Cryptic diversity with wide salinity tolerance in the putative euryhaline Testudinella clypeata (Rotifera, Monogononta)

Zoological Journal of the Linnean Society

Volumn 168, Issue 1, 2013, Pages 17-28

  Leasi, Francesca ^a,b   Tang, Cuong Q ^b   De Smet, Willem H ^c   Fontaneto, Diego ^b,d  

^a ACADEMY OF NATURAL SCIENCES OF DREXEL UNIVERSITY   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d CNR   (Italy)

Author keywords

DNA taxonomy; Ecological distribution; Ecological tolerance; Generalized mixed Yule coalescent (GMYC) model; Geographical distribution; Meiofauna; Microscopic organisms; Salt waters; Traditional taxonomy

Indexed keywords

ANIMALIA; BRACHIONUS PLICATILIS; MONOGONONTA; ROTIFERA; TESTUDINELLA CLYPEATA;

EID: 84875942703     PISSN: 00244082     EISSN: 10963642     Source Type: Journal    
DOI: 10.1111/zoj.12020     Document Type: Article

References (54)

1. Birky CW, Adams J, Gemmel M, Perry J. 2010. Using population genetic theory and DNA sequences for species detection and identification in asexual organisms. PLoS ONE 5: e10609.
2. Birky CW, Wolf C, Maughan H, Herbertson L, Henry E. 2005. Speciation and selection without sex. Hydrobiologia 546: 29-45.
3. Bledzki LA, Ellison AM. 2003. Diversity of rotifers from northeastern U.S.A. bogs with new species records for North America and New England. Hydrobiologia 497: 53-62.
4. Boaden PJS. 1976. Soft meiofauna of sand from the Delta region of the Rhine, Meuse and Sheldt. Netherlands Journal of Sea Research 10: 461-471.
5. Campillo S, García-Roger EM, Carmona MJ, Serra M. 2011. Local adaptation in rotifer populations. Evolutionary Ecology 25: 933-947.
6. Curini-Galletti M, Artois T, Delogu V, De Smet WH, Fontaneto D, Jondelius U, Leasi F, Martinez A, Meyer-Wachsmuth I, Nilsson KS, Tongiorgi P, Worsaae K, Todaro MA. 2012. Patterns of diversity in soft-bodied meiofauna: dispersal ability and body size matter. PLoS ONE 7: e33801.
7. De Ridder M, Segers H. 1997. Monogonont Rotifera recorded in the world literature (except Africa) from 1960 to 1992. Studiedocumenten van het Koninklijk Belgisch Instituut voor Natuurwetenschappen 88: 1-481.
8. De Salle R. 2006. Species discovery versus species identification in DNA barcoding efforts: response to Rubinoff. Conservation Biology 20: 1545-1547.
9. De Smet WH. 2009. A review of the marine and brackish-water species of Testudinella (Rotifera: Monogononta, Testudinellidae), with the description of two new species. Zootaxa 2092: 1-20.
10. Ekman S. 1953. Zoogeography of the sea. London: Sidgwick & Jackson Ltd.
11. Epp RW, Winston PW. 1977. Osmotic regulation in the brackish water rotifer Brachionus plicatilis. The Journal of Experimental Biology 68: 151-156.
12. Epp RW, Winston PW. 1978. The effects of salinity and pH on the activity and oxygen consumption of Brachionus plicatilis (Rotatoria). Comparative Biochemistry and Physiology Part A: Physiology 59: 9-12.
13. Folmer O, Black M, Hoeh W, Lutz R, Vrigenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294-299.
14. Fontaneto D, De Smet WH, Ricci C. 2006. Rotifers in saltwater environments, re-evaluation of an inconspicuous taxon. Journal of the Marine Biological Association of the United Kingdom 86: 623-656.
15. Fontaneto D, Giordani I, Melone G, Serra M. 2007. Disentangling the morphological stasis in two rotifer species of the Brachionus plicatilis species complex. Hydrobiologia 583: 297-302.
16. Fontaneto D, Kaya M, Herniou EA, Barraclough TG. 2009. Extreme levels of hidden diversity in microscopic animals (Rotifera) revealed by DNA taxonomy. Molecular Phylogenetics & Evolution 53: 182-189.
17. Giannella C, Zito FA, Colonna F, Paradiso A, Marzullo F, Alaibac M, Schittulli F. 1997. Comparison of formalin, ethanol, and Histochoice fixation on the PCR amplification from paraffin-embedded breast cancer tissue. European Journal of Clinical Chemistry and Clinical Biochemistry: Journal of the Forum of European Clinical Chemistry Societies 35: 633-635.
18. Giere O. 2009. Meiobenthology: the microscopic motile fauna of aquatic sediments, 2nd edn. Berlin, Heidelberg: Springer-Verlag.
19. Gilbert JJ, Walsh EJ. 2005. Brachionus calyciflorus is a species complex: mating behavior and genetic differentiation among four geographically isolated strains. Hydrobiologia 546: 257-265.
20. Gómez A. 2005. Molecular ecology of rotifers: from population differentiation to speciation. Hydrobiologia 546: 83-99.
21. Gómez A, Carmona MJ, Serra M. 1997. Ecological factors affecting gene flow in the Brachionus plicatilis complex (Rotifera). Oecologia 111: 350-356.
22. Gómez A, Serra M, Carvalho GR, Lunt DH. 2002. Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera). Evolution 56: 1431-1444.
23. Gribble KE, Welch DBM. 2012. The mate recognition protein gene mediates reproductive isolation and speciation in the Brachionus plicatilis cryptic species complex. BMC Evolutionary Biology 12: 134.
24. Guindon S, Gascuel O. 2003. A simple, fast and accurate method to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696-704.
25. Hebert PD, Stoeckle MY, Zemlak TS, Francis CM. 2004. Identification of birds through DNA barcodes. PLoS Biology 2: e312.
26. Kacena MA, Troiano NW, Coady CE, Horowitz MC. 2004. HistoChoice® as an alternative to formalin fixation of undecalcified bone specimens. Biotechnic & Histochemistry 79: 185-190.
27. Keane TM, Creevey CJ, Pentony MM, Naughton TJ, McInerney JO. 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.
28. Khlebovich VV, Aladin NV. 2010. The salinity factor in animal life. Herald of the Russian Academy of Sciences 80: 299-304.
29. Kieneke A, Martínez Arbizu PM, Fontaneto D. 2012. Spatially structured populations with a low level of cryptic diversity in European marine Gastrotricha. Molecular Ecology 21: 1239-1254.
30. Lowe CD, Kemp SJ, Díaz-Avalos C, Montagnes DJS. 2007. How does salinity tolerance influence the distributions of Brachionus plicatilis sibling species? Marine Biology 150: 377-386.
31. McNamara J, Faria S. 2012. Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: a review. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 82: 997-1014.
32. Nelson DR. 2002. Current status of the tardigrada: evolution and ecology. Integrative and Comparative Biology 42: 652-659.
33. Obertegger U, Fontaneto D, Flaim G. 2012. Using DNA taxonomy to solve the ecological drivers of plankton diversity: occurrence of Synchaeta (Rotifera, Monogononta) in mountain lakes. Freshwater Biology 57: 1545-1553.
34. Ortells R, Gómez A, Serra M. 2003. Coexistence of cryptic rotifer species: ecological and genetic characterisation of Brachionus plicatilis. Freshwater Biology 48: 2194-2202.
35. Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP. 2006. Sequence based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55: 595-609.
36. Puillandre N, Bouchet P, Boisselier-Dubayle MC, Brisset J, Buge B, Castelin M, Chagnoux S, Christophe T, Corbari L, Lambourdière J, Lozouet P, Marani G, Rivasseau A, Silva N, Terryn Y, Tillier S, Utge J, Samadi S. 2012a. New taxonomy and old collections: integrating DNA barcoding into the collection curation process. Molecular Ecology Resources 12: 396-402.
37. Puillandre N, Lambert A, Brouillet S, Achaz G. 2012b. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21: 1864-1877.
38. R Development Core Team. 2012. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available at: http://www.R-project.org/
39. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
40. Sanderson MJ. 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution 19: 101-109.
41. Schönborn W. 2003. Lehrbuch der Limnologie. Stuttgart: Schweizerbart.
42. Schröder T, Walsh EJ. 2007. Cryptic speciation in the cosmopolitan Epiphanes senta complex (Monogononta, Rotifera) with the description of new species. Hydrobiologia 593: 129-140.
43. Segers H, De Smet WH, Fischer C, Fontaneto D, Michaloudi E, Wallace RL, Jersabek CD. 2012. Towards a list of available names in zoology, partim Phylum Rotifera. Zootaxa 3179: 61-68.
44. Segers H, Mertens J. 1997. New Rotifera from the Korup National Park, Cameroon. Journal of Natural History 31: 663-668.
45. Smith MA, Wood DM, Janzen DH, Hallwachs W, Hebert PD. 2007. DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists. Proceedings of the National Academy of Sciences of the United States of America 104: 4967-4972.
46. Suatoni E, Vicario S, Rice S, Snell T, Caccone A. 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.
47. Tang CQ, Leasi F, Obertegger U, Kieneke A, Barraclough TG, Fontaneto D. 2012. Widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proceedings of the National Academy of Sciences, USA 109: 16208-16212.
48. Walker KF. 1981. A synopsis of ecological information on the saline lake rotifer Brachionus plicatilis Müller, 1786. Hydrobiologia 81: 159-181.
49. Wallace RL, Snell TW, Ricci C, Nogrady T. 2006. Rotifera: biology, ecology and systematics. In: Segers H, ed. Guides to the identification of the microinvertebrates of the continental waters of the world. Volume 1. Leiden: Kenobi Productions, Ghent, and Backhuys Publishers, 1-299.
50. Walsh EJ, Schröder T, Wallace RL, Rico-Martinez R. 2009. Speciation in Lecane bulla (Monogononta: Rotifera) in Chihuahuan Desert waters. Verhandlungen Internationale Vereinigung für Limnologie 30: 1046-1050.
51. Wei N, De Smet WH, Xu R. 2011. Two new brackish-water species of Testudinella (Rotifera: Testudinellidae) from Qi'ao Island in the Pearl River estuary, China, with a key to marine and brackish-water Testudinella. Zootaxa 3051: 41-56.
52. Wiemers M, Fiedler K. 2007. Does the DNA barcoding gap exist? - a case study in blue butterflies (Lepidoptera: Lycaenidae). Frontiers in Zoology 4: 8.
53. Willems WR, Curini-Galletti M, Ferrero TJ, Fontaneto D, Heiner I, Huys R, Ivanenko VN, Kristensen RM, Kanneby T, MacNaughton MO, Martínez Arbizu P, Todaro MA, Sterrer W, Jondelius U. 2009. Meiofauna of the Koster-area, results from a workshop at the Sven Lovén Centre for Marine Sciences (Tjärnö, Sweden). Meiofauna Marina 17: 1-34.
54. Ziemann H, Schulz CJ. 2011. Methods for biological assessment of salt-loaded running waters - fundamentals, current positions and perspectives. Limnologica 41: 90-95.