Spatially structured populations with a low level of cryptic diversity in European marine gastrotricha

Molecular Ecology

Volumn 21, Issue 5, 2012, Pages 1239-1254

  Kieneke, Alexander ^a   Martínez Arbizu, Pedro M ^a   Fontaneto, Diego ^b  

^a SENCKENBERG DEUTSCHES ENTOMOLOGISCHES INSTITUT   (Germany)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

18S; cytochrome c oxidase subunit I gene; Gastrotricha; marine meiofauna; NE Atlantic; phylogeography

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; CELL NUCLEUS; CLASSIFICATION; DNA SEQUENCE; EUROPE; GENE FLOW; GENETIC VARIABILITY; GENETICS; INVERTEBRATE; PHYLOGEOGRAPHY; POPULATION GENETICS;

ANIMALS; CELL NUCLEUS; DNA, MITOCHONDRIAL; EUROPE; GENE FLOW; GENETIC VARIATION; GENETICS, POPULATION; INVERTEBRATES; PHYLOGEOGRAPHY; SEQUENCE ANALYSIS, DNA;

ANIMALIA; GASTROTRICHA; TURBANELLA; TURBANELLA AMBRONENSIS; TURBANELLA BOCQUETI; TURBANELLA CORNUTA; TURBANELLA HYALINA; TURBANELLA MUSTELA;

EID: 84857633925     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2011.05421.x     Document Type: Article

References (82)

1. Armonies W, (1988) Active emergence of meiofauna from intertidal sediment. Marine Ecology Progress Series, 43, 151-159.
2. Armonies W, (1989) Meiofaunal emergence from intertidal sediment measured in the field: significant contribution to nocturnal planktonic biomass in shallow waters. Helgoland Marine Research, 43, 29-43.
3. Artois T, Fontaneto D, Hummon WD, et al. (2011) Ubiquity of microscopic animals? Evidence from the morphological approach in species identification. In: Biogeography of Microscopic Organisms, is Everything Small Everywhere? (ed, Fontaneto D,), pp. 244-283. Systematics Association & Cambridge University Press, Cambridge.
4. Avise JC, (2000) Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, Massachusetts.
5. Baker JM, Funch P, Giribet G, (2007) Cryptic speciation in the recently discovered American cycliophoran Symbion americanus; genetic structure and population expansion. Marine Biology, 151, 2183-2193.
6. Beebee TJC, Rove G, (2008) An Introduction to Molecular Ecology, 2nd edn. Oxford University Press, Oxford.
7. Birky CW Jr, 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. doi:.
8. Bleidorn C, Kruse I, Albrecht S, et al. (2006) Mitochondrial sequence data expose the putative cosmopolitan polychaete Scoloplos armiger (Annelida, Orbiniidae) as a species complex. BMC Evolutionary Biology, 6, 47.
9. Casu M, Curini-Galletti M, (2004) Sibling species in interstitial flatworms: a case study using Monocelis lineata (Proseriata: Monocelididae). Marine Biology, 145, 669-679. (Pubitemid 39384685)
10. Chen G, Hare MP, (2011) Cryptic diversity and comparative phylogeography of the estuarine copepod Acartia tonsa on the US Atlantic coast. Molecular Ecology, 20, 2425-2441.
11. Clement M, Posada D, Crandall KA, (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1660.
12. Dal Zotto M, Ghiviriga S, Kånneby T, et al. (2010) Probing Gastrotricha Taxonomy with DNA Barcoding (abstract) In: 14 th International Meiofauna Conference. Book of Abstracts. (eds, Gheerardyn H, Bezarra TN, Cnudde C, et al.), p. 103. VLIZ Special Publication 44.
13. Derycke S, Backeljau T, Vanfleteren J, et al. (2005) Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina. Marine Ecology Progress Series, 300, 91-103. (Pubitemid 41475380)
14. Derycke S, Fonseca G, Vierstraete A, et al. (2008a) Disentangling taxonomy within the Rhabditis (Pellioditis) marina (Nematoda, Rhabditidae) species complex using molecular and morphological tools. Zoological Journal of the Linnean Society, 152, 1-15. (Pubitemid 351156550)
15. Derycke S, Remerie T, Backeljau T, et al. (2008b) Phylogeography of the Rhabditis (Pellioditis) marina species complex: evidence for long-distance dispersal, and for range expansions and restricted gene flow in the northeast Atlantic. Molecular Ecology, 17, 3306-3322. (Pubitemid 352030142)
16. Derycke S, De Ley P, Tandingan De Ley I, et al. (2010) Linking DNA sequences to morphology: cryptic diversity and population genetic structure in the marine nematode Thoracostoma trachygaster (Nematoda, Leptosomatidae). Zoologica Scripta, 39, 276-289.
17. Edmands S, (2001) Phylogeography of the intertidal copepod Tigriopus californicus reveals substantially reduced population differentiation at northern latitudes. Molecular Ecology, 10, 1743-1750. (Pubitemid 32667729)
18. Folmer O, Black M, Hoeh W, et al. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294-299.
19. Fontaneto D, (ed.) (2011) Biogeography of Microscopic Organisms, is Everything Small Everywhere? Systematics Association & Cambridge University Press, Cambridge.
20. Fontaneto D, Herniou EA, Boschetti C, et al. (2007) Evidence for independently evolving species in bdelloid rotifers. PLoS Biology, 5, 914-921. (Pubitemid 46631866)
21. Fontaneto D, Barraclough TG, Chen K, et al. (2008) Molecular evidence for broad-scale distributions in bdelloid rotifers: everything is not everywhere but most things are very widespread. Molecular Ecology, 17, 3136-3146. (Pubitemid 351861455)
22. Giere O, (2009) Meiobenthology. The Microscopic Motile Fauna of Aquatic Sediments. Springer, Berlin.
23. Giribet G, Sørensen MV, Funch P, et al. (2004) Investigations into the phylogenetic position of Micrognathozoa using four molecular loci. Cladistics, 20, 1-13. (Pubitemid 38370662)
24. Gollner S, Fontaneto D, Martínez Arbizu P, (2011) Molecular taxonomy confirms morphological classification of deep-sea hydrothermal vent copepods (Dirivultidae) and suggests broad physiological tolerance of species and frequent dispersal along ridges. Marine Biology, 158, 221-231.
25. Gõmez A, Serra M, Carvalho GR, et al. (2002) Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera). Evolution, 56, 1431-1444. (Pubitemid 34881594)
26. Gõmez A, Hughes RN, Wright PJ, et al. (2007) Mitochondrial DNA phylogeography and mating compatibility reveal marked genetic structuring and speciation in the NE Atlantic bryozoan Celleporella hyalina. Molecular Ecology, 16, 2173-2188. (Pubitemid 46718922)
27. Guindon S, Gascuel O, (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology, 52, 696-704. (Pubitemid 37365050)
28. Hewitt GM, (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society, 58, 247-276. (Pubitemid 26389802)
29. Hewitt GM, (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London B, 359, 183-195. (Pubitemid 38231471)
30. Hudson RR, Slatkin M, Maddison WP, (1992) Estimation of levels of gene flow from DNA-sequence data. Genetics, 132, 583-589.
31. Hummon WD, (2010) Marine Gastrotricha of San Juan Island, Washington, USA, with notes on some species from Oregon and California. Meiofauna Marina, 18, 11-40.
32. Hummon WD, Kelly JL, (2011) Turbanella amphiatlantica, a new species of Gastrotricha (Macrodasyida) from eastern North America and northwest Europe. Meiofauna Marina, 19, 61-70.
33. Keane TM, Creevey CJ, Pentony MM, et al. (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.
34. Kieneke A, Fontaneto D, (2010) Holocene population history of two common marine gastrotrich species in the North Sea/Baltic Sea area inferred from mtDNA sequence variability (abstract). In: 14 th International Meiofauna Conference. Book of Abstracts (eds, Gheerardyn H, Bezarra TN, Cnudde C, et al.), p. 47. VLIZ Special Publication 44.
35. Køje M, Kristiansen A, (1999) Havets dyr og planter. Gads Forlag, Copenhagen.
36. Kumar S, SkjÅ∥veland Š, Orr RJS, et al. (2009) AIR: A batch-oriented web program package for construction of supermatrices ready for phylogenomic analyses. BMC Bioinformatics, 10, 357.
37. Leasi F, Todaro MA, (2009) Meiofaunal cryptic species revealed by confocal microscopy: the case of Xenotrichula intermedia (Gastrotricha). Marine Biology, 156, 1335-1346.
38. Lee CE, (2000) Global phylogeography of a cryptic copepod species complex and reproductive isolation between genetically proximate " populations". Evolution, 54, 2014-2027. (Pubitemid 32113829)
39. Librado P, Rozas J, (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
40. Littlewood DT, Telford MJ, Clough KA, et al. (1998) Gnathostomulida-an enigmatic metazoan phylum from both morphological and molecular perspectives. Journal of Molecular Phylogenetics and Evolution, 9, 72-79. (Pubitemid 128350014)
41. Lucentini L, Rebora M, Puletti ME, et al. (2011) Geographical and seasonal evidence of cryptic diversity in the Baetis rhodani complex (Ephemeroptera, Baetidae) revealed by means of DNA taxonomy. Hydrobiologia, 673, 215-228.
42. Maguire C, (1976) Turbanella varians n. sp., a marine Gastrotrich with local morphological variants. Cahier de Biologie Marine, 17, 185-194.
43. Manylov OG, Vladychenskaya NS, Milyutina IA, et al. (2004) Analysis of 18S rRNA gene sequences suggests significant molecular differences between Macrodasyida and Chaetonotida (Gastrotricha). Molecular Phylogenetics and Evolution, 30, 850-854. (Pubitemid 38260981)
44. Mills S, Lunt DH, Gõmez A, (2007) Global isolation by distance despite strong regional phylogeography in a small metazoan. BMC Evolutionary Biology, 7, 225.
45. Montero-Pau J, Ramos-Rodriguez E, Serra M, Gomez A, (2011) Long-term coexistence of rotifer cryptic species. PLoS ONE, 6, e21530.
46. Nylander JAA, (2004) MrModeltest 2.3. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Sweden.
47. O'Brien HE, Parrent JL, Jackson JA, et al. (2005) Fungal community analysis by large-scale sequencing of environmental samples. Applied Environmental Microbiology, 71, 5544-5550. (Pubitemid 41338289)
48. Oksanen J, Blanchet FG, Kindt R, et al. (2010) Vegan: Community Ecology Package. R Package Version 1.17-3. Available from:.
49. Ortells R, Gõmez A, Serra M, (2003) Coexistence of cryptic rotifer species: ecological and genetic characterisation of Brachionus plicatilis. Freshwater Biology, 48, 2194-2202. (Pubitemid 38012633)
50. Paradis E, Bolker B, Claude J, et al. (2010) Package Ape 2.6-1. Analyses of Phylogenetics and Evolution. Available from:.
51. Pereira TJ, Fonseca G, Mundo-Ocampo M, et al. (2010) Diversity of free-living marine nematodes (Enoplida) from Baja California assessed by integrative taxonomy. Marine Biology, 157, 1665-1678.
52. Petrov NB, Pegova AN, Manylov OG, et al. (2007) Molecular phylogeny of Gastrotricha on the basis of a comparison of the 18S rRNA genes: Rejection of the hypothesis of a relationship between Gastrotricha and Nematoda. Molecular Biology, 41, 445-452. (Pubitemid 47145716)
53. Pons J, Barraclough TG, Gomez-Zurita J, et al. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology, 55, 595-609.
54. Provan J, Bennett KD, (2008) Phylogeographic insights into cryptic glacial refugia. Trends in Ecology and Evolution, 23, 564-571.
55. R Development Core Team (2010) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available from:.
56. Radziejewska T, Gruzka P, Rokicka-Praxmajer J, (2006) A home away from home: a meiobenthic assemblage in a ship's ballast water tank sediment. Oceanologia, 48, 259-265. (Pubitemid 44830229)
57. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574. (Pubitemid 37038874)
58. Rothe BH, Schmidth-Rhaesa A, (2008) Variation in the nervous system in three species of the genus Turbanella (Gastrotricha, Macrodasyida). Meiofauna Marina, 16, 175-184.
59. Rozen S, Skaletsky HJ, (2000) Primer3 on the WWW for general users and for biologist programmers. In: Bioinformatics Methods and Protocols: Methods in Molecular Biology (eds, Krawetz S, and, Misener S,), pp. 365-386. Humana Press, Totowa, New Jersey.
60. Sanderson MJ, (2002) Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution, 19, 101-109. (Pubitemid 34008052)
61. Sanna D, Lai T, Francalacci P, et al. (2009) Population structure of the Monocelis lineata (Proseriata, Monocelididae) species complex assessed by phylogenetic analysis of the mitochondrial Cytochrome c Oxidase subunit I (COI) gene. Genetics and Molecular Biology, 32, 864-867.
62. Schmidt H, Westheide W, (2000) Are the meiofaunal polychaetes Hesionides arenaria and Stygocapitella subterranea true cosmopolitan species?-Results of RAPD-PCR investigations. Zoologica Scripta, 29, 17-27. (Pubitemid 30114808)
63. Sørensen MV, Sterrer W, Giribet G, (2006) Gnathostomulid phylogeny inferred from a combined approach of four molecular loci and morphology. Cladistics, 22, 32-58.
64. Suatoni E, Vicario S, Rice S, et al. (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. (Pubitemid 44311537)
65. Tamura K, Dudley J, Nei M, et al. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596-1599. (Pubitemid 47236692)
66. Tamura K, Peterson D, Peterson N, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731-2739.
67. Teuchert G, (1968) On Reproduction and Development of the Macrodasyoidea (Gastrotricha). Zeitschrift für Morphologie der Tiere, 63, 343-418.
68. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673-4680. (Pubitemid 24354800)
69. Todaro MA, Hummon WD, (2008) An overview and a dichotomous key to genera of the phylum Gastrotricha. Meiofauna Marina, 16, 3-20.
70. Todaro MA, Fleeger JW, Hu YP, et al. (1996) Are meiofauna species cosmopolitan? Morphological and molecular analysis of Xenotrichula intermedia (Gastrotricha: Chaetonotida). Marine Biology, 125, 735-742.
71. Todaro MA, Littlewood DTJ, Balsamo M, et al. (2003) The interrelationships of the Gastrotricha using nuclear small rRNA subunit sequence data, with an interpretation based on morphology. Zoologischer Anzeiger, 242, 145-156. (Pubitemid 37027732)
72. Todaro MA, Telford MJ, Lockyer AE, et al. (2006) Interrelationships of the Gastrotricha and their place among the Metazoa inferred from 18S rRNA genes. Zoologica Scripta, 35, 251-259. (Pubitemid 44046464)
73. Westheide W, Schmidt H, (2003) Cosmopolitan versus cryptic meiofaunal polychaete species: an approach to a molecular taxonomy. Helgoland Marine Research, 57, 1-6. (Pubitemid 36509135)
74. Wieser W, (1957) Gastrotricha Macrodasyoidea from the Intertidal of Puget Sound. Transactions of the American Microscopical Society, 76, 372-381.
75. Wilke T, Schultheiß R, Albrecht C, (2009) As time goes by: A simple fool's guide to molecular clock approaches in invertebrates. American Malacological Bulletin, 27, 25-45.
76. Willet CS, Ladner JT, (2009) Investigations of fine-scale phylogeography in Tigriopus californicus reveal historical patterns of population divergence. BMC Evolutionary Biology, 9, 139.
77. Winnepenninckx B, Backeljau T, Mackey LY, et al. (1995) 18S rRNA data indicate that Aschelminthes are polyphyletic in origin and consist of at least three distinct clades. Molecular Biology and Evolution, 12, 1132-1137.
78. Wirz A, Pucciarelli S, Miceli C, et al. (1999) Novelty in phylogeny of gastrotricha: evidence from 18S rRNA gene. Molecular Phylogenetics and Evolution, 13, 314-318. (Pubitemid 129499341)
79. Wuyts J, De Rijk P, Van de Peer Y, et al. (2000) Comparative analysis of more than 3000 sequences reveals the existence of two pseudoknots in area V4 of eukaryotic small subunit ribosomal RNA. Nucleic Acid Research, 28, 4698-4708.
80. Xia X, Lemey P, (2009) Assessing substitution saturation with DAMBE. In: The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny, 2nd edn (eds, Lemey P, Salemi M, and, Vandamme A-M,), pp. 611-626. Cambridge University Press, Cambridge.
81. Xia X, Xie Z, (2001) DAMBE: Software Package for Data Analysis in Molecular Biology and Evolution. The Journal of Heredity, 92, 371-373. (Pubitemid 32848767)
82. Xia X, Xie Z, Salemi M, et al. (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution, 26, 1-7. (Pubitemid 36029247)