Skip to main content
SpringerLink
Log in

Molecular variability in the Celleporella hyalina (Bryozoa; Cheilostomata) species complex: evidence for cryptic speciation from complete mitochondrial genomes

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

The bryozoan Celleporella has been shown to be composed of multiple, often cryptic, lineages. We sequenced two complete mitochondrial (mt) genomes of the Celleporella hyalina species complex from Wales, UK and Norway (i) to determine genetic divergence at the complete mt genome level, and (ii) to design new molecular markers for examining the interrelationships amongst the major lineages. In addressing (i), we estimated genetic divergence at three levels: (a) nucleotide diversity (π), (b) genome size, and (c) gene order. Genes nad4L, nad6, and atp8 showed the highest levels of divergence, and rrnL, rrnS, and cox1 showed the lowest levels. Inter-genome nucleotide divergence of protein-coding and ribosomal RNA genes, measured as π, was 0.21. The two genomes differed substantially in size, with the Norwegian genome being 2,573 base pairs (bp) longer than the Welsh genome, 17,265 and 14,692 bp, respectively. This difference in size is attributable to long non-coding regions present in the Norwegian genome. Both genomes exhibit similar gene orders, except for the translocation of one transfer RNA (trnA). Considering the high nucleotide diversity, genome size difference and change in gene order, these mt genomes are considered sufficiently divergent to have originated from two distinct species. In addressing (ii) we designed PCR primers that flank the most conserved regions of the genome: 1,300 bp of cox1 and a contiguous 2,000 bp fragment of rrnL + rrnS. The primers have yielded products for tissue from Wales, Norway, New Zealand, Alaska and Chile and should provide useful tools in establishing species- and population-level diversity within the Celleporella complex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Mayr E (1942) Systematics and the origin of species, from the viewpoint of a zoologist. Harvard University Press, Cambridge

    Google Scholar 

  2. Willughby RJ, Derham W (1718) Philosophical letters between the late learned Mr. Ray and several of his ingenious correspondents, natives and foreigners: To which are added those of Francis Willughby Esq: the whole consisting of many curious discoveries and improvements in the history of quadrupeds, birds, fishes, insects, plants, fossils, fountains, W and J Innys, London

  3. Winker K (2005) Sibling species were first recognized by William Derham (1718). Auk 122:706–707

    Article  Google Scholar 

  4. Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155

    Article  PubMed  Google Scholar 

  5. Bálint M, Domisch S, Engelhardt CHM, Haase P, Lehrian S, Sauer J, Theissinger K, Pauls SU, Nowak C (2011) Cryptic biodiversity loss linked to global climate change. Nat Clim Change 1:313–318

    Article  Google Scholar 

  6. Lindner A, Govindarajan AF, Migotto AE (2011) Cryptic species, life cycles, and the phylogeny of Clytia (Cnidaria: Hydrozoa: Campanulariidae). Zootaxa 2980:23–36

    Google Scholar 

  7. Baird HP, Miller KJ, Stark JS (2011) Evidence of hidden biodiversity, ongoing speciation and diverse patterns of genetic structure in giant Antarctic amphipods. Mol Ecol 20:3439–3454

    Article  PubMed  Google Scholar 

  8. Sundberg P, Vodoti ET, Zhou H, Strand M (2009) Polymorphism hides cryptic species in Oerstedia dorsalis (Nemertea, Hoplonemertea). Biol J Linn Soc 98:556–567

    Article  Google Scholar 

  9. Williams S, Apte D, Ozawa T, Kaligis F, Nakano T (2011) Speciation and dispersal along continental coastlines and island arcs in the Indo-West-Pacific turbinid gastropod genus Lunella. Evolution 65:1752–1771

    Article  PubMed  Google Scholar 

  10. Luttikhuizen PC, Bol A, Cardoso JFMF, Dekker R (2011) Overlapping distributions of cryptic Scoloplos cf. armiger species in the western Wadden Sea. J Sea Res 66:231–237

    Article  Google Scholar 

  11. Hunter RL, Halanych KM (2008) Evaluating connectivity in the brooding brittle star Astrotoma agassizii across the drake passage in the Southern Ocean. J Hered 99:137–148

    Article  CAS  PubMed  Google Scholar 

  12. Xavier JR, Rachello-Dolmen PG, Parra-Velandia F, Schönberg CHL, Breeuwer JAJ, van Soest RWM (2010) Molecular evidence of cryptic speciation in the “cosmopolitan” excavating sponge Cliona celata (Porifera, Clionaidae). Mol Phylogent Evol 56:13–20

    Article  CAS  Google Scholar 

  13. Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216

    Article  Google Scholar 

  14. Chimenz Gusso C, Boccia P, Giovannini N (2004) Importance of faunistic and taxonomic studies for a correct analysis of the zoogeography of Mediterranean Bryozoa. Biogeographia 25:93–108

    Google Scholar 

  15. Lee H-J, Kwan Y-S, Kong S-R, Min BS, Seo JE, Won Y-J (2011) DNA barcode examination of Bryozoa (Class: Gymnolaemata) in Korean seawater. Korean J Syst Zool 27:159–163

    Article  Google Scholar 

  16. Dick MH, Herrera-Cubilla A, Jackson JBC (2003) Molecular phylogeny and phylogeography of free-living Bryozoa (Cupuladriidae) from both sides of the Isthmus of Panama. Mol Phylogenet Evol 27:355–371

    Article  CAS  PubMed  Google Scholar 

  17. Schwaninger H (1999) Population structure of the widely dispersing marine bryozoan Membranipora membranacea (Cheilostomata): implications for population history, biogeography, and taxonomy. Mar Biol 135:411–423

    Article  Google Scholar 

  18. Schwaninger H (2008) Global mitochondrial DNA phylogeography and biogeographic history of the antitropically and longitudinally disjunct marine bryozoan Membranipora membranacea (Cheilostomata): another cryptic marine sibling species complex? Mol Phylogenet Evol 49:893–908

    Article  CAS  PubMed  Google Scholar 

  19. Nikulina EA, Hanel R, Schäfer P (2007) Cryptic speciation and paraphyly in the cosmopolitan bryozoan Electra pilosa—impact of the Tethys closing on species evolution. Mol Phylogenet Evol 45:765–776

    Article  CAS  PubMed  Google Scholar 

  20. Nikulina EA (2008) Taxonomy and ribosomal DNA-based phylogeny of the Electra crustulenta species group (Bryozoa: Cheilostomata) with revision of Borg’s varieties and description of Electra moskvikvendi n. sp. from the Western Baltic Sea. Org Divers Evol 8:215–229

    Article  Google Scholar 

  21. Davidson SK, Haygood MG (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”. Biol Bull 196:273–280

    Article  CAS  PubMed  Google Scholar 

  22. Mackie JA, Keough MJ, Norman JA, Christidis L (2001) Mitochondrial evidence of geographical isolation within Bugula dentata Lamouroux. In: Wyse Jackson PN, Buttler CJ, Spencer Jones ME (eds) Bryozoan Studies 2001, Proceedings of the 12th International Bryozoology Association Conference, AA Balkema Publishers, Dublin, pp 199–206

  23. McGovern TM, Hellberg ME (2003) Cryptic species, cryptic endosymbionts, and geographical variation in chemical defenses in the bryozoan Bugula neritina. Mol Ecol 12:1207–1215

    Article  CAS  PubMed  Google Scholar 

  24. Mackie JA, Keough MJ, Christidis L (2006) Invasion patterns inferred from cytochrome oxidase I sequences in three bryozoans, Bugula neritina, Watersipora subtorquata, and Watersipora arcuata. Mar Biol 149:285–295

    Article  CAS  Google Scholar 

  25. Thorpe JP, Beardmore JA, Ryland JS (1978) Genetic evidence for cryptic speciation in the marine bryozoan Alcyonidium gelatinosum. Mar Biol 49:27–32

    Article  Google Scholar 

  26. Thorpe JP, Ryland JS, Beardmore JA (1978) Genetic variation and biochemical systematics in the marine bryozoan Alcyonidium mytili. Mar Biol 49:343–350

    Article  Google Scholar 

  27. Thorpe JP, Ryland JS (1979) Cryptic speciation detected by biochemical genetics in three ecologically important intertidal bryozoans. Estuar Coast Shelf S 8:395–398

    Article  CAS  Google Scholar 

  28. Hincks T (1880) A history of the British marine Polyzoa, vol 1. J Van Hoorst, London

    Book  Google Scholar 

  29. Kluge GA (1975) Bryozoa of the Northern Seas of the USSR. Amerind Publishing Co, New Delhi

    Google Scholar 

  30. Morris PA (1980) The bryozoan family Hippothoidae (Cheilostomata–Ascophora) with emphasis on the genus Hippothoa. Mg S AHF 10:1–115

    Google Scholar 

  31. Moyano GHI (1986) Bryozoa marinos Chilenos VI. Cheilostomata Hippothoidae: south eastern Pacific species. Bol Soc Biol Concepción 57:89–135

    Google Scholar 

  32. Hoare K, Goldson AJ, Giannasi N, Hughes RN (2001) Molecular phylogeography of the cosmopolitan bryozoan Celleporella hyalina: cryptic speciation? Mol Phylogenet Evol 18:488–492

    Article  CAS  PubMed  Google Scholar 

  33. Gómez A, Wright PJ, Lunt DH, Cancino JM, Carvalho GR, Hughes RN (2007) Mating trials validate the use of DNA barcoding to reveal cryptic speciation of a marine bryozoan taxon. P Roy Soc Lond B Bio 274:199–207

    Article  Google Scholar 

  34. Gómez A, Hughes RN, Wright PJ, Carvalho GR, Lunt DH (2007) Mitochondrial DNA phylogeography and mating compatibility reveal marked genetic structuring and speciation in the NE Atlantic bryozoan Celleporella hyalina. Mol Ecol 16:2173–2188

    Article  PubMed  Google Scholar 

  35. Hughes RN, Gómez A, Wright PJ, Moyano HI, Cancino JM, Carvalho GR, Lunt DH (2008) Molecular phylogeny supports division of the ‘cosmopolitan’ taxon Celleporella (Bryozoa; Cheilostomata) into four major clades. Mol Phylogenet Evol 46:369–374

    Article  CAS  PubMed  Google Scholar 

  36. Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686–W689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Laslett D, Canbäck B (2008) ARWEN, a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics 24:172–175

    Article  CAS  PubMed  Google Scholar 

  38. Drummond AJ, 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 v5.4. http://www.geneious.com/

  39. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (* and other methods), version 4. Sinauer Associates, Sunderland

    Google Scholar 

  40. Perna NT, Kocher TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol 41:353–358

    Article  CAS  PubMed  Google Scholar 

  41. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Katoh K, Kuma K-I, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  44. Yang C-H, Chang H-W, Ho C-H, Chou Y-C, Chuang L-Y (2011) Conserved PCR primer set designing for closely-related species to complete mitochondrial genome sequencing using a sliding window-based PSO algorithm. PLoS ONE 6:e17729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Oliveira DCSG, Raychoudhury R, Lavrov DV, Werren JH (2008) Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae). Mol Biol Evol 25:2167–2180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Jia WZ, Yan HB, Guo AJ, Zhu XQ, Wang YC, Shi WG, Chen HT, Zhan F, Zhang SH, Fu BQ, Littlewood DTJ, Cai XP (2010) Complete mitochondrial genomes of Taenia multiceps, T. hydatigena and T. pisiformis: additional molecular markers for a tapeworm genus of human and animal health significance. BMC Genomics 11:447

    Article  PubMed  PubMed Central  Google Scholar 

  47. Soroka M (2010) Characteristics of mitochondrial DNA of unionid bivalves (Mollusca: Bivalvia: Unionidae). II. Comparison of complete sequences of maternally inherited mitochondrial genomes of Sinanodonta woodiana and Unio pictorum. Folia Malacol 18:189–209

    Article  Google Scholar 

  48. Podsiadlowski L, Carapelli A, Nardi F, Dallai R, Koch M, Boore JL, Frati F (2006) The mitochondrial genomes of Campodea fragilis and Campodea lubbocki (Hexapoda: Diplura): high genetic divergence in a morphologically uniform taxon. Gene 381:49–61

    Article  CAS  PubMed  Google Scholar 

  49. Inoue JG, Miya M, Lam K, Tay BH, Danks JA, Bell J, Walker TI, Venkatesh B (2010) Evolutionary origin and phylogeny of the modern holocephalans (Chondrichthyes: Chimaeriformes): a mitogenomic perspective. Mol Biol Evol 27:2576–2586

    Article  CAS  PubMed  Google Scholar 

  50. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Moritz C, Dowling TE, Brown WM (1986) Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annu Rev Ecol Syst 18:269–292

    Article  Google Scholar 

  52. Moritz C, Dowling TE, Brown WM (1987) Tandem duplication in animal mitochondrial DNAs: variation in incidence and gene content among lizards. Proc Natl Acad Sci USA 84:7183–7187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. San Mauro D, Gower DJ, Zardoya R, Wilkinson M (2005) A hotspot of gene order rearrangement by tandem duplication and random loss in the vertebrate mitochondrial genome. Mol Biol Evol 23:227–234

    Article  PubMed  Google Scholar 

  54. Waeschenbach A, Telford MJ, Porter JS, Littlewood DTJ (2006) The complete mitochondrial genome of Flustrellidra hispida and the phylogenetic position of Bryozoa among the Metazoa. Mol Phylogenet Evol 40:195–207

    Article  CAS  PubMed  Google Scholar 

  55. Jang KH, Hwang UW (2009) Complete mitochondrial genome of Bugula neritina (Bryozoa, Gymnolaemata, Cheilostomata): phylogenetic position of Bryozoa and phylogeny of lophophorates within the Lophotrochzoa. BMC Genomics 10:167

    Article  PubMed  PubMed Central  Google Scholar 

  56. Sun M, Wu Z, Shen X, Ren J, Liu X, Liu H, Liu B (2009) The complete mitochondrial genome of Watersipora subtorquata (Bryozoa, Gymnolaemata, Ctenostomata) with phylogenetic consideration of Bryozoa. Gene 439:17–24

    Article  CAS  PubMed  Google Scholar 

  57. Nesnidal MP, Helmkampf M, Bruchhaus I, Hausdorf B (2011) The complete mitochondrial genome of Flustra foliacea (Ectoprocta, Cheilostomata)—compositional bias affects phylogenetic analyses of lophotrochozoan relationships. BMC Genomics 12:572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Sun M, Shen X, Liu H, Liu X, Wu Z, Liu B (2011) Complete mitochondrial genome of Tubulipora flabellaris (Bryozoa: Stenolaemata): the first representative from the class Stenolaemata with unique gene order. Mar Genomics 4:159–165

    Article  PubMed  Google Scholar 

  59. Boore JL, Collins TM, Stanton D, Daehler LL, Brown WM (1995) Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature 376:163–165

    Article  CAS  PubMed  Google Scholar 

  60. Rokas A, Holland PWH (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15:454–459

    Article  PubMed  Google Scholar 

  61. Larget B, Kadane JB, Simon DL (2005) A Bayesian approach to the estimation of ancestral genome arrangements. Mol Phylogenet Evol 36:214–223

    Article  CAS  PubMed  Google Scholar 

  62. Dowton M, Cameron SL, Dowavic JI, Austin AD, Whiting MF (2009) Characterization of 67 mitochondrial tRNA gene rearrangements in the Hymenoptera suggests that mitochondrial tRNA gene position is selectively neutral. Mol Biol Evol 26:1607–1617

    Article  CAS  PubMed  Google Scholar 

  63. Sheffield NC, Hiatt KD, Valentine MC, Song HJ, Whiting MF (2010) Mitochondrial genomics in Orthoptera using MOSAS. Mitochondrial DNA 21:87–104

    Article  CAS  PubMed  Google Scholar 

  64. Hyman IT, Ho SYW, Jermiin LS (2007) Molecular phylogeny of Australian helicarionidae euconulidae and related groups (Gastropoda: Pulmonata: Stylommatophora) based on mitochondrial DNA. Mol Phylogenet Evol 45:792–812

    Article  CAS  PubMed  Google Scholar 

  65. Zhou Y, Zhang JY, Zheng RQ, Yu BG, Yang G (2009) Complete nucleotide sequence and gene organization of the mitochondrial genome of Paa spinosa (Anura: Ranoidae). Gene 447:86–96

    Article  CAS  PubMed  Google Scholar 

  66. Waeschenbach A, Taylor PD, Littlewood DTJ (2012) A molecular phylogeny of bryozoans. Mol Phylogenet Evol 62:718–735

    Article  PubMed  Google Scholar 

  67. Navarrete ZA, Cancino JM, Moyano HI, Hughes RN (2004) Morphological differentiation in the Celleporella hyalina (Linnaeus, 1767) complex (Bryozoa: Cheilostomata) along the Chilean coast. In: Moyano GHI, Cancino JM, Wyse Jackson PN (eds) Bryozoan Studies 2004. Proceedings of the 13th International Bryozoology Association Conference, Concepción, Chile, pp 207–213

  68. Palumbi S, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. University of Hawaii, Department of Zoology and Kewalo Marine Laboratory, Honolulu

    Google Scholar 

  69. Hughes RN (2005) Lessons in modularity: the evolutionary ecology of colonial invertebrates. Sci Mar 69:169–179

    Article  Google Scholar 

  70. Cheetham AH, Jackson JBC, Hayek LAC (1994) Quantitative genetics of bryozoan phenotypic evolution. II. Analysis of selection and random change in fossil species using reconstructed genetic parameters. Evolution 48:360–375

    Article  Google Scholar 

Download references

Acknowledgments

We thank the staff at the NHM sequencing facility for their sequencing expertise, Christoffer Schander and Christiane Todt for facilitating the sample collection for the Norwegian genome, and Tim Littlewood and Karin Fehlauer Ale for critical reading of the manuscript. This project was funded by the Natural Environment Research Council, grant number NE/E015298/1, and the Centre for Integrated Research in the Rural Environment, Aberystwyth and Bangor Universities.

Author information

Authors and Affiliations

  1. Department of Zoology, The Natural History Museum, DC1 712, Cromwell Road, London, SW7 5BD, UK

    Andrea Waeschenbach

  2. Centre for Marine Biodiversity and Biotechnology, School of Life Science, Heriot Watt University, John Muir Building, Riccarton Campus, Edinburgh, EH14 4AS, UK

    Joanne S. Porter

  3. School of Biological Sciences, University of Bangor, Deiniol Road, Bangor, Gwynedd, LL57 2UW, UK

    Roger N. Hughes

Authors
  1. Andrea Waeschenbach
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joanne S. Porter
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roger N. Hughes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea Waeschenbach.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 71 kb)

Supplementary material 2 (DOC 136 kb)

Suppl. Fig 1 Pairwise alignments of the 22 tRNA, indicating conserved sites with asterisks. (EPS 338 kb)

11033_2012_1714_MOESM4_ESM.tif

Suppl. Fig. 2 Gel-images of PCR products for a) cox1 (Cellep_cox1F + Cellep_cox1R), product size 1,300 bp, and b) rrnL + rrnS (Cellep_16SR + Cellep_12SF_deg), product size ~ 2000 bp. M = Hyperladder I marker (Bioline); 1 = Wales; 2 = Norway; 3 = New Zealand; 4 = Alaska (Homer); 5 = Alaska (Seldovia); 6 = Chile. (TIFF 3365 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Waeschenbach, A., Porter, J.S. & Hughes, R.N. Molecular variability in the Celleporella hyalina (Bryozoa; Cheilostomata) species complex: evidence for cryptic speciation from complete mitochondrial genomes. Mol Biol Rep 39, 8601–8614 (2012). https://doi.org/10.1007/s11033-012-1714-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-012-1714-9

Keywords

Search

Navigation