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
J. C. Avise (2000) Phylogeography: The History and Formation of Species Harvard University Press Cambridge, Massachusetts 447
S. A. Bailey I. C. Duggan C. D. A. Overdijk Particlevan P. T. Jenkins H. J. MacIsaac (2003) ArticleTitleViability of invertebrate diapausing eggs collected from residual ballast water Limnology and Oceanography 48 1701–1710
D. A. Baum K. L. Shaw (1995) Genealogical perspectives on the species problem P. C. Hoch A. G. Stephenson (Eds) Experimental and Molecular Approaches to Plant Biosystematics Missouri Botanical Garden Columbia, Missouri 289–303
H. K. Berrieman D. H. Lunt A. Gómez (2005) ArticleTitleBehavioural reproductive isolation in a rotifer hybrid zone Hydrobiologia 546 125–134
C. W. Birky P. Fuerst T. Maruyama (1989) ArticleTitleOrganelle 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 Occurrence Handle2714640
C. W. Birky (2001) ArticleTitleThe inheritance of genes in mitochondria and chloroplasts: Laws, mechanisms, and models Annual Review of Genetics 35 125–148 Occurrence Handle10.1146/annurev.genet.35.102401.090231 Occurrence Handle11700280
T. B. Birt A. J. Baker (2000) Polymerase Chain Reaction A. J. Baker (Eds) Molecular Methods in Ecology Blackwell Science Oxford 50–64
R. W. Black L. B. Slobodkin (1987) ArticleTitleWhat is cyclomorphosis Freshwater Biology 18 373–378
M. G. Boileau P. D. N. Hebert S. S. Schwartz (1992) ArticleTitleNonequilibrium gene frequency divergence – persistent founder effects in natural populations Journal of Evolutionary Biology 5 25–39 Occurrence Handle10.1046/j.1420-9101.1992.5010025.x
R. T. Brumfield P. Beerli D. A. Nickerson S. V. Edwards (2003) ArticleTitleThe utility of single nucleotide polymorphisms in inferences of population history Trends in Ecology & Evolution 18 249–256
C. E. Cáceres (1997) ArticleTitleTemporal 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 Occurrence Handle10.1073/pnas.94.17.9171 Occurrence Handle11038565
G. R. Carvalho (1998) Advances in Molecular Ecology IOS Press Amsterdam 313
J. Ciros-Pérez M. J. Carmona M. Serra (2001) ArticleTitleResource competition between sympatric sibling rotifer species Limnology and Oceanography 46 1511–1523
J. Ciros-Pérez A. Gómez M. Serra (2001) ArticleTitleOn 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 Occurrence Handle10.1093/plankt/23.12.1311
C. Cousyn L. Meester J. K. Colbourne L. Brendonck D. Verschuren F. Volckaert (2001) ArticleTitleRapid, 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 Occurrence Handle10.1073/pnas.111606798 Occurrence Handle11353872
L. Meester ParticleDe (1996) ArticleTitleLocal genetic differentiation and adaptation in freshwater zooplankton: patterns and processes Ecoscience 3 385–399
L. Meester ParticleDe A. Gómez B. Okamura K. Schwenk (2002) ArticleTitleThe Monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms Acta Oecologica 23 121–135 Occurrence Handle10.1016/S1146-609X(02)01145-1
A. M. Derry P. D. N. Hebert E. E. Prepas (2003) ArticleTitleEvolution of rotifers in saline and subsaline lakes: A molecular phylogenetic approach Limnology and Oceanography 48 675–685
H. J. Dumont (1983) ArticleTitleBiogeography of rotifers Hydrobiologia 104 19–30 Occurrence Handle10.1007/BF00045948
D. Ebert C. Haag M. Kirkpatrick M. Riek J. W. Hottinger V. I. Pajunen (2002) ArticleTitleA selective advantage to immigrant genes in a Daphnia metapopulation Science 295 485–488 Occurrence Handle10.1126/science.1067485 Occurrence Handle11799241
O. Folmer M. Black W. Hoeh R. Lutz R. Vrijenhoek (1994) ArticleTitleDNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates Molecular Marine Biology and Biotechnology 3 294–299 Occurrence Handle7881515
G. Fussmann S. Ellner N. Stasio ParticleDe SuffixJr (2003) ArticleTitleMicroevolution as a critical component of plankton dynamics Proceedings of the Royal Society of London Series B-Biological Sciences 270 1015–1022 Occurrence Handle10.1098/rspb.2003.2335
J. J. Gilbert (2001) ArticleTitleSpine development in Brachionus quadridentatus from an Australian billabong: genetic variation and induction by Asplanchna Hydrobiologia 446 19–28
J. J. Gilbert E. J. Walsh (2005) ArticleTitleBrachionus calyciflorus is a species complex: Mating behaviour and genetic differentation among four geographically isolated strains Hydrobiologia 546 257–265
D. B. Goldstein C. Schlotterer (1999) Microsatellites: Evolution and Applications Oxford University Press Oxford 352
A. Gómez M. Serra (1995) ArticleTitleBehavioral reproductive isolation among sympatric strains of Brachionus plicatilis Muller 1786: Insights into the status of this taxonomic species Hydrobiologia 313 111–119 Occurrence Handle10.1007/BF00025938
A. Gómez M. Temprano M. Serra (1995) ArticleTitleEcological genetics of a cyclical parthenogen in temporary habitats Journal of Evolutionary Biology 8 601–622 Occurrence Handle10.1046/j.1420-9101.1995.8050601.x
A. Gómez T. W. Snell (1996) ArticleTitleSibling species and cryptic speciation in the Brachionus plicatilis species complex (Rotifera) Journal of Evolutionary Biology 9 953–964 Occurrence Handle10.1046/j.1420-9101.1996.9060953.x
A. Gómez M. J. Carmona M. Serra (1997) ArticleTitleEcological factors affecting gene flow in the Brachionus plicatilis complex (Rotifera) Oecologia 111 350–356 Occurrence Handle10.1007/s004420050245
A. Gómez (1998) ArticleTitleAllozyme electrophoresis: its application to rotifers Hydrobiologia 387/388 385–393 Occurrence Handle10.1023/A:1017075503161
A. Gómez C. Clabby G. R. Carvalho (1998) ArticleTitleIsolation and characterization of microsatellite loci in a cyclically parthenogenetic rotifer, Brachionus plicatilis Molecular Ecology 7 1619–1621 Occurrence Handle9819915
A. Gómez G. R. Carvalho (2000) ArticleTitleSex, parthenogenesis and genetic structure of rotifers: microsatellite analysis of contemporary and resting egg bank populations Molecular Ecology 9 203–214 Occurrence Handle10.1046/j.1365-294x.2000.00849.x Occurrence Handle10672164
A. Gómez G. R. Carvalho D. H. Lunt (2000) ArticleTitlePhylogeography 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 Occurrence Handle10.1098/rspb.2000.1268
A. Gómez G. J. Adcock D. H. Lunt G. R. Carvalho (2002a) ArticleTitleThe 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 Occurrence Handle10.1046/j.1420-9101.2002.00368.x
A. Gómez M. Serra G. R. Carvalho D. H. Lunt (2002b) ArticleTitleSpeciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera) Evolution 56 1431–1444
C. R. Haag J. W. Hottinger M. Riek D. Ebert (2002) ArticleTitleStrong inbreeding depression in a Daphnia metapopulation Evolution 56 518–526 Occurrence Handle11989682
P. D. N. Hebert A. Cywinska S. L. Ball J. R. DeWaard (2003) ArticleTitleBiological identifications through DNA barcodes Proceedings of the Royal Society of London Series B-Biological Sciences 270 313–321 Occurrence Handle10.1098/rspb.2002.2218
W. Hofmann (1983) ArticleTitleOn temporal variation in the rotifer Keratella cochlearis (Gosse) – the question of Lauterborn-cycles Hydrobiologia 101 247–254
P. Jarne P. J. L. Lagoda (1996) ArticleTitleMicrosatellites, from molecules to populations and back Trends in Ecology & Evolution 11 424–429
D. G. Jenkins A. L. Buikema SuffixJr. (1998) ArticleTitleDo similar communities develop in similar sites? a test with zooplankton structure and function Ecological Monographs 68 421–443
C. E. King (1977) ArticleTitleGenetics of reproduction, variation and adaptation in rotifers Archiv für Hydrobiologie. Ergebnisse der Limnologie 8 187–201
C. E. King (1980) The genetic structure of zooplankton communities W. C. Kerfoot (Eds) Evolution and Ecology of Zooplankton Communities The University Press of New England Hanover (N.H.) 315–328
N. Knowlton (2000) ArticleTitleMolecular genetic analyses of species boundaries in the sea Hydrobiologia 420 73–90 Occurrence Handle10.1023/A:1003933603879
C. Leutbecher (2000) ArticleTitleA routine method of DNA-extraction from extremely small metazoans, e.g. single rotifer specimens for RAPD-PCR analyses Hydrobiologia 437 133–137 Occurrence Handle10.1023/A:1026546705582
Y. C. Li A. B. Korol T. Fahima A. Beiles E. Nevo (2002) ArticleTitleMicrosatellites: genomic distribution, putative functions and mutational mechanisms: a review Molecular Ecology 11 2453–2465 Occurrence Handle10.1046/j.1365-294X.2002.01643.x Occurrence Handle12453231
M. Lynch M. Pfrender K. Spitze N. Lehman J. Hicks D. Allen L. Latta M. Ottene F. Bogue J. Colbourne (1999) ArticleTitleThe quantitative and molecular genetic architecture of a subdivided species Evolution 53 100–110
D. B. Mark Welch M. Meselson (2000) ArticleTitleEvidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange Science 288 1211–1215 Occurrence Handle10817991
K. K. Morgan J. Hicks K. Spitze L. Latta M. E. Pfrender C. S. Weaver M. Ottone M. Lynch (2001) ArticleTitlePatterns of genetic architecture for life-history traits and molecular markers in a subdivided species Evolution 55 1753–1761 Occurrence Handle11681731
R. Ortells T. W. Snell A. Gómez M. Serra (2000) ArticleTitlePatterns of genetic differentiation in resting egg banks of a rotifer species complex in Spain Archiv für Hydrobiologie 149 529–551
R. Ortells (2002) Diversidad Genética y Ecológica en Especies Crípticas de Rotíferos Patrones y Procesos, Universitat de Valencia Valencia, Spain 193
R. Ortells A. Gómez M. Serra (2003) ArticleTitleCoexistence of rotifer cryptic species: ecological and genetic characterisation of Brachionus plicatilis Freshwater Biology 48 2194–2202 Occurrence Handle10.1046/j.1365-2427.2003.01159.x
S. R. Palumbi (1996) The Polymerase Chain Reaction D. M. Hillis C. B. K. Moritz Marble (Eds) Molecular Systematics Sinauer Sunderland, MA 205–247
M. E. Pfrender K. Spitze N. Lehman (2000) ArticleTitleMulti-locus genetic evidence for rapid ecologically based speciation in Daphnia Molecular Ecology 9 1717–1735 Occurrence Handle10.1046/j.1365-294x.2000.01062.x Occurrence Handle11091309
C. R. Primmer A. P. Moller H. Ellegren (1996) ArticleTitleA wide-range survey of cros-species microsatellite amplification in birds Molecular Ecology 5 365–378 Occurrence Handle10.1046/j.1365-294X.1996.00092.x Occurrence Handle8688957
C. R. Primmer J. Merila (2002) ArticleTitleA low rate of microsatellite amplification success in Ranid frogs Conservation Genetics 3 445–449 Occurrence Handle10.1023/A:1020519218836
F. J. Rahel (2002) ArticleTitleHomogenisation of freshwater faunas Annual Review of Ecology and Systematics 33 291–315 Occurrence Handle10.1146/annurev.ecolsys.33.010802.150429
H. Segers (1996) ArticleTitleBiogeography of littoral Lecane Rotifera Hydrobiologia 323 169–197 Occurrence Handle10.1007/BF00007845
H. Segers (2002) ArticleTitleThe nomenclature of the Rotifera: annotated checklist of valid family- and genus-group names Journal of Natural History 36 631–640 Occurrence Handle10.1080/002229302317339707
M. Serra M. J. Carmona M. R. Miracle (1994) ArticleTitleSurvival analysis of 3 clones of Brachionus plicatilis (Rotifera) Hydrobiologia 277 97–105
M. Serra A. Galiana A. Gómez (1997) ArticleTitleSpeciation in monogonont rotifers Hydrobiologia 358 63–70 Occurrence Handle10.1023/A:1003155617297
M. Serra A. Gómez M. J. Carmona (1998) ArticleTitleEcological genetics of Brachionus sympatric sibling species Hydrobiologia 388 373–384 Occurrence Handle10.1023/A:1017083820908
J. B. Shurin (2000) ArticleTitleDispersal limitation, invasion resistance and the structure of pond zooplankton populations Ecology 81 3074–3086
T. W. Snell K. Carrillo (1984) ArticleTitleBody size variation among strains of the rotifer Brachionus plicatilis Aquaculture 37 359–367 Occurrence Handle10.1016/0044-8486(84)90300-4
P. Stenberg M. Lundmark A. Saura (2003) ArticleTitleMLGsim: a program for detecting clones using a simulation approach Molecular Ecology Notes 3 329–331 Occurrence Handle10.1046/j.1471-8286.2003.00408.x
P. Sunnucks A. C. C. Wilson L. B. Behegaray L. B. Zenger J. French A. C. Taylor (2000) ArticleTitleSSCP is not that difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and molecular ecology Molecular Ecology 9 1699–1710 Occurrence Handle10.1046/j.1365-294x.2000.01084.x Occurrence Handle11091307
D. Tautz P. Arctander A. Minelli R. H. Thomas A. P. Vogler (2003) ArticleTitleA plea for DNA taxonomy Trends in Ecology & Evolution 18 70–74
D. J. Taylor P. D. N. Hebert J. K. Colbourne (1996) ArticleTitlePhylogenetics and evolution of the Daphnia longispina group (Crustacea) based on 12S rDNA sequence and allozyme variation Molecular Phylogenetics and Evolution 5 495–510 Occurrence Handle10.1006/mpev.1996.0045 Occurrence Handle8744763
A. R. Templeton (1998) ArticleTitleNested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history Molecular Ecology 7 381–397 Occurrence Handle10.1046/j.1365-294x.1998.00308.x Occurrence Handle9627999
P. Vos R. Hogers M. Bleeker M. Reijans T. Lee M. Hornes A. Fritjers J. Pot J. Peleman M. Kuiper M. Zabeau (1995) ArticleTitleAFLP: a new technique for DNA fingerprinting Nucleic Acids Research 23 4407–4414 Occurrence Handle7501463
P. S. Walsh D. A. Metzger R. Higuchi (1991) ArticleTitleChelex-100 as a Medium for Simple Extraction of DNA for Pcr- Based Typing from Forensic Material Biotechniques 10 506–513 Occurrence Handle1867860
R. K. Wayne J. A. Leonard A. Cooper (1999) ArticleTitleFull of sound and fury: the recent history of ancient DNA Annual Review of Ecology and Systematics 30 457–477 Occurrence Handle10.1146/annurev.ecolsys.30.1.457
L. J. Weider A. Hobaek T. J. Crease H. Stibor (1996) ArticleTitleMolecular characterization of clonal population structure and biogeography of arctic apomictic Daphnia from Greenland and Iceland Molecular Ecology 5 107–118 Occurrence Handle9147686
L. J. Weider A. Hobaek (1997) ArticleTitlePostglacial dispersal, glacial refugia, and clonal structure in Russian/Siberian populations of the Arctic Daphnia pulex complex Heredity 78 363–372 Occurrence Handle10.1038/sj.hdy.6881290
Y. Zhao C. E. King (1989) ArticleTitleEcological genetics of the rotifer Brachionus plicatilis in Soda Lake, Nevada, USA Hydrobiologia 185 175–181 Occurrence Handle10.1007/BF00036605
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Gómez, A. Molecular Ecology of Rotifers: From Population Differentiation to Speciation. Hydrobiologia 546, 83–99 (2005). https://doi.org/10.1007/s10750-005-4104-7
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DOI: https://doi.org/10.1007/s10750-005-4104-7