Cryptic species in the cosmopolitan Bugula neritina complex (Bryozoa, Cheilostomata)

Zoologica Scripta

Volumn 43, Issue 2, 2014, Pages 193-205

  Fehlauer Ale, Karin H ^a   Mackie, Joshua A ^b   Lim Fong, Grace E ^c   Ale, Ezequiel ^a   Pie, Marcio R ^d   Waeschenbach, Andrea ^e  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b SAN JOSE STATE UNIVERSITY   (United States)

^c RANDOLPH MACON COLLEGE   (United States)

^d FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^e DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84894257317     PISSN: 03003256     EISSN: 14636409     Source Type: Journal    
DOI: 10.1111/zsc.12042     Document Type: Article

References (63)

1. Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K. K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22, 148-155.
2. Bock, D. G., MacIsaac, H. J. & Cristescu, M. E. (2012) Multilocus genetic analyses differentiate between widespread and spatially restricted cryptic species in a model ascidian. Proceedings of the Royal Society B: Biological Sciences, 279, 2377-2385.
3. Burset, M., Seledtsov, I. A. & Solovyev, V. V. (2000) Analysis of canonical and non-canonical splice sites in mammalian genomes. Nucleic Acids Research, 28, 4364-4375.
4. Carlton, J. T. & Geller, J. B. (1993) Ecological roulette - the global transport of nonindigenous marine organisms. Science, 261, 78-82.
5. Clement, M., Posada, D. & Crandall, K. A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1659.
6. Darling, J. A., Bagley, M. J., Roman, J., Tepolt, C. K. & Geller, J. B. (2008) Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus. Molecular Ecology, 17, 4992-5007.
7. Davidson, S. K. & Haygood, M. G. (1999) Identification of sibling species of the bryozoan Bugula neritina that produce different anticancer bryostatins and harbor distinct strains of the bacterial symbiont "Candidatus Endobugula sertula". The Biological Bulletin, 196, 273-280.
8. Davidson, S. K., Allen, S. W., Lim, G. E., Anderson, C. M. & Haygood, M. G. (2001) Evidence for the biosynthesis of bryostatins by the bacterial symbiont "Candidatus Endobugula sertula" of the bryozoan Bugula neritina. Applied and Environmental Microbiology, 67, 4531-4537.
9. Drummond, A. J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T. & Wilson, A. (2011). Geneious v5.5.7 Available via http://www.geneious.com.
10. Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (version 3.1): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics, 1, 47-50.
11. Floerl, O., Inglis, G. J. & Gordon, D. P. (2009) Patterns of taxonomic diversity and relatedness among native and non-indigenous bryozoans. Diversity and Distributions, 15, 438-449.
12. Florence, W. K., Hayward, P. J. & Gibbons, M. J. (2007) Taxonomy of shallow-water Bryozoa from the west coast of South Africa. African Natural History, 3, 1-58.
13. Folino-Rorem, N. C., Darling, J. A. & D'Ausilio, C. A. (2009) Genetic analysis reveals multiple cryptic invasive species of the hydrozoan genus Cordylophora. Biological Invasions, 11, 1869-1882.
14. Fu, Y. X. (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915-925.
15. Goslee, S. C. & Urban, D. L. (2007) The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software, 22, 1-19.
16. Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696-704.
17. Hao, J.-S., Li, C.-X., Sun, X.-Y. & Yang, Q. (2005) Phylogeny and divergence time estimation of cheilostome bryozoans based on mitochondrial 16S rRNA sequences. Chinese Science Bulletin, 50, 1205-1211.
18. Haygood, M. G. & Davidson, S. K. (1997) Small-subunit rRNA genes and in situ hybridization with oligonucleotides specific for the bacterial symbionts in the larvae of the bryozoan Bugula neritina and proposal of "Candidatus Endobugula sertula". Applied and Environmental Microbiology, 63, 4612-4616.
19. Hoare, K., Goldson, A. J., Giannasi, N. & Hughes, R. N. (2001) Molecular phylogeography of the cosmopolitan bryozoan Celleporella hyalina: cryptic speciation? Molecular Phylogenetics and Evolution, 18, 488-492.
20. Ignacio, B. L., Julio, L. M., Junqueira, A. O. R. & Ferreira-Silva, M. A. G. (2010) Bioinvasion in a Brazilian Bay: filling Gaps in the Knowledge of Southwestern Atlantic Biota. PLoS ONE, 5, e13065.
21. Jang, K. H. & Hwang, U. W. (2009) Complete mitochondrial genome of Bugula neritina (Bryozoa, Gymnolaemata, Cheilostomata): phylogenetic position of Bryozoa and phylogeny of lophophorates within the Lophotrochozoa. BMC Genomics, 10, 167.
22. Kaluza, P., Kolzsch, A., Gastner, M. T. & Blasius, B. (2010) The complex network of global cargo ship movements. Journal of the Royal Society Interface, 7, 1093-1103.
23. Katoh, K., Kuma, K., Toh, H. & Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33, 511-518.
24. Keough, M. J. & Chernoff, H. (1987) Dispersal and population variation in the bryozoan Bugula neritina. Ecology, 68, 199-210.
25. Knowlton, N. (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia, 420, 73-90.
26. Leaché, A. D. & Fujita, M. K. (2010) Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proceedings of the Royal Society B, 277, 3071-3077.
27. Lee, C. E., Remfert, J. L. & Chang, Y.-M. (2007) Response to selection and evolvability of invasive populations. Genetica, 129, 179-192.
28. Lee, H.-J., Kwan, Y.-S., Kong, S.-R., Min, B. S., Seo, J. E. & Won, Y.-J. (2011) DNA barcode examination of Bryozoa (class: Gymnolaemata) in Korean seawater. Korean Journal of Systematic Zoology, 27, 159-163.
29. Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
30. Lim, G. (2004) Bugula (Bryozoa) and Their Bacterial Symbionts: A Study in Symbiosis, Molecular Phylogenetics and Secondary Metabolism. Ph.D. Dissertation. San Diego, CA: University of California.
31. Lim-Fong, G. E., Regali, L. A. & Haygood, M. G. (2008) Evolutionary relationships of "Candidatus Endobugula" bacterial symbionts and their Bugula bryozoan hosts. Applied Environmental Microbiology, 74, 3605-3609.
32. Lopanik, N., Lindquist, N. & Targett, N. (2004) Potent cytotoxins produced by a microbial symbiont protect host larvae from predation. Oecologia, 139, 131-139.
33. Mackie, J. A., Keough, M. J., Norman, J. A. & Christidis, L. (2002) Mitochondrial evidence of geographical isolation within Bugula dentata Lamouroux. In P. N. Wyse-Jackson, C. J. Buttler & M. Spencer-Jones (Eds) Bryozoan Studies 2001(pp. 199-206). Tokyo, Lisse, Abingdon, Exton: A.A. Balkema Publishers.
34. Mackie, J. A., Keough, M. J. & Christidis, L. (2006) Invasion patterns inferred from cytochrome oxidase I sequences in three bryozoans, Bugula neritina, Watersipora subtorquata, and Watersipora arcuata. Marine Biology, 149, 285-295.
35. Mackie, J. A., Darling, J. A. & Geller, J. B. (2012) Ecology of cryptic invasions: latitudinal segregation among Watersipora (Bryozoa) species. Nature Scientific Reports, 2, 871.
36. Mathew, M. (2010) Differential Gene Expression in Bugula Neritina During Symbiotic Association With "Candidatus Endobugula Sertula". M.Sc Thesis Atlanta, Georgia: Georgia State University.
37. McGovern, T. M. & Hellberg, M. E. (2003) Cryptic species, cryptic endosymbionts, and geographical variation in chemical defences in the bryozoan Bugula neritina. Molecular Ecology, 12, 1207-1215.
38. Nikulina, E. A., Hanel, R. & Schäfer, P. (2007) Cryptic speciation and paraphyly in the cosmopolitan bryozoan Electra pilosa - Impact of the Tethys closing on species evolution. Molecular Phylogenetics and Evolution, 45, 765-776.
39. Okuyama, M., Wada, H. & Ishii, T. (2006) Phylogenetic relationships of freshwater bryozoans (Ectoprocta, Phylactolaemata) inferred from mitochondrial ribosomal DNA sequences. Zoologia Scripta, 35, 243-249.
40. Pineda, M. C., López-Legentil, S. & Turon, X. (2011) The Whereabouts of an Ancient Wanderer: global Phylogeography of the Solitary Ascidian Styela plicata. PLoS ONE, 6, e25495.
41. Piola, R. F. & Johnston, E. L. (2006) Differential tolerance to metals among populations of the introduced bryozoan Bugula neritina. Marine Biology, 148, 997-1010.
42. Pleijel, F., Jondelius, U., Norlinder, E., Nygren, A., Oxelman, B., Schander, C., Sundberg, P. & Thollesson, M. (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution, 48, 369-371.
43. Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253-1256.
44. Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21, 1864-1877.
45. Ramalho, L. V., Muricy, G. & Taylor, P. D. (2005) Taxonomy and distribution of Bugula (Bryozoa: Cheilostomata: anasca) in Rio de Janeiro state, Brazil. In H. I. Moyano, J. M. Cancino & P. N. Wyse-Jackson (Eds) Bryozoan Studies 2005 (pp. 231-243). Leiden: AA Balkema Publishers.
46. Rannala, B. & Yang, Z. (2003) Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics, 164, 1645-1656.
47. Ratnasingham, S. & Hebert, P. D. N. (2007) The Barcode of Life Data System. Molecular Ecology Notes, 7, 355-364.
48. Ronquist, F. & Huelsenbeck, J. P. (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574.
49. Ryland, J. S., Bishop, J. D. D., De Blauwe, H., El Nagar, A., Minchin, D., Wood, C. A. & Yunnie, A. L. E. (2011) Alien species of Bugula (Bryozoa) along the Atlantic coasts of Europe. Aquatic Invasions, 6, 17-31.
50. Schroth, W., Jarms, G., Streit, B. & Schierwater, B. (2002) Speciation and phylogeography in the cosmopolitan marine moon jelly, Aurelia sp. BMC Evolutionary Biology, 2, 1-10.
51. Schwaninger, H. R. (2008) Global mitochondrial DNA phylogeography and biogeographic history of the antitropically and longitudinally disjunct marine bryozoan Membranipora membranacea L. (Cheilostomata): another cryptic marine sibling species complex? Molecular Phylogenetics and Evolution, 49, 893-908.
52. Sharp, K. H., Davidson, S. K. & Haygood, M. G. (2007) Localization of 'Candidatus Endobugula sertula' and the bryostatins throughout the life cycle of the bryozoan Bugula neritina. ISME Journal, 1, 693-702.
53. Smith, K. F., Stefaniak, L., Saito, Y., Gemmill, C. E. C., Cary, S. C. & Fidler, A. E. (2012) Increased Inter-Colony Fusion Rates Are Associated with Reduced COI Haplotype Diversity in an Invasive Colonial Ascidian Didemnum vexillum. PLoS ONE, 7, e30473.
54. Swofford, D. L. (2003). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). version 4. Sinauer Associates.
55. Tajima, F. (1989) Statistical-Method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595.
56. Tilbrook, K. J. (2006). Cheilostomatous Bryozoa From the Solomon Islands. Santa Barbara Museum of Natural History Monographs 4 (Studies in Biodiversity Number 3). 386 pp.
57. Trindade-Silva, A. E., Lim-Fong, G. E., Sharp, K. H. & Haygood, M. G. (2010) Bryostatins: biological context and biotechnological prospects. Current Opinion in Biotechnology, 21, 834-842.
58. Vieira, L. M., Migotto, A. E. & Winston, J. E. (2008) Synopsis and annotated checklist of Recent marine Bryozoa from Brazil. Zootaxa, 1810, 1-39.
59. Wang, H., Zhang, H., Wong, Y. H., Voolstra, C., Ravasi, T., Bajic, V. B. & Qian, P. Y. (2010) Rapid transcriptome and proteome profiling of a nonmodel marine invertebrate, Bugula neritina. Proteomics, 10, 2972-2981.
60. Watts, P. C., Thorpe, J. P. & Taylor, P. D. (1998) Natural and anthropogenic dispersal mechanisms in the marine environment: a study using cheilostome Bryozoa. Philosophical Transactions of the Royal Society B: Biological Sciences, 353, 453-464.
61. Wendt, D. E. (2000) Energetics of larval swimming and metamorphosis in four species of Bugula (Bryozoa). The Biological Bulletin, 198, 346-356.
62. Winston, J. E. & Woollacott, R. M. (2008) Redescription and revision of some red-pigmented Bugula species. Bulletin of the Museum of Comparative Zoology, 159, 179-212.
63. Yang, Z. & Rannala, B. (2010) Bayesian species delimitation using multilocus sequence data. Proceedings of the National Academy of Sciences of The United States of America, 107, 9264-9269.