Hydrobiologia

, Volume 796, Issue 1, pp 39–58 | Cite as

Fifteen species in one: deciphering the Brachionus plicatilis species complex (Rotifera, Monogononta) through DNA taxonomy

  • Scott Mills
  • J. Arturo Alcántara-Rodríguez
  • Jorge Ciros-Pérez
  • Africa Gómez
  • Atsushi Hagiwara
  • Kayla Hinson Galindo
  • Christian D. Jersabek
  • Reza Malekzadeh-Viayeh
  • Francesca Leasi
  • Jae-Seong Lee
  • David B. Mark Welch
  • Spiros Papakostas
  • Simone Riss
  • Hendrik Segers
  • Manuel Serra
  • Russell Shiel
  • Radoslav Smolak
  • Terry W. Snell
  • Claus-Peter Stelzer
  • Cuong Q. Tang
  • Robert L. Wallace
  • Diego Fontaneto
  • Elizabeth J. Walsh
ROTIFERA XIV

Abstract

Understanding patterns and processes in biological diversity is a critical task given current and rapid environmental change. Such knowledge is even more essential when the taxa under consideration are important ecological and evolutionary models. One of these cases is the monogonont rotifer cryptic species complex Brachionus plicatilis, which is by far the most extensively studied group of rotifers, is widely used in aquaculture, and is known to host a large amount of unresolved diversity. Here we collate a dataset of previously available and newly generated sequences of COI and ITS1 for 1273 isolates of the B. plicatilis complex and apply three approaches in DNA taxonomy (i.e. ABGD, PTP, and GMYC) to identify and provide support for the existence of 15 species within the complex. We used these results to explore phylogenetic signal in morphometric and ecological traits, and to understand correlation among the traits using phylogenetic comparative models. Our results support niche conservatism for some traits (e.g. body length) and phylogenetic plasticity for others (e.g. genome size).

Keywords

Biodiversity COI Cryptic species Evolution ITS1 Phylogenetic comparative methods Zooplankton 

Notes

Acknowledgments

We acknowledge support from the staff of the Department of Biological Sciences at the University of Texas at El Paso, especially B. Smith, T. Valenzuela, L. and L. Hamden. Two anonymous reviewers provided useful comments to improve an earlier draft of the manuscript. Funding was provided by UTEP’s Office of Research and Sponsored Projects, College of Science, Department of Biological Sciences, NSF DEB 1257068 (E. J. Walsh) and NSF DEB 1257116 (R. L. Wallace).

Supplementary material

10750_2016_2725_MOESM1_ESM.jpg (391 kb)
Supplementary Figure S1. ITS1 from BEAST (JPEG 392 kb)
10750_2016_2725_MOESM2_ESM.jpg (436 kb)
Supplementary Figure S2. ITS1 from PhyML (JPEG 436 kb)
10750_2016_2725_MOESM3_ESM.jpg (1.7 mb)
Supplementary Figure S3. COI from BEAST (JPEG 1704 kb)
10750_2016_2725_MOESM4_ESM.jpg (1.7 mb)
Supplementary Figure S4. COI from PhyML (JPEG 1710 kb)
10750_2016_2725_MOESM5_ESM.jpg (436 kb)
Supplementary Figure S5. RAxML on combined alignment (JPEG 437 kb)
10750_2016_2725_MOESM6_ESM.txt (102 kb)
Supplementary File S1. List of all 1273 isolates with accession numbers for COI and ITS1. For each isolate, the identification of unique sequences, and the attribution to the 15 species is reported. [GenBank accessions to be disclosed later] (TXT 103 kb)
10750_2016_2725_MOESM7_ESM.docx (95 kb)
Supplementary material 7 (DOCX 96 kb)
10750_2016_2725_MOESM8_ESM.txt (0 kb)
Supplementary File S3. Phylogeny of the 14 species with COI and ITS1 in newick format (TXT 1 kb)

References

  1. Appeltans, W., S. T. Ahyong, G. Anderson, M. V. Angel, T. Artois, N. Bailly, R. Bamber, A. Barber, I. Bartsch, A. Berta, M. Błażewicz-Paszkowycz, P. Bock, G. Boxshall, C. B. Boyko, S. Nunes Brandao, R. A. Bray, N. L. Bruce, S. D. Cairns, T.-Y. Chan, L. Cheng, A. G. Collins, T. Cribb, M. Curini-Galletti, F. Dahdouh-Guebas, P. J. F. Davie, M. N. Dawson, O. De Clerck, W. Decock, S. De Grave, N. J. de Voogd, D. P. Domning, C. C. Emig, C. Erséus, W. Eschmeyer, K. Fauchald, D. G. Fautin, S. W. Feist, C. H. J. M. Fransen, H. Furuya, O. Garcia-Alvarez, S. Gerken, D. Gibson, A. Gittenberger, S. Gofas, L. Gómez-Daglio, D. P. Gordon, M. D. Guiry, F. Hernandez, B. W. Hoeksema, R. R. Hopcroft, D. Jaume, P. Kirk, N. Koedam, S. Koenemann, J. B. Kolb, R. M. Kristensen, A. Kroh, G. Lambert, D. B. Lazarus, R. Lemaitre, M. Longshaw, J. Lowry, E. Macpherson, L. P. Madin, C. Mah, G. Mapstone, P. A. McLaughlin, J. Mees, K. Meland, C. G. Messing, C. E. Mills, T. N. Molodtsova, R. Mooi, B. Neuhaus, P. K. L. Ng, C. Nielsen, J. Norenburg, D. M. Opresko, M. Osawa, G. Paulay, W. Perrin, J. F. Pilger, G. C. B. Poore, P. Pugh, G. B. Read, J. D. Reimer, M. Rius, R. M. Rocha, J. I. Saiz-Salinas, V. Scarabino, B. Schierwater, A. Schmidt-Rhaesa, K. E. Schnabel, M. Schotte, P. Schuchert, E. Schwabe, H. Segers, C. Self-Sullivan, N. Shenkar, V. Siegel, W. Sterrer, S. Stöhr, B. Swalla, M. L. Tasker, E. V. Thuesen, T. Timm, M. A. Todaro, X. Turon, S. Tyler, P. Uetz, J. van der Land, B. Vanhoorne, L. P. van Ofwegen, R. W. M. van Soest, J. Vanaverbeke, G. Walker-Smith, T. C. Walter, A. Warren, G. C. Williams, S. P. Wilson & M. J. Costello, 2012. The magnitude of global marine species diversity. Current Biology 22: 2189–2202.CrossRefPubMedGoogle Scholar
  2. Alcántara-Rodríguez, J. A., J. Ciros-Pérez, E. Ortega-Mayagoitia, C. R. Serranía-Soto & E. Piedra-Ibarra, 2012. Local adaptation in populations of a Brachionus group plicatilis cryptic species inhabiting three deep crater lakes in Central Mexico. Freshwater Biology 57: 728–740.CrossRefGoogle Scholar
  3. Bickford, D., D. J. Lohman, N. S. Sodhi, P. K. Ng, R. Meier, K. Winker, K. K. Ingram & I. Das, 2007. Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22: 148–155.CrossRefPubMedGoogle Scholar
  4. Blomberg, S. P., T. Garland Jr & A. R. Ives, 2003. Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution 57: 717–745.CrossRefPubMedGoogle Scholar
  5. Brummitt, R. K. 2001. World Geographical Scheme for Recording Plant Distributions, 2 edn. International Working Group on Taxonomic Databases For Plant Sciences (TDWG).Google Scholar
  6. Butlin, R., J. Bridle & D. Schluter, 2009. Speciation and Patterns of Diversity. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  7. 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
  8. Campillo, S., E. M. García-Roger, M. J. Carmona, A. Gómez & M. Serra, 2009. Selection on life-history traits and genetic population divergence in rotifers. Journal of Evolutionary Biology 22: 2542–2553.CrossRefPubMedGoogle Scholar
  9. Carmona, M. J., N. Dimas-Flores, E. M. García-Roger & M. Serra, 2009. Selection of low investment in sex in a cyclically parthenogenetic rotifer. Journal of Evolutionary Biology 22: 1975–1983.CrossRefPubMedGoogle Scholar
  10. Charin, N. N., 1947. O novom vide kolovratki is roda Brachionus. Doklady Akademii Nauk SSSR 56: 107–108.Google Scholar
  11. 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.CrossRefGoogle Scholar
  12. Ciros-Pérez, J., M. J. Carmona & M. Serra, 2001b. Resource competition between sympatric sibling rotifer species. Limnology and Oceanography 46: 1511–1523.CrossRefGoogle Scholar
  13. Ciros-Pérez, J., M. J. Carmona, S. Lapesa & M. Serra, 2004. Predation as a factor mediating resource competition among rotifer sibling species. Limnology and Oceanography 49: 40–50.CrossRefGoogle Scholar
  14. Ciros-Pérez, J., E. Ortega-Mayagoitia & J. Alcocer, 2015. The role of ecophysiological and behavioral traits in structuring the zooplankton assemblage in a deep, oligotrophic, tropical lake. Limnology and Oceanography 60: 2158–2172.CrossRefGoogle Scholar
  15. Costello, M. J., S. Wilson & B. Houlding, 2012. Predicting total global species richness using rates of species description and estimates of taxonomic effort. Systematic Biology 61: 871–883.CrossRefPubMedGoogle Scholar
  16. Curini-Galletti, M., T. Artois, V. Delogu, W. H. De Smet, D. Fontaneto, U. Jondelius, F. Leasi, A. Martínez, I. Meyer-Wachsmuth, K. S. Nilsson, P. Tongiorgi, K. Worsaae & M. A. Todaro, 2012. Patterns of diversity in soft-bodied meiofauna: dispersal ability and body size matter. PloS One 7: e33801.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Dahms, H. U., A. Hagiwara & J. S. Lee, 2011. Ecotoxicology, ecophysiology, and mechanistic studies with rotifers. Aquatic Toxicology 101: 1–12.CrossRefPubMedGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. Dellicour, S. & J.-F. Flot, 2015. Delimiting species-poor data sets using single molecular markers: a study of barcode gaps, haplowebs and GMYC. Systematic Biology 64: 900–908.CrossRefPubMedGoogle Scholar
  20. Doyle, J. J., 1995. The irrelevance of allele tree topologies for species delimitation, and a non-topological alternative. Systematic Botany 20: 574–588.CrossRefGoogle Scholar
  21. 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
  22. Ezard, T. H. G., T. Fujisawa & T. G. Barraclough, 2009. splits: SPecies’ LImits by Threshold Statistics. http://R-Forge.R-project.org/projects/splits/.
  23. Flot, J.-F., A. Couloux & S. Tillier, 2010. Haplowebs as a graphical tool for delimiting species: a revival of Doyle’s field for recombination approach and its application to the coral genus Pocillopora in Clipperton. BMC Evolutionary Biology 10: 372.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Fontaneto, D., 2011. Biogeography of Microscopic Organisms: is Everything Small Everywhere?. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  25. Fontaneto, D., 2014. Molecular phylogenies as a tool to understand diversity in rotifers. International Review of Hydrobiology 99: 178–187.CrossRefGoogle Scholar
  26. Fontaneto, D., G. F. Ficetola, R. Ambrosini & C. Ricci, 2006. Patterns of diversity in microscopic animals: are they comparable to those in protists or in larger animals? Global Ecology and Biogeography 15: 153–162.CrossRefGoogle Scholar
  27. 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
  28. 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
  29. Fontaneto, D., C. Q. Tang, U. Obertegger, F. Leasi F. & T. G. Barraclough, 2012. Different diversification rates between sexual and asexual organisms. Evolutionary Biology 39: 262–270Google Scholar
  30. Fontaneto, D., J.-F. Flot & C. Q. Tang, 2015. Guidelines for DNA taxonomy with a focus on the meiofauna. Marine Biodiversity 45: 433–451.CrossRefGoogle Scholar
  31. Fujisawa, T. & T. G. Barraclough, 2013. Delimiting species using single-locus data and the generalized mixed Yule coalescent (GMYC) approach: a revised method and evaluation on simulated datasets. Systematic Biology 62: 707–724.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Fukusho, K., 1983. Present status and problems in culture of the rotifer Brachionus plicatilis for fry production of marine fishes in Japan. In Hector, R. (ed.), Symposium Internacionale de Aquaculture, Coquimbo: 361–374Google Scholar
  33. Fu, Y., K. Hirayama & Y. Natsukari, 1991a. Morphological differences between two types of the rotifer Brachionus plicatilis O.F. Muller. Journal of Experimental Marine Biology and Ecology 151: 29–41.CrossRefGoogle Scholar
  34. Fu, Y., K. Hirayama & Y. Natsukari, 1991b. Genetic divergence between S and L type strains of the rotifer Brachionus plicatilis O.F. Muller. Journal of Experimental Marine Biology and Ecology 151: 43–56.CrossRefGoogle Scholar
  35. Fu, Y., A. Hagiwara & K. Hirayama, 1993. Crossing between seven strains of the rotifer Brachionus plicatilis. Nippon Suisan Gakkaishi 59: 2009–2016.CrossRefGoogle Scholar
  36. Gabaldón, C., M. J. Carmona, J. Montero-Pau & M. Serra, 2015. Long-term competitive dynamics of two cryptic rotifer species: diapause and fluctuating conditions. PloS One 10: e0124406.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Gabaldón, C., D. Fontaneto, J. Montero-Pau, M. J. Carmona & M. Serra, 2016, Ecological differentiation in cryptic rotifer species: what we can learn from the B. plicatilis complex. Hydrobiologia. doi:10.1007/s10750-016-2723-9.
  38. Garamszegi, L. Z., 2014. Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology. Springer, Berlin.CrossRefGoogle Scholar
  39. García-Morales, A. E. & M. Elías-Gutiérrez, 2013. DNA barcoding of freshwater Rotifera in Mexico: Evidence of cryptic speciation in common rotifers. Molecular Ecology Resources 13: 1097–1107.PubMedGoogle Scholar
  40. Gilbert, J. J. & R. S. Stemberger, 1984. Asplanchna-induced polymorphism in the rotifer Keratella slacki. Limnology and Oceanography 29: 1309–1316.CrossRefGoogle Scholar
  41. Gómez, A. & M. Serra, 1995. Behavioral reproductive isolation among sympatric strains of Brachionus plicatilis Müller 1786: insights into the status of this taxonomic species. Hydrobiologia 313: 111–119.CrossRefGoogle Scholar
  42. Gómez, A. & T. W. Snell, 1996. Sibling species in the Brachionus plicatilis species complex. Journal of Evolutionary Biology 9: 953–964.CrossRefGoogle Scholar
  43. 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
  44. 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 B: Biological Sciences 267: 2189–2197.CrossRefGoogle Scholar
  45. 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
  46. Gómez, A., J. Montero-Pau, D. H. Lunt, M. Serra & S. Campillo, 2007. Persistent genetic signatures of colonization in Brachionus manjavacas rotifers in the Iberian Peninsula. Molecular Ecology 16: 3228–3240.CrossRefPubMedGoogle Scholar
  47. Guidon, S. & O. Gascuel, 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696–704.CrossRefGoogle Scholar
  48. 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 B: Biological Sciences 270: 313–321.CrossRefGoogle Scholar
  49. Hwang, D. S., H. U. Dahms, H. G. Park & J. S. Lee, 2013. A new intertidal Brachionus and intrageneric phylogenetic relationships among Brachionus as revealed by allometry and CO1-ITS1 gene analysis. Zoological Studies 52: 1–10.CrossRefGoogle Scholar
  50. Jersabek, C. D. & E. Bolortsetseg, 2010. Mongolian rotifers (Rotifera, Monogononta)–a checklist with annotations on global distribution and autecology. Proceedings of the Academy of Natural Sciences of Philadelphia 159: 119–168.CrossRefGoogle Scholar
  51. Kamilar, J. M. & N. Cooper, 2013. Phylogenetic signal in primate behaviour, ecology and life history. Philosophical Transactions of the Royal Society B 368: 20120341.CrossRefGoogle Scholar
  52. Katoh, K., G. Asimenos & H. Toh, 2009. Multiple alignment of DNA sequences with MAFFT. Methods in Molecular Biology 537: 39–64.CrossRefPubMedGoogle Scholar
  53. Keane, T. M., C. J. Creevey, M. M. Pentony, T. J. Naughton & J. O. Mclnerney, 2006. Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evolutionary Biology 6: 29.CrossRefPubMedPubMedCentralGoogle Scholar
  54. King, C. E. & Y. Zhao, 1987. Coexistence of rotifer (Brachionus plicatilis) clones in Soda Lake, Nevada. Hydrobiologia 147: 57–64.CrossRefGoogle Scholar
  55. Knowlton, N., 1993. Sibling species in the sea. Annual Review of Ecology and Systematics 24: 189–216.CrossRefGoogle Scholar
  56. Kutikova, L.A., 1970 Rotifer Fauna USSR. Fauna USSR. 104. Leningrad: Akademii Nauk SSSRGoogle Scholar
  57. Lowe, C. D., S. J. Kemp, A. D. Bates & D. J. S. Montagnes, 2005. Evidence that the rotifer Brachionus plicatilis is not an osmoconformer. Marine Biology 146: 923–929.CrossRefGoogle Scholar
  58. Lubzens, E. & O. Zmora, 2003. Production and nutritional value of rotifers. In McEvoy, L. A. (ed.), Live Feeds in Marine Aquaculture. Blackwell, Oxford: 17–64.CrossRefGoogle Scholar
  59. Malekzadeh-Viayeh, R., R. Pak-Tarmani, N. Rostamkhani & D. Fontaneto, 2014. Diversity of the rotifer Brachionus plicatilis species complex (Rotifera: Monogononta) in Iran through integrative taxonomy. Zoological Journal of the Linnean Society 170: 233–244.CrossRefGoogle Scholar
  60. Mayr, E., 1963. Animal Species and Evolution. Belknap Press of Harvard University Press, Cambridge.CrossRefGoogle Scholar
  61. Mills, S., A. Gómez & D. H. Lunt, 2007. Global isolation by distance despite strong regional phylogeography in a small metazoan. BMC Evolutionary Biology 7: 225.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Montero-Pau, J., E. Ramos-Rodríguez, M. Serra & A. Gómez, 2011. Long-term coexistence of rotifer cryptic species. PloS ONE 6: e21530.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Müller, O. F., 1786. Animacula infusoria fluviatilia et marina, quae detexit, systematice descripsit et ad vivum delineari curavit. Havniae [Copenhagen] et Lipsiae [Leipzig]: cura Othonis Fabricii, typis Nicolai Mölleri.Google Scholar
  64. Münkemüller, T., S. Lavergne, B. Bzeznik, S. Dray, T. Jombart, K. Schiffers & W. Thuiller, 2012. How to measure and test phylogenetic signal. Methods in Ecology and Evolution 3: 743–756.CrossRefGoogle Scholar
  65. Obertegger, U., G. Flaim & D. Fontaneto, 2014. Cryptic diversity within the rotifer Polyarthra dolichoptera along an altitudinal gradient. Freshwater Biology 59: 2413–2427.CrossRefGoogle Scholar
  66. Oogami, H., 1976. On the morphology of Brachionus plicatilis. Newsletter from Izu Branch, Shizuoka Prefectural Fisheries Research Center 184: 2–5.Google Scholar
  67. Orme, C. D. L., R. Freckleton, G. Thomas, T. Petzoldt, S. Fritz, N. Isaac, W. Pearse, 2013. Caper: comparative analyses of phylogenetics and evolution in R. R package version 0.5.2. http://CRAN.R-project.org/package=caper.
  68. 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 für Hydrobiologie 149: 529–551.CrossRefGoogle Scholar
  69. Ortells, R., A. Gómez & M. Serra, 2003. Coexistence of cryptic rotifer species: ecological and genetic characterisation of Brachionus plicatilis. Freshwater Biology 48: 2194–2202.CrossRefGoogle Scholar
  70. Pagel, M., 1999. Inferring the historical patterns of biological evolution. Nature 401: 877–884.CrossRefPubMedGoogle Scholar
  71. Papakostas, S., E. Michaloudi, K. Proios, M. Brehm, L. Verhage, J. Rota, C. Pena, G. Stamou, V. L. Pritchard, D. Fontaneto & S. A. J. Declerck, 2016. Integrative taxonomy recognizes evolutionary units despite widespread mitonuclear discordance: evidence from a rotifer cryptic species complex. Systematic Biology. doi:10.1093/sysbio/syw016.
  72. Paradis, E., J. Claude & K. Strimmer, 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290.CrossRefPubMedGoogle Scholar
  73. Pfenninger, M. & K. Schwenk, 2007. Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology 7: 121.CrossRefPubMedPubMedCentralGoogle Scholar
  74. Puillandre, N., A. Lambert, S. Brouillet & G. Achaz, 2012. ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology 21: 1864–1877.CrossRefPubMedGoogle Scholar
  75. R Core Team, 2014. R: a Language and Environment for Statistical Computing. R Core Team. R Foundation for Statistical Computing, ViennaGoogle Scholar
  76. Rambaut, A., M. A. Suchard, D. Xie & A. J. Drummond, 2013. Tracer v1.5. http://beast.bio.ed.ac.uk/tracer.
  77. Revell, L. J., 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3: 217–223.CrossRefGoogle Scholar
  78. Rumengan, I. F. M., H. Kayano & K. Hirayama, 1991. Karyotypes of S and L type rotifers Brachionus plicatilis OF Müller. Journal of Experimental Marine Biology and Ecology 154: 171–176.CrossRefGoogle Scholar
  79. Rumengan, I. F. M., Y. Fu, H. Kayano & K. Hirayama, 1993. Chromosomes and isozymes of hypotriploid strains of the rotifer Brachionus plicatilis. Hydrobiologia 255: 213–217.CrossRefGoogle Scholar
  80. Sanderson, M. J., 2003. r8 s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19: 301–302.CrossRefPubMedGoogle Scholar
  81. Sarma, S. S. S., R. A. L. Resendiz & S. Nandini, 2011. Morphometric and demographic responses of brachionid prey (Brachionus calyciflorus Pallas and Plationus macracanthus (Daday)) in the presence of different densities of the predator Asplanchna brightwellii (Rotifera: Asplanchnidae). Hydrobiologia 662: 179–187.CrossRefGoogle Scholar
  82. Segers, H., 1995. Nomenclatural consequences of some recent studies on Brachionus plicatilis (Rotifera, Brachionidae). Hydrobiologia 313(314): 121–122.CrossRefGoogle Scholar
  83. Segers, H. & W. H. De Smet, 2008. Diversity and endemism in Rotifera: a review, and Keratella Bory de St Vincent. Biodiversity and Conservation 17: 303–316.CrossRefGoogle Scholar
  84. Serra, M. & M. R. Miracle, 1983. Biometric analysis of Brachionus plicatilis ecotypes from Spanish lagoons. Hydrobiologia 104: 279–291.CrossRefGoogle Scholar
  85. Serra, M. & M. R. Miracle, 1987. Biometric variation in three strains of Brachionus plicatilis as a direct response to abiotic variables. Hydrobiologia 147: 83–89.CrossRefGoogle Scholar
  86. Serra, M., A. Gómez & M. J. Carmona, 1998. Ecological genetics of Brachionus sympatric sibling species. Hydrobiologia 387: 373–384.CrossRefGoogle Scholar
  87. Serrano, L., M. R. Miracle & M. Serra, 1986. Differential response of Brachionus plicatilis (Rotifera) ecotypes to various insecticides. Journal of Environmental Biology 7: 259–275.Google Scholar
  88. Serrano, L., M. Serra & M. R. Miracle, 1989. Size variation in Brachionus plicatilis resting eggs. Hydrobiologia 186(187): 381–386.CrossRefGoogle Scholar
  89. Snell, T. W., 1989. Systematics, reproductive isolation and species boundaries in rotifers. Hydrobiologia 186(187): 299–310.CrossRefGoogle Scholar
  90. Snell, T. W., 1998. Chemical ecology of rotifers. Hydrobiologia 387(388): 267–276.CrossRefGoogle Scholar
  91. Snell, T. W. & K. Carrillo, 1984. Body size variation among strains of the rotifer Brachionus plicatilis. Aquaculture 37: 359–367.CrossRefGoogle Scholar
  92. Snell, T. W. & C. A. Hawkinson, 1983. Behavioral reproductive isolation among populations of the rotifer Brachionus plicatilis. Evolution 37: 1294–1305.CrossRefPubMedGoogle Scholar
  93. Snell, T. W. & G. Persoone, 1989. Acute toxicity bioassays using rotifers. I. A test for brackish and marine environments with Brachionus plicatilis. Aquatic Toxicology 14: 65–80.CrossRefGoogle Scholar
  94. Snell, T. W., R. K. Johnston, K. E. Gribble & D. B. Mark Welch, 2015. Rotifers as experimental tools for investigating aging. Invertebrate Reproduction & Development 59: 5–10.CrossRefGoogle Scholar
  95. Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.CrossRefPubMedPubMedCentralGoogle Scholar
  96. 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
  97. 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
  98. Tang, C. Q., F. Leasi, U. Obertegger, A. Kieneke, T. G. Barradough & 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
  99. Tang, C. Q., U. Obertegger, D. Fontaneto & T. G. Barraclough, 2014a. Sexual species are separated by larger genetic gaps than asexual species in rotifers. Evolution 68: 2901–2916.CrossRefPubMedPubMedCentralGoogle Scholar
  100. Tang, C. Q., A. Humphreys, D. Fontaneto & T. G. Barraclough, 2014b. Effects of phylogenetic reconstruction method on the robustness of species delimitation using single locus data. Methods in Ecology and Evolution 5: 1086–1094.CrossRefPubMedPubMedCentralGoogle Scholar
  101. Trontelj, P. & C. Fiser, 2009. Cryptic species diversity should not be trivialised. Systematics and Biodiversity 7: 1–3.CrossRefGoogle Scholar
  102. Tschugunoff, N. L., 1921. Über das Plankton des nördlichen Teiles des Kaspisees. Raboty Volzhskoj Biologicheskoj Stancii, Saratov 6: 159–162.Google Scholar
  103. Wallace, R. L., T. W. Snell, C. Ricci & T. Nogrady, 2006. Rotifera. Vol. 1. Biology, ecology and systematics. In Dumont, H. J. F. (eds), Guides to the Identification of the Microinvertebrates of the Continental Waters of the World, Vol. 23, 2nd ed. Ghent, Kenobi Productions: 1–299.Google Scholar
  104. Watanabe, T., C. Kitajima & S. Fujita, 1983. Nutritional values of live organisms used in Japan for mass propagation of fish: a review. Aquaculture 34: 115–143.CrossRefGoogle Scholar
  105. Wiens, J. J. & C. H. Graham, 2005. Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics 36: 519–539.CrossRefGoogle Scholar
  106. Xiang, X. L., Y. L. Xi, X. L. Wen, G. Zhang, J. X. Wang & K. Hu, 2011. Genetic differentiation and phylogeographical structure of the Brachionus calyciflorus complex in eastern China. Molecular Ecology 20: 3027–3044.CrossRefPubMedGoogle Scholar
  107. Zhang, J., P. Kapli, P. Pavlidis & A. Stamatakis, 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Scott Mills
    • 1
  • J. Arturo Alcántara-Rodríguez
    • 2
  • Jorge Ciros-Pérez
    • 2
  • Africa Gómez
    • 3
  • Atsushi Hagiwara
    • 4
  • Kayla Hinson Galindo
    • 5
  • Christian D. Jersabek
    • 6
  • Reza Malekzadeh-Viayeh
    • 7
  • Francesca Leasi
    • 8
  • Jae-Seong Lee
    • 9
  • David B. Mark Welch
    • 10
  • Spiros Papakostas
    • 11
  • Simone Riss
    • 12
  • Hendrik Segers
    • 13
  • Manuel Serra
    • 14
  • Russell Shiel
    • 15
  • Radoslav Smolak
    • 16
  • Terry W. Snell
    • 17
  • Claus-Peter Stelzer
    • 12
  • Cuong Q. Tang
    • 18
  • Robert L. Wallace
    • 19
  • Diego Fontaneto
    • 20
  • Elizabeth J. Walsh
    • 5
  1. 1.James Cook UniversityTownsvilleAustralia
  2. 2.Proyecto de Investigación en Limnología Tropical, FES IztacalaUniversidad Nacional Autónoma de MéxicoMexico CityMexico
  3. 3.School of Biological, Biomedical and Environmental SciencesUniversity of HullHullUK
  4. 4.Graduate School of Fisheries and Environmental SciencesNagasaki UniversityNagasakiJapan
  5. 5.Department of Biological SciencesUniversity of Texas at El PasoEl PasoUSA
  6. 6.Department of Organismal BiologyUniversity of SalzburgSalzburgAustria
  7. 7.Artemia and Aquatic Research InstituteUrmia UniversityUrmiaIran
  8. 8.Department of Invertebrate ZoologySmithsonian National Museum of Natural HistoryWashingtonUSA
  9. 9.Department of Biological Science, College of ScienceSungkyunkwan UniversitySuwonSouth Korea
  10. 10.Josephine Bay Paul Center for Comparative Molecular Biology and EvolutionMarine Biological LaboratoryWoods HoleUSA
  11. 11.Division of Genetics and Physiology, Department of BiologyUniversity of TurkuTurkuFinland
  12. 12.Research Institute for LimnologyUniversity of InnsbruckMondseeAustria
  13. 13.OD NatureRoyal Belgian Institute of Natural SciencesBrusselsBelgium
  14. 14.Institut Cavanilles de Biodiversitat i Biologia EvolutivaUniversitat de ValènciaValenciaSpain
  15. 15.Biological SciencesUniversity of AdelaideAdelaideAustralia
  16. 16.Department of Ecology, Faculty of Humanities and Natural SciencesPresov UniversityPresovSlovakia
  17. 17.School of BiologyGeorgia Institute of TechnologyAtlantaUSA
  18. 18.Department of Life SciencesThe Natural History MuseumLondonUK
  19. 19.Department of BiologyRipon CollegeRiponUSA
  20. 20.Institute of Ecosystem StudyNational Research Council of ItalyVerbania PallanzaItaly

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