of Lower Invertebrates. Clarendon Press, Oxford: 210–223.
Mark Welch, D. B. & M. Meselson, 2000. Evidence for the evolution of bdelloid rotifers without sexual recombination or genetic exchange. Science 288: 1211–1215.
Mark Welch, D. B. & M. Meselson, 2003. Oocyte nuclear DNA content and GC proportion in rotifers of the anciently asexual Class Bdelloidea. Biological Journal of the Linnean Society 79: 85–91.
Mark Welch, D. B., M. P. Cummings, D. M. Hillis & M. Meselson, 2004. Divergent gene copies in the asexual class Bdelloidea (Rotifera) separated before the bdelloid radiation or within bdelloid families. Proceedings of National Academy of Sciences, USA 101: 1622–1625.
Mark Welch, D. B., J. L. Mark Welch & M. Meselson, 2008. Evidence for degenerate tetraploidy in bdelloid rotifers. Proceedings of National Academy of Sciences, USA 105: 5145–5149.
Marotta, R., F. Leasi, A. Uggetti, C. Ricci & G. Melone, 2010. Dry and survive: morphological changes during anhydrobiosis in a bdelloid rotifer. Journal of Structural Biology 171: 11–17.
Marotta, R., A. Uggetti, C. Ricci, F. Leasi & G. Melone, 2012. Surviving starvation: changes accompanying starvation tolerance in a bdelloid rotifer. Journal of Morphology 273: 1–7.
Maynard Smith, J., 1986. Contemplating life without sex. Nature 324: 300–301.
Melone, G. & M. Ferraguti, 1994. The spermatozoon of Brachionus plicatilis (Rotifera, Monogononta) with some notes on sperm ultrastructure in Rotifera. Acta Zoologica 75: 81–88.
Melone, G. & M. Ferraguti, 1999. Rotifera. In Jamieson, B. G. M. (ed.), Reproductive Biology of Invertebrates – Vol.IX, Part A, Progress in Male Gamete Biology. Oxford and IBH Publishing Co., New Delhi: 157–169.
Melone, G. & D. Fontaneto, 2005. Trophi structure in bdelloid rotifers. Hydrobiologia 546: 197–202.
Melone, G. & C. Ricci, 1995. Rotatory apparatus in bdelloids. Hydrobiologia 313(314): 91–98.
Melone, G., C. Ricci, H. Segers & R. L. Wallace, 1998. Phylogenetic relationships of phylum Rotifera with emphasis on the families of Bdelloidea. Hydrobiologia 387(388): 101–107.
Nelson, D. R., R. Guidetti, & Rebecchi, L. 2015. Phylum Tardigrada. In Thorp, J. & D.C. Rogers (eds), Ecology and General Biology: Thorp and Covich’s Freshwater Invertebrates. Academic Press: 347–380.
Poinar, G. O. & C. Ricci, 1992. Bdelloid rotifers in dominican amber: evidence for parthenogenetic continuity. Experientia 48: 408–410.
Pouchkina-Stantcheva, N., B. M. McGee, C. Boschetti, D. Tolleter, S. Chakrabortee, A. V. Popova, F. Meersman, D. Macherel, D. K. Hincha & A. Tunnacliffe, 2007. Functional divergence of former alleles in an ancient asexual invertebrate. Science 318: 268–271.
Ricci, C., 1980. Experimental observations on maternal reproductive rate and offspring characteristics. Hydrobiologia 73: 21–25.
Ricci, C., 1983. Life histories of some species of rotifera bdelloidea. Hydrobiologia 104: 175–180.
Ricci, C., 1998. Anhydrobiotic capabilities of bdelloid rotifers. Hydrobiologia 387(388): 321–326.
Ricci, C., 2001. Dormancy patterns in rotifers. Hydrobiologia 446(447): 1–11.
Ricci, C. & G. Melone, 2000. Key to the identification of the genera of bdelloid rotifers. Hydrobiologia 418: 73–80.
Ricci, C. & F. Perletti, 2006. Starve and survive: stress tolerance and life-history traits of a bdelloid rotifer. Functional Ecology 20: 340–346
Ricci, C., L. Vaghi & M. L. Manzini, 1987. Desiccation of rotifers (Macrotrachela quadricornifera): Survival and reproduction. Ecology 68: 1488–1494.
Ricci, C., N. Santo, E. Radaelli & A. M. Bolzern, 1999. Epigenetic inheritance systems in bdelloid rotifers. I. Maternal-age-related biochemical effects. Italian Journal of Zoology 66: 333–339.
Ricci, C., G. Melone & E. J. Walsh, 2001. A carnivorous bdelloid rotifer, Abrochtha carnivora n.sp. Invertebrate Biology 120(2): 136–141.
Ricci, C., G. Melone, N. Santo & M. Caprioli, 2003. Morphological response of a bdelloid rotifer to desiccation. Journal of Morphology 257: 246–253.
Ricci, C., M. Caprioli & D. Fontaneto, 2007. Stress and fitness in parthenogens: is dormancy a key feature for bdelloid rotifers? BMC Evolutionary Biology. doi:10.1186/1471-2148-7-S2-S9.
Ricci, C., M. Caprioli, D. Fontaneto & G. Melone, 2008. Volume and morphology changes of a bdelloid rotifer species (Macrotrachela quadricornifera) during anhydrobiosis. Journal of Morphology 269: 233–239.
Schwander, T., 2016. Evolution: the end of an ancient asexual scandal. Current Biology 26: R233–R235.
Segers, H., 2007. Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa 1564: 1–104.
Signorovitch, A., J. Hur, E. Gladyshev & M. Meselson, 2015. Allele sharing and evidence for sexuality in mitochondrial clade of bdelloid rotifers. Genetics 200: 581–590.
Tunnacliffe, A., J. Lapinski & B. McGee, 2005. A putative LEA protein, but no trehalose, is present in anhydrobiotic bdelloid rotifers. Hydrobiologia 546: 315–321.
Wesenberg-Lund, C., 1930. Contributions to the biology of the Rotifera, Part II: the periodicity and sexual periods. Memoires de l’Académie Royal de Sciences et Lettres, Copenhague: 1–230.
Wey-Fabrizius, A., H. Herlyn, B. Rieger, D. Rosenkranz, A. Witek, D. Mark Welch, I. Ebersberger & T. Hanken, 2014. Transcriptome data reveal syndermatan relatioships and suggest the evolution of endoparasitism via an epizoic stage. PLOS ONE 9(2): e88618. doi:10.1371/journal.pone.0088618.
Wilson, C. G., 2011. Desiccation-tolerance in bdelloid rotifers facilitates spatiotemporal escape from multiple species of parasitic fungi. Biological Journal of the Linnean Society 104: 564–574.
Wilson, C. G. & P. W. Sherman, 2010. Anciently asexual Bdelloid Rotifers escape lethal fungal parasites by drying up and blowing away. Science 327: 574–576.
Wilson, C. G. & P. W. Sherman, 2013. Spatial and temporal escape from fungal parasitism in natural communities of anciently asexual bdelloid rotifers. Proceedings of the Royal Society B Biological Sciences. doi:10.1098/rspb.2013.1255.
Wallace, R. L., T. W. Snell, C. Ricci & T. Nogrady, 2006. Rotifera. Volume 1: biology, ecology and systematics (2nd edition). In Segers, H. (ed), Guides to the Identification of the Microinvertebrates of the Continental Waters of the World. Backuys Publishers, Leiden, 299 pp.
Zelinka, C., 1892. Studien über Räderthiere. III. Zur Entwicklungsgeschichte der Räderthiere nebst Bemerkungen über ihre Anatomie und Biologie. Zeitschrift fur wissenschaftliche Zoologie 53: 1–159.
Acknowledgments
The author thanks the organizing committee of the Rotifer International Symposium, and chiefly Miloslav Devetter, for the kind invitation to offer a ‘personal’ story and contribution to bdelloid rotifers research. The author thanks Hans Ramløv who, together with Nadia Santo, produced the metabolism graph in his lab and is allowing me to use it. Indications about the dormancy of Nematodes and Tardigrades came from Aldo Zullini and Roberto Bertolani, colleagues who I wish to thank. The author also thanks Charles King for his comments, suggestions and revision of an earlier version of the manuscript and her husband, Giulio Melone, for his continuous, silent encouragements. Anonymous referees greatly contributed to the improvement of the clarity of my contribution, and I wish to thank them for the generous help.
Author information
Authors and Affiliations
Corresponding author
Additional information
Guest editors: M. Devetter, D. Fontaneto, C. D. Jersabek, D. B. Mark Welch, L. May & E. J. Walsh / Evolving rotifers, evolving science
Rights and permissions
About this article
Cite this article
Ricci, C. Bdelloid rotifers: ‘sleeping beauties’ and ‘evolutionary scandals’, but not only. Hydrobiologia 796, 277–285 (2017). https://doi.org/10.1007/s10750-016-2919-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-016-2919-z