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Molecular ecology of rotifers: from population differentiation to speciation

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Rotifera X

Part of the book series: Developments in Hydrobiology ((DIHY,volume 181))

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Abstract

The development of cost-effective molecular tools allowing the amplification of minute amounts of DNA effectively opened the field of molecular ecology for rotifers. Here I review these techniques and the advances they have provided in the understanding of sibling species complexes, clonal structure, resting egg banks, population structure, phylogeographic patterns and phylogenetic relationships in rotifers. Most of the research to date has focused on the rotifer species complex Brachionus plicatilis. The use of DNA sequence and microsatellite variation, in the context of the background knowledge of life history, mating behaviour, and temporal population dynamics in these organisms have revolutionised our views into the processes shaping the genetic diversity in aquatic invertebrates. Rotifers have populations with a very high number of clones in genetic equilibrium. In temporary populations clonal selection is effective in eroding the number of clones. Rotifer populations are strongly differentiated genetically for neutral markers, even at small geographical scales, and exhibit deep phylogeographic structure which might reflect the impact of Pleistocene glaciations. Despite the high potential for dispersal afforded by resting eggs, rotifers display persistent historical colonisation effects, with gene flow effective only at a local scale and with marked isolation by distance. Instances of long-distance transcontinental migration resulting in successful colonisation have also been revealed. B. plicatilis is composed of a group of several ancient species and sympatry is common. Despite this, the presence of cosmopolitan species in this species complex cannot be discounted. I discuss future priorities and point out the main areas where our knowledge is still insufficient.

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References

  • Avise, J. C., 2000. Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, Massachusetts, 447 pp.

    Google Scholar 

  • Bailey, S. A., I. C. Duggan, C. D. A. Overdijk, P. T. Jenkins & H. J. MacIsaac, 2003. Viability of invertebrate diapausing eggs collected from residual ballast water. Limnology and Oceanography 48: 1701–1710.

    Google Scholar 

  • Baum, D. A. & K. L. Shaw, 1995. Genealogical perspectives on the species problem. In Hoch, P. C. & A. G. Stephenson (eds), Experimental and Molecular Approaches to Plant Biosystematics. Missouri Botanical Garden, Columbia, Missouri, 289–303.

    Google Scholar 

  • Berrieman, H. K., D. H. Lunt & A. Gómez, (2005). Behavioural reproductive isolation in a rotifer hybrid zone. Hydrobiologia 546: 125–134.

    Article  CAS  Google Scholar 

  • Birky, C. W., P. Fuerst & T. Maruyama, 1989. Organelle gene diversity under migration, mutation, and drift — equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121: 613–627.

    PubMed  Google Scholar 

  • Birky, C. W., 2001. The inheritance of genes in mitochondria and chloroplasts: Laws, mechanisms, and models. Annual Review of Genetics 35: 125–148.

    Article  CAS  PubMed  Google Scholar 

  • Birt, T. B. & A. J. Baker, 2000. Polymerase Chain Reaction. In Baker, A. J. (ed.), Molecular Methods in Ecology. Blackwell Science, Oxford, 50–64.

    Google Scholar 

  • Black, R. W. & L. B. Slobodkin, 1987. What is cyclomorphosis. Freshwater Biology 18: 373–378.

    Google Scholar 

  • Boileau, M. G., P. D. N. Hebert & S. S. Schwartz, 1992. Nonequilibrium gene frequency divergence — persistent founder effects in natural populations. Journal of Evolutionary Biology 5: 25–39.

    Article  Google Scholar 

  • Brumfield, R. T., P. Beerli, D. A. Nickerson & S. V. Edwards, 2003. The utility of single nucleotide polymorphisms in inferences of population history. Trends in Ecology & Evolution 18: 249–256.

    Article  Google Scholar 

  • Cáceres, C. E., 1997. Temporal variation, dormancy, and coexistence: a field test of the storage effect. Proceedings of the National Academy of Sciences of the United States of America 94: 9171–9175.

    PubMed  Google Scholar 

  • Carvalho, G. R., 1998. Advances in Molecular Ecology. IOS Press, Amsterdam, 313 pp.

    Google Scholar 

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

    Google Scholar 

  • 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.

    Google Scholar 

  • Cousyn, C., L. Meester, J. K. Colbourne, L. Brendonck, D. Verschuren & F. Volckaert, 2001. Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes. Proceedings of the National Academy of Sciences of the United States of America 98: 6256–6260.

    Article  CAS  PubMed  Google Scholar 

  • De Meester, L., 1996. Local genetic differentiation and adaptation in freshwater zooplankton: patterns and processes. Ecoscience 3: 385–399.

    Google Scholar 

  • De Meester, L., A. Gómez, B. Okamura & K. Schwenk, 2002. The Monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecologica 23: 121–135.

    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.

    CAS  Google Scholar 

  • Dumont, H. J., 1983. Biogeography of rotifers. Hydrobiologia 104: 19–30.

    Article  Google Scholar 

  • Ebert, D., C. Haag, M. Kirkpatrick, M. Riek, J. W. Hottinger & V. I. Pajunen, 2002. A selective advantage to immigrant genes in a Daphnia metapopulation. Science 295: 485–488.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Fussmann, G., S. Ellner & N. De Stasio Jr, 2003. Microevolution as a critical component of plankton dynamics. Proceedings of the Royal Society of London Series B-Biological Sciences 270: 1015–1022.

    Article  Google Scholar 

  • Gilbert, J. J., 2001. Spine development in Brachionus quadridentatus from an Australian billabong: genetic variation and induction by Asplanchna. Hydrobiologia 446: 19–28.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Goldstein, D. B. & C. Schlotterer, 1999. Microsatellites: Evolution and Applications. Oxford University Press, Oxford, 352 pp.

    Google Scholar 

  • Gómez, A. & M. Serra, 1995. Behavioral reproductive isolation among sympatric strains of Brachionus plicatilis Muller 1786: Insights into the status of this taxonomic species. Hydrobiologia 313: 111–119.

    Article  Google Scholar 

  • Gómez, A., M. Temprano & M. Serra, 1995. Ecological genetics of a cyclical parthenogen in temporary habitats. Journal of Evolutionary Biology 8: 601–622.

    Google Scholar 

  • Gómez, A. & T. W. Snell, 1996. Sibling species and cryptic speciation in the Brachionus plicatilis species complex (Rotifera). Journal of Evolutionary Biology 9: 953–964.

    Google Scholar 

  • Gómez, A., M. J. Carmona & M. Serra, 1997. Ecological factors affecting gene flow in the Brachionus plicatilis complex (Rotifera). Oecologia 111: 350–356.

    Google Scholar 

  • Gómez, A., 1998. Allozyme electrophoresis: its application to rotifers. Hydrobiologia 387/388: 385–393.

    Google Scholar 

  • Gómez, A., C. Clabby & G. R. Carvalho, 1998. Isolation and characterization of microsatellite loci in a cyclically parthenogenetic rotifer, Brachionus plicatilis. Molecular Ecology 7: 1619–1621.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Gómez, A., G. R. Carvalho & D. H. Lunt, 2000. Phylogeography and regional endemism of a passively dispersing zooplankter: mitochondrial DNA variation in rotifer resting egg banks. Proceedings of the Royal Society of London Series B-Biological Sciences 267: 2189–2197.

    Google Scholar 

  • Gómez, A., G. J. Adcock, D. H. Lunt & G. R. Carvalho, 2002a. The interplay between colonisation history and gene flow in passively dispersing zooplankton: microsatellite analysis of rotifer resting egg banks. Journal of Evolutionary Biology 15: 158–171.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Haag, C. R., J. W. Hottinger, M. Riek & D. Ebert, 2002. Strong inbreeding depression in a Daphnia metapopulation. Evolution 56: 518–526.

    PubMed  Google Scholar 

  • Hebert, P. D. N., A. Cywinska, S. L. Ball & J. R. DeWaard, 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Series B-Biological Sciences 270: 313–321.

    Article  CAS  Google Scholar 

  • Hofmann, W., 1983. On temporal variation in the rotifer Keratella cochlearis (Gosse) — the question of Lauterborncycles. Hydrobiologia 101: 247–254.

    Google Scholar 

  • Jarne, P. & P. J. L. Lagoda, 1996. Microsatellites, from molecules to populations and back. Trends in Ecology & Evolution 11: 424–429.

    Google Scholar 

  • Jenkins, D. G. & A. L. Buikema Jr., 1998. Do similar communities develop in similar sites? a test with zooplankton structure and function. Ecological Monographs 68: 421–443.

    Google Scholar 

  • King, C. E., 1977. Genetics of reproduction, variation and adaptation in rotifers. Archiv fü r Hydrobiologie. Ergebnisse der Limnologie 8: 187–201.

    Google Scholar 

  • King, C. E., 1980. The genetic structure of zooplankton communities. In Kerfoot, W. C. (ed.), Evolution and Ecology of Zooplankton Communities. The University Press of New England, Hanover (N.H.), 315–328.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Leutbecher, C., 2000. A routine method of DNA-extraction from extremely small metazoans, e.g. single rotifer specimens for RAPD-PCR analyses. Hydrobiologia 437: 133–137.

    Article  Google Scholar 

  • Li, Y. C., A. B. Korol, T. Fahima, A. Beiles & E. Nevo, 2002. Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Molecular Ecology 11: 2453–2465.

    Article  CAS  PubMed  Google Scholar 

  • Lynch, M., M. Pfrender, K. Spitze, N. Lehman, J. Hicks, D. Allen, L. Latta, M. Ottene, F. Bogue & J. Colbourne, 1999. The quantitative and molecular genetic architecture of a subdivided species. Evolution 53: 100–110.

    Google Scholar 

  • Mark Welch, D. B. & M. Meselson, 2000. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288: 1211–1215.

    Google Scholar 

  • Morgan, K. K., J. Hicks, K. Spitze, L. Latta, M. E. Pfrender, C. S. Weaver, M. Ottone & M. Lynch, 2001. Patterns of genetic architecture for life-history traits and molecular markers in a subdivided species. Evolution 55: 1753–1761.

    CAS  PubMed  Google Scholar 

  • Ortells, R., T. W. Snell, A. Gómez & M. Serra, 2000. Patterns of genetic differentiation in resting egg banks of a rotifer species complex in Spain. Archiv fü r Hydrobiologie 149: 529–551.

    Google Scholar 

  • Ortells, R., 2002. Diversidad Genética y Ecológica en Especies Crípticas de Rotíferos. Patrones y Procesos, Universitat de Valencia, Valencia, Spain, 193 pp.

    Google Scholar 

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

    Article  Google Scholar 

  • Palumbi, S. R., 1996. The Polymerase Chain Reaction. In Hillis, D. M. & C. B. K. Moritz Marble (eds), Molecular Systematics. Sinauer, Sunderland, MA., 205–247.

    Google Scholar 

  • Pfrender, M. E., K. Spitze & N. Lehman, 2000. Multi-locus genetic evidence for rapid ecologically based speciation in Daphnia. Molecular Ecology 9: 1717–1735.

    Article  CAS  PubMed  Google Scholar 

  • Primmer, C. R., A. P. Moller & H. Ellegren, 1996. A wide-range survey of cros-species microsatellite amplification in birds. Molecular Ecology 5: 365–378.

    Article  CAS  PubMed  Google Scholar 

  • Primmer, C. R. & J. Merila, 2002. A low rate of microsatellite amplification success in Ranid frogs. Conservation Genetics 3: 445–449.

    Article  CAS  Google Scholar 

  • Rahel, F. J., 2002. Homogenisation of freshwater faunas. Annual Review of Ecology and Systematics 33: 291–315.

    Article  Google Scholar 

  • Segers, H., 1996. Biogeography of littoral Lecane Rotifera. Hydrobiologia 323: 169–197.

    Article  Google Scholar 

  • Segers, H., 2002. The nomenclature of the Rotifera: annotated checklist of valid family-and genus-group names. Journal of Natural History 36: 631–640.

    Article  Google Scholar 

  • Serra, M., M. J. Carmona & M. R. Miracle, 1994. Survival analysis of 3 clones of Brachionus plicatilis (Rotifera). Hydrobiologia 277: 97–105.

    Article  Google Scholar 

  • Serra, M., A. Galiana & A. Gómez, 1997. Speciation in monogonont rotifers. Hydrobiologia 358: 63–70.

    Article  Google Scholar 

  • Serra, M., A. Gómez & M. J. Carmona, 1998. Ecological genetics of Brachionus sympatric sibling species. Hydrobiologia 388: 373–384.

    Google Scholar 

  • Shurin, J. B., 2000. Dispersal limitation, invasion resistance and the structure of pond zooplankton populations. Ecology 81: 3074–3086.

    Google Scholar 

  • Snell, T. W. & K. Carrillo, 1984. Body size variation among strains of the rotifer Brachionus plicatilis. Aquaculture 37: 359–367.

    Article  Google Scholar 

  • Stenberg, P., M. Lundmark & A. Saura, 2003. MLGsim: a program for detecting clones using a simulation approach. Molecular Ecology Notes 3: 329–331.

    Article  CAS  Google Scholar 

  • Sunnucks, P., A. C. C. Wilson, L. B. Behegaray, L. B. Zenger, J. French & A. C. Taylor, 2000. SSCP is not that difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and molecular ecology. Molecular Ecology 9: 1699–1710.

    Article  CAS  PubMed  Google Scholar 

  • Tautz, D., P. Arctander, A. Minelli, R. H. Thomas & A. P. Vogler, 2003. A plea for DNA taxonomy. Trends in Ecology & Evolution 18: 70–74.

    Article  Google Scholar 

  • Taylor, D. J., P. D. N. Hebert & J. K. Colbourne, 1996. Phylogenetics and evolution of the Daphnia longispina group (Crustacea) based on 12S rDNA sequence and allozyme variation. Molecular Phylogenetics and Evolution 5: 495–510.

    Article  CAS  PubMed  Google Scholar 

  • Templeton, A. R., 1998. Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Molecular Ecology 7: 381–397.

    Article  CAS  PubMed  Google Scholar 

  • Vos, P., R. Hogers, M. Bleeker, M. Reijans, T. Lee, M. Hornes, A. Fritjers, J. Pot, J. Peleman, M. Kuiper & M. Zabeau, 1995. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23: 4407–4414.

    CAS  PubMed  Google Scholar 

  • Walsh, P. S., D. A. Metzger & R. Higuchi, 1991. Chelex-100 as a Medium for Simple Extraction of DNA for Pcr-Based Typing from Forensic Material. Biotechniques 10: 506–513.

    CAS  PubMed  Google Scholar 

  • Wayne, R. K., J. A. Leonard & A. Cooper, 1999. Full of sound and fury: the recent history of ancient DNA. Annual Review of Ecology and Systematics 30: 457–477.

    Article  Google Scholar 

  • Weider, L. J., A. Hobaek, T. J. Crease & H. Stibor, 1996. Molecular characterization of clonal population structure and biogeography of arctic apomictic Daphnia from Greenland and Iceland. Molecular Ecology 5: 107–118.

    CAS  PubMed  Google Scholar 

  • Weider, L. J. & A. Hobaek, 1997. Postglacial dispersal, glacial refugia, and clonal structure in Russian/Siberian populations of the Arctic Daphnia pulex complex. Heredity 78: 363–372.

    Article  Google Scholar 

  • Zhao, Y. & C. E. King, 1989. Ecological genetics of the rotifer Brachionus plicatilis in Soda Lake, Nevada, USA. Hydrobiologia 185: 175–181.

    Article  Google Scholar 

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Gómez, A. (2005). Molecular ecology of rotifers: from population differentiation to speciation. In: Herzig, A., Gulati, R.D., Jersabek, C.D., May, L. (eds) Rotifera X. Developments in Hydrobiology, vol 181. Springer, Dordrecht. https://doi.org/10.1007/1-4020-4408-9_7

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