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Chromosomes of Pacific hydrothermal vent invertebrates: towards a greater understanding of the relationship between chromosome and molecular evolution

Published online by Cambridge University Press:  19 August 2009

D.R. Dixon ,
M.T. Jolly ,
W.F. Vevers  and
L.R.J. Dixon
D.R. Dixon
Affiliation:
The Marine Biological Association, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK
M.T. Jolly*
Affiliation:
The Marine Biological Association, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK
W.F. Vevers
Affiliation:
The Marine Biological Association, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK
L.R.J. Dixon
Affiliation:
The Marine Biological Association, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK
*
Correspondence should be addressed to: M.T. Jolly, The Marine Biological Association, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK email: [email protected]
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Abstract

Karyotypes for several East Pacific Rise hydrothermal vent invertebrates are described here for the first time: the vestimentiferans Riftia pachyptila and Oasisia alvinae, the alvinellid polychaetes Alvinella pompejana, A. caudata and Paralvinella grasslei, the polynoid polychaetes Branchinotogluma grasslei and Branchipolynoe symmytilida, the serpulid Laminatubus alvini and the mytilid bivalve Bathymodiolus thermophilus. For comparative purposes, the karyotype of the Atlantic vent mussel Bathymodiolus azoricus is also described here for the first time. Each species has its own unique chromosomal characteristics which can be interpreted both in terms of group characteristics and species divergence. From comparisons with published results on other vent species and closely-related coastal species, we identified a positive correlation between chromosome number variation and molecular divergence at two ribosomal ribonucleic acid gene loci (the 18S and 28S rRNA). Whilst the patterns of chromosome divergence we found were generally within the ranges previously reported for these taxonomic groupings, there was an apparent inconsistency in the case of Branchipolynoe symmytilida (EPR) and Branchipolynoe seepensis (MAR), which show a greater degree of divergence at the chromosome level compared with other members of the same genus. Moreover, polychaetes as a whole showed greater variation in the number and structural divergence of chromosomes compared to Mytilids (structural information only). Our findings highlight the great potential for chromosome analysis in future taxonomic and evolutionary studies of the deep-sea vent fauna.

Keywords

chromosomesPacific hydrothermal vents18S rRNA28S rRNA
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 90 , Issue 1 , February 2010 , pp. 15 - 31
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

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References

REFERENCES

Atwater, T. (1989) Plate tectonic history of the northeast Pacific and western North America. In Winterer, E.L., Hussong, D.M. and Decker, R.W. (eds) The geology of North America Volume IV. The Eastern Pacific Ocean and Hawaii. Boulder, CO: Geological Society of America, pp. 21–71.Google Scholar
Barsotti, G. and Meluzzi, C. (1968) Osservazioni su Mytilus edulis L. e Mytilus galloprovincialis Lamarck. Conchiglie (Milan) 4, 50–58.Google Scholar
Black, M.B., Halanych, K.M., Maas, P.A.Y., Hoeh, W.R., Hashimoto, J., Desbruyères, D., Lutz, R.A. and Vrijenhoek, R.C. (1997) Molecular systematics of vestimentiferan tubeworms from hydrothermal vents and cold-water seeps. Marine Biology 130, 141–149.Google Scholar
Bonnet, E. and Van de Peer, Y. (2002) zt: a software tool for simple and partial Mantel tests. Journal of Statistical Software 7, 1–12.Google Scholar
Carson, H.L. (1982) Speciation as a major reorganization of polygenic balances. In Bariozzi, C. (ed.) Mechanisms of speciation. New York: Alan R. Liss, pp. 411–433.Google Scholar
Chevaldonné, P., Jollivet, D., Desbruyères, D., Lutz, R.A. and Vrijenhoek, R.C. (2002) Sister-species of eastern Pacific hydrothermal vent worms (Ampharetidae, Alvinellidae, Vestimentifera) provide new mitochondrial CoI clock calibration. Cahiers de Biologie Marine 43, 367–370.Google Scholar
Dasgupta, S. and Austin, A.P. (1960) The chromosomes numbers and nuclear cytology of some common British serpulids. Quarterly Journal of Microscopical Science 101, 395–400.Google Scholar
Dixon, D.R. and Flavell, N. (1986) A comparative study of the chromosomes of Mytilus edulis and Mytilus galloprovincialis. Journal of the Marine Biological Association of the United Kingdom 66, 219–228.Google Scholar
Dixon, D.R., McFadzen, I.R.B. and Sisley, K. (1986) Heterochromatic marker regions (nucleolar organisers) in the chromosomes of the common mussel, Mytilus edulis (Mollusca: Pelecypoda). Journal of Experimental Marine Biology and Ecology 97, 205–212.Google Scholar
Dixon, D.R., Simpson-White, R. and Dixon, L.R.J. (1992) Evidence for thermal stability of ribosomal DNA sequences in hydrothermal-vent organisms. Journal of the Marine Biological Association of the United Kingdom 72, 519–527.Google Scholar
Dixon, D.R., Pascoe, P.L., Gibbs, P.E. and Pasantes, J.J. (1994) The nature of Robertsonian chromosomal polymorphism in Nucella lapillus: a re-examination. In Beaumont, A. (ed.) Genetics and evolution of aquatic organisms. London: Chapman and Hall, pp. 389–399.Google Scholar
Dixon, D.R., Pascoe, P.L. and Dixon, L.R.J. (1998) Karyotypic differences between two species of Pomatoceros, P. triqueter and P. lamarckii (Polychaeta: Serpulidae). Journal of the Marine Biological Association of the United Kingdom 78, 1113–1126.Google Scholar
Dixon, D.R., Dixon, L.R.J., Pascoe, P.L. and Wilson, J.T. (2001) Chromosomal and nuclear characteristics of deep-sea hydrothermal-vent organisms: correlates of increased growth rate. Marine Biology 139, 251–255.Google Scholar
Dixon, D.R., Pruski, A.M., Dixon, L.R.J. and Jha, A.N. (2002a) Marine invertebrate eco-genotoxicology: a methodological overview. Mutagenesis 17, 495–507.Google Scholar
Dixon, D.R., Dixon, L.R.J., Shillito, B. and Gwynn, J.P. (2002b) Background and induced levels of DNA damage in Pacific deep-sea vent polychaetes: the case for avoidance. Cahiers de Biologie Marine 43, 333–336.Google Scholar
Ebied, A-B.M. and Aly, F.M. (2004) Cytogenetic studies on metaphase chromosomes of six bivalve species of families Mytilidae and Veneridae (Nucinelloidea, Mollusca). Cytologia 69, 261–273.Google Scholar
Gilbert, C., O'Brien, P.C., Bronner, G., Yang, F., Hassanin, A., Ferguson-Smith, M.A. and Robinson, T.J. (2006) Chromosome painting and molecular dating indicate a low rate of chromosomal evolution in golden moles (Mammalia, Chrysochloridae). Chromosome Research 14, 793–803.Google Scholar
Halanych, K.M., Lutz, R.A. and Vrijenhoek, R.C. (1998) Evolutionary origins and age of vestimentiferan tube-worms. Cahiers de Biologie Marine 39, 355–358.Google Scholar
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Jacobs, D.K. and Lindberg, D.R. (1998) Oxygen and evolutionary patterns in the sea: onshore/offshore trends and recent recruitment of deep-sea faunas. Proceedings of the National Academy of Sciences of the USA 95, 9396–9401.Google Scholar
Jollivet, D., Comtet, T., Chevaldonné, P., Hourdez, S., Desbruyères, D. and Dixon, D.R. (1998a) Unexpected relationship between dispersal strategies and speciation within the association Bathymodiolus (Bivalvia)–Branchipolynoe (polychaeta) inferred from the rDNA neutral ITS2 marker. Cahiers de Biologie Marine 39, 359–362.Google Scholar
Jollivet, D., Dixon, L.R.J., Desbruères, D. and Dixon, D.R. (1998b) Ribosomal (rDNA) variation in a deep-sea hydrothermal vent polychaete, Alvinella pompejana, from 13°N on the East Pacific Rise. Journal of the Marine Biological Association of the United Kingdom 78, 113–130.Google Scholar
Jones, W.J., Won, Y-J., Maas, P.A.Y., Smith, P.J., Lutz, R.A. and Vrijenhoek, R.C. (2006) Evolution of habitat use by deep-sea mussels. Marine Biology 148, 841–851.Google Scholar
King, M. (1993) Species evolution—the role of chromosome change. Cambridge: Cambridge University Press.Google Scholar
Kligerman, A.D. and Bloom, S.E. (1977) Rapid chromosome preparations from solid tissues of fishes. Journal of the Fisheries Research Board of Canada 34, 266–269.Google Scholar
Knowlton, N., Weigt, L.A., Solórzano, L.A., Mills, D.K. and Bermingham, E. (1993) Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science 260, 1629–1632.Google Scholar
Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 116, 111–120.Google Scholar
Kumar, S., Tamura, K., Jacobsen, I.B. and Nei, M. (2001) Molecular Evolutionary Genetics Analysis software. Arizona State University, Tempe, USA.Google Scholar
Kupriyanova, E.K., MacDonald, T.A. and Rouse, G.W. (2006) Phylogenetic relationships within the Serpulidae (Sabellida, Annelida) inferred from molecular and morphological data. Zoologica Scripta 35, 421–439.Google Scholar
Levan, A., Fredga, K. and Sandberg, A.A. (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52, 201–220.Google Scholar
Little, C.T.S. and Vrijenhoek, R.C. (2003) Are hydrothermal vent animals living fossils? Trends in Ecology and Evolution 18, 582–588.Google Scholar
Lutz, R.A., Shank, T., Fornari, D., Haymon, R., Lilley, M., Von Damm, K. and Desbruyères, D. (1994) Rapid growth at the deep-sea vents. Nature 371, 663–664.Google Scholar
Martínez-Lage, A., González-Tizón, A. and Méndez, J. (1996) Chromosome differences between European mussel populations (genus Mytilus). Caryologia 49, 343–355.Google Scholar
Matson, S.E., Davis, J.P. and Chew, K.K. (2003) Laboratory hybridization of the mussels, Mytilus trossulus and M. galloprovincialis: larval growth, survival and early development. Journal of Shellfish Research 22, 423–430.Google Scholar
Pascoe, P.L. and Dixon, D.R. (1994) Structural chromosomal polymorphism in the dog-whelk Nucella lapillus (Mollusca: Neogastropoda). Marine Biology 118, 247–253.Google Scholar
Pond, D.W., Allen, C.E., Bell, M.V., van Dover, C.L., Fallick, A.E., Dixon, D.R. and Sargent, J.R. (2002) Origins of long-chain polyunsaturated fatty acids in the hydrothermal vent worms Ridgeia piscesae and Protis hydrothermica. Marine Ecology Progress Series 225, 219–226.Google Scholar
Rex, M.A., McClain, C.R., Johnson, N.A., Etter, R.J., Allen, J.A., Bouchet, P. and Warén, A. (2005) A source-sink hypothesis for abyssal biodiversity. American Naturalist 165, 163–178.Google Scholar
Rouse, G.W. (2001) A cladistic analysis of Siboglinidae Caullery, 1914 (Polychaeta, Annelida): formerly the phyla Pogonophora and Vestimentifera. Zoological Journal of the Linnean Society 132, 55–80.Google Scholar
Rumpler, Y. (2000) What cytogenetic studies may tell us about species diversity and speciation of lemurs. International Journal of Primatology 21, 865–881.Google Scholar
Samadi, S., Quéméré, E., Lorion, J., Tillier, A., von Cosel, R., Lopez, P., Cruaud, C., Couloux, A. and Boisselier-Dubayle, M-C. (2007) Molecular phylogeny in mytilids supports the wooden steps to deep-sea vents hypothesis. Comptes Rendus Biologies 330, 446–456.Google Scholar
Samstad, S. (1971) Chromosome numbers in Serpula vermicularis L. and Filograna implexa Berkeley. Norwegian Journal of Zoology 19, 169–175.Google Scholar
Seed, R. (1992) Systematic evolution and distribution of mussels belonging to the genus Mytilus: an overview. American Malacological Bulletin 9, 123–137.Google Scholar
Skibinski, D.O.F., Ahmad, M. and Beardmore, J.A. (1978) Genetic evidence for naturally occurring hybrids between Mytilus edulis and Mytilus galloprovincialis. Evolution 32, 354–364.Google Scholar
Thiriot-Quiévreux, C. (1994) Advances in cytogenetics of aquatic organisms. In Beaumont, A. (ed.) Genetics and evolution of aquatic organisms. London: Chapman and Hall, pp. 369–388.Google Scholar
Thiriot-Quiévreux, C. (2002) Review of the literature on bivalve cytogenetics in the last ten years. Cahiers de Biologie Marine 43, 17–26.Google Scholar
Tunnicliffe, V. (1988) Biogeography and evolution of hydrothermal vent fauna in the eastern Pacific Ocean. Proceedings of the Royal Society of London B 233, 347–366.Google Scholar
White, M.J.D. (1978) Modes of speciation. San Francisco: W.H. Freeman & Co.Google Scholar
Won, Y., Young, C.R., Lutz, R.A. and Vrijenhoek, R.C. (2003) Dispersal barriers and isolation among deep-sea mussel populations (Mytilidae: Bathymodiolus) from eastern Pacific hydrothermal vents. Molecular Ecology 12, 169–184.Google Scholar
Zbawicka, M., Wenne, R. and Skibinski, D.O.F. (2003) Mitochondrial DNA variation in populations of the mussel Mytilus trossulus from the Southern Baltic. Hydrobiologia 499, 1–3.Google Scholar