Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-31T16:53:56.511Z Has data issue: false hasContentIssue false
  • English
  • Français

Ribosomal (rDNA) Variation in a Deep Sea Hydrothermal Vent Polychaete, Alvinella Pompejana, From 13°N on the East Pacific Rise

Published online by Cambridge University Press:  11 May 2009

D. Jollivet ,
L.R.J. Dixon ,
D. Desbruyeres  and
D.R. Dixon
D. Jollivet
Affiliation:
Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, PL1 2PB.
L.R.J. Dixon
Affiliation:
Plymouth Marine Laboratory, Citadel Hill, Plymouth, PL1 2PB.
D. Desbruyeres
Affiliation:
IFREMER, Centre de Brest, DRO/EP, BP 70, 29280, Plouzané, France.
D.R. Dixon
Affiliation:
Plymouth Marine Laboratory, Citadel Hill, Plymouth, PL1 2PB.
Get access Rights & Permissions [Opens in a new window]

Extract

The rDNA repeat-unit of the vent polychaete Alvinella pompejana was investigated using restriction analysis. Mapping revealed evidence of rDNA polymorphism within and between individuals which was due to individual restriction site variation and sequence rearrangements involving spacer regions. The size of the repeat unit was 10.5 kb with virtually no evidence of length variation. Sequence inversions indicated the presence of two spatially-distinct subfamilies of repeats, probably on different chromosome pairs. Animals from contrasting vent habitats with respect to age and chemical emissions (young vs old chimneys and white vs black smokers) from within the 13°N/EPR (East Pacific Rise) vent sector were analysed for evidence of population differentiation. Based on individual restriction site variation, average FST estimates across neighbouring populations were in the region of ~0.05 and differed significantly from zero. This level of genetic differentiation is comparable to values reported previously for allozymes. Spatial and temporal allelic frequency variances estimated from pairwise combinations (i.e. s2S and s2T) strongly suggested that differences in allelic frequency were the result of repeated extinction/recolonization events associated with the vent instability. Estimates of the effective population size derived from standardized temporal allelic frequency variances Fks were very low compared to actual population size indicating great temporal fluctuations in the former. Theoretically, such an effective population size is not sufficient to maintain the observed level of polymorphism within the 13N/EPR vent sector. Results are therefore consistent with a ‘propagule’ colonization-type model in which extinction/recolonization rates are high. In Alvinella, planktonic larval dispersal appears sufficient to overcome any genetic differentiation resulting from drift, but these findings also indicate that propagules may only be capable of dispersing a few tens of kilometres per generation.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 78 , Issue 1 , February 1998 , pp. 113 - 130
Copyright
Copyright © Marine Biological Association of the United Kingdom 1998

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arnheim, N., 1983. Concerted evolution of multigene families. In Evolution of genes and proteins (ed. M., Nei), pp 38–61. Sunderland: Sinauer Press.Google Scholar
Black, M.B., 1991. Genetic (allozyme) variation in Vestimentifera (Ridgeia spp.) from hydrothermal vents of the Juan de Fuca Ridge (northern Pacific Ocean). MSc thesis, University of Victoria, Canada.Google Scholar
Black, M.B., Lutz, R.A. & Vrijenhoek, R.C., 1994. Gene flow among vestimentiferan tube worm (Rifia pachyptila) populations from hydrothermal vents of the eastern Pacific. Marine Biology, 120, 33–39.CrossRefGoogle Scholar
Brown, D.D., Wensink, P.C. & Jordan, E., 1972. A comparison of the ribosomal DNAs of Xenopus laevis and Xenopus mulleri: evolution of tandem genes. Journal of Molecular Biology, 63, 57–73.CrossRefGoogle Scholar
Brown, S.D.M. & Dover, G.A., 1981. Organization and evolutionary progress of a dispersed repetitive family of sequences in widely separated rodent genomes. Journal of Molecular Biology, 150, 441–66.CrossRefGoogle ScholarPubMed
Cherry, R., Desbruyeres, D., Heyraud, M. & Nolan, C. 1992. High levels of natural radioactivity in hydrothermal vent polychaetes. Compte Rendus de VAcademie des Sciences de Paris, serie III, 315, 21–26.Google Scholar
Chevaldonne, P. & Jollivet, D., 1993. Videoscopic study of deep-sea hydrothermal vent alvinellid polychaete populations: biomass estimation and behaviour. Marine Ecology Progress Series, 95, 251–262.CrossRefGoogle Scholar
Chevaldonné, P., Jollivet, D., Vangriesheim, A. & Desbruyères, D., 1997. Hydrothermal-vent alvinellid polychaete dispersal in the eastern Pacific. 1. Influence of vent site distribution, bottom currents and biological patterns. Limnology and Oceanography, 42, 67–80.CrossRefGoogle Scholar
Craddock, C., Hoeh, W. R., Lutz, R. A. & Vrijenhoek, R. C. 1995. Extensive gene flow among mytilid (Bathymodiolus thermophilus) populations from hydrothermal vents of the eastern Pacific. Marine Biology, 124, 137–146.CrossRefGoogle Scholar
Crow, J.F. & Kimura, M., 1970. An introduction to population genetics theory. New York: Harper & Row.Google Scholar
Davis, S.K., Strassman, J.E., Hughes, C., Pletscher, L.S. & Templeton, A.R., 1990. Population structure and kinship in Polistes (Hymenoptera, Vesperidae): an analysis using ribosomal DNA and protein electrophoresis. Evolution, 44, 1242–1253.CrossRefGoogle Scholar
Desbruyères, D. & Laubier, L., 1980. Alvinella pompejana gen. sp. nov., aberrant Ampharetidae from East Pacific Rise hydrothermal vents. Oceanologica Ada, 3, 267–274.Google Scholar
Desbruyères, D. & Laubier, L., 1986. Les Alvinellidae, une famille nouvelle d'annélides polychètes inféodées aux sources hydrothermales sous-marines: systématique, biologie et écologie. Canadian Journal of Zoology, 64, 2227–2245.CrossRefGoogle Scholar
Dixon, D.R., Dixon, L.R.J. & Tunnicliffe, V., 1994. Attributes of ribosomal DNA in alvinellid polychaetes from hydrothermal vents. In Actes de la 4ème Conférence Internationale des Polychètes (ed. J.C., Dauvin et al.), pp. 85–92, Paris: Elsevier Press. [Mémoires du Muséum d'Histoire Naturelle.]Google Scholar
Dixon, D.R., Jollivet, D., Dixon, L.R.J., Nott, J.A. & Holland, P.W.H., 1995. The molecular identification of early life-history stages of hydrothermal vent organisms. In Hydrothermal vents and processes (ed. L.M., Parson et al.), pp. 343–350. [Geological Society Special Publication, 87.]Google Scholar
Dover, G.A., 1982. Molecular drive: a cohesive mode of species evolution. Nature, London, 299, 111–117.CrossRefGoogle ScholarPubMed
Ewens, W.J., Spielman, R.S. & Harris, H., 1981. Estimation of genetic variation at the DNA level from restriction endonuclease data. Proceedings of the National Academy of Sciences of the United States of America, 78, 3748–3750.CrossRefGoogle ScholarPubMed
Feral, J.P., Philippe, H., Desbruyères, D., Laubier, L., Derelle, E. & Chenuil, A., 1994. Phylogénie moléculaire de polychètes Alvinellidae des sources hydrothermales actives de l'océan Pacifique. Compte Rendus de l'Acade´mie des Sciences de Paris, Life Sciences, 317, 771–779.Google Scholar
Flavell, R.B., 1986. Repetitive DNA and chromosome evolution in plants. Philosophical Transactions of the Royal Society of London B, 312, 227–242.Google Scholar
Flavell, R.B., Odell, M., Sharp, P., Nevo, E. & Beiles, A., 1986. Variation in the intergenic spacer of ribosomal DNA of wild wheat, Triticum dicoccoides, in Israel. Molecular Biology and Evolution, 3, 547–558.Google Scholar
Gilpin, M., 1991. The genetic effective size of a metapopulation. Biological journal of the Linnean Society, 42, 165–175.Google Scholar
Haymon, R.M. et al., 1993. Volcanic eruption of the mid-ocean ridge along the East Pacific Rise crest at 9°45 52'N: direct submersible observations of sea-floor phenomena associated with an eruption event in April, 1991. Earth and Planetary Sciences Letters, 119, 85–101.Google Scholar
Hedgecock, D., 1994. Does variance in reproductive success limit effective population sizes of marine organisms? In Genetics and evolution of aquatic organisms (ed. A.R., Beaumont), pp. 122–134. Chapman & Hall.Google Scholar
Hedgecock, D., Chow, V. & Waples, R.S., 1992. Effective population numbers of shellfish broodstocks estimated from temporal variance in allelic frequencies. Aquaculture, 108, 215–232.Google Scholar
Hedgecock, D. & Sly, F., 1990. Genetic drift and effective population sizes of hatchery-propagated stocks of the Pacific oyster, Crassostrea gigas. Aquaculture, 88, 21–38.CrossRefGoogle Scholar
Hekinian, R. & Fouquet, Y., 1985. Volcanism and metallogenesis of axial and off-axial structures on the East Pacific Rise near 13°N. Economic Geology, 80, 221–249.CrossRefGoogle Scholar
Hessler, R.R., Smithey, W.M., Boudrias, M.A., Keller, C.H., Lutz, R.A. & Childress, J.J., 1988. Temporal change in megafauna at the Rose Garden hydrothermal vent. Deep-Sea Research, 35, 1681–1710.Google Scholar
Hoelzel, A.R. & Dover, G.A., 1991. Molecular Genetic Ecology. Oxford: IRL Press.Google Scholar
Holland, P.W.H., 1993. Cloning genes using the polymerase chain reaction. In Essential developmental biology practical approach (ed. C.D., Stern and P.W.H., Holland), pp. 242–255. Oxford: IRL Press and Oxford University Press.Google Scholar
Holland, P.W.H., Hacker, A.M. & Williams, N.A., 1991. A molecular analysis of the phylogenetic affinities of Saccoglossus cambrensis Brambell & Cole (Hemichordata). Philosophical Transactions of the Royal Society of London B, 332, 185–189.Google Scholar
Jha, A.N., Hutchinson, T.H., Mackay, J.M., Elliott, B.M., Pascoe, P.L. & Dixon, D.R., 1995. The chromosomes of Platynereis dumerilii (Polychaeta: Nereidae). journal of the Marine Biological Association of the United Kingdom, 75, 551–562.Google Scholar
Jollivet, D., 1993. Distribution et évolution de la faune associée aux sources hydrothermales profondes 13°N sur la dorsale du Pacifique oriental: le cas particulier des polychètes Alvinellidae. Thèse de Doctorat nouveau régime, Océanologie Biologique, Université de Bretagne Occidentale, FranceGoogle Scholar
Jollivet, D., Desbruyères, D., Bonhomme, F. & Moraga, D., 1995a. Genetic differentiation of deep-sea hydrothermal vent alvinellid populations (Annelida: Polychaeta) along the East Pacific Rise. Heredity, 74, 376–391.CrossRefGoogle Scholar
Jollivet, D., Desbruyères, D., Ladrat, C. & Laubier, L., 1995b. Evidence for differences in thermostability of AAT, GPI and PGM allozymes in the deep-sea hydrothermal vent alvinellid polychaetes. Marine Ecology Progress Series, 123, 125–136.CrossRefGoogle Scholar
Kessler, C., Holtke, H.J., Seibl, R., Burg, J. & Muhlegger, K., 1990. Non-radioactive labelling and detection of nucleic acids. I. A novel DNA labelling and detection system based on digoxigenin: anti-digoxigenin ELISA principle. Biology and Chemistry Hoppe Seyler, 371, 917–927.CrossRefGoogle Scholar
Levitan, D.R. & Petersen, C., 1995. Sperm limitation in the sea. Trends in Ecology and Evolution, 10, 228–231.Google Scholar
Long, E.O. & Dawid, I.B., 1980. Repeated genes in eukaryotes. Annual Review in Biochemistry, 49, 727–764.Google Scholar
Lutz, R.A., 1988. Dispersal of organisms at deep-sea hydrothermal vents: a review. Oceanologica Acta, 8, 23–29. [Special issue.]Google Scholar
Lutz, R.A., Jablonski, D., Rhoads, D.C. & Turner, R.D., 1980. Larval dispersal of a deep-sea hydrothermal vent bivalve from the Galapagos Rift. Marine Biology, 57, 127–133.Google Scholar
Maruyama, T. & Kimura, M., 1980. Genetic variability and effective population size when local extinction and recolonization of subpopulations are frequent. Proceedings of the National Academy of Sciences of the United States of America, 77, 6710–6714.CrossRefGoogle ScholarPubMed
McCauley, D.E., 1991. Genetic consequences of local population extinction and recolonization. Trends in Ecology and Evolution, 6, 5–8.CrossRefGoogle ScholarPubMed
McHugh, D., 1989. Population structure and reproductive biology of two sympatric hydrothermal vent polychaetes, Paralvinella pandorae and P. palmiformis. Marine Biology, 103, 95–106.Google Scholar
McHugh, D., 1993. A comparative study of reproduction and development in the polychaete family Terebellidae. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 185, 153–167.Google Scholar
McHugh, D. & Tunnicliffe, V., 1994. Ecology and reproductive biology of the hydrothermal vent polychaete Amphisamytha galapagensis (Ampharetidae). Marine Ecology Progress Series, 106, 111–120.CrossRefGoogle Scholar
Nunney, L. & Campbell, K.A., 1993. Assessing minimum viable population size: demography meets population genetics. Trends in Ecology and Evolution, 8, 234—239.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E.R. & Maniatis, T., 1989. Molecular cloning: a laboratory manual. New York: Cold Spring Harbor Laboratory.Google Scholar
Slatkin, M., 1985. Gene flow in natural populations. Annual Review in Ecology and Systematics, 16, 393–430.CrossRefGoogle Scholar
Southern, E., 1975. Gel electrophoresis of restriction fragments. Methods in Enzymology, 68, 152–176.CrossRefGoogle Scholar
Tunnicliffe, V., 1991. The biology of hydrothermal vents: ecology and evolution. Oceanography and Marine Biology. Annual Review, 29, 319–407.Google Scholar
Tunnicliffe, V. & Juniper, S.K., 1990. Dynamic character of the hydrothermal vent habitat and the nature of sulphide chimney fauna. Progress in Oceanography, 24, 1–13.CrossRefGoogle Scholar
Van Dover, C.L., Factor, J.R., Williams, A.B. & Berg, C.J., 1985. Reproductive patterns of decapod crustaceans from hydrothermal vents. Bulletin of the Biological Society of Washington, 6, 223–227.Google Scholar
Wade, M.J. & McCauley, D.E., 1988. Extinction and recolonization: effects on the genetic differentiation of local populations. Evolution, 42, 995–1005.Google Scholar
Waples, R.S., 1989. A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics, 121, 379–391.CrossRefGoogle ScholarPubMed
Watremez, P. & Kervevan, C., 1990. Origine des variations de l'activité hydrothermale: premiers éléments de réponse d'un modèle numérique simple. Compte Rendus de I'Académie des Sciences de Paris, se´rie II, 311, 153–158.Google Scholar
Weir, B.S., 1990. Intraspecific differentiation. In Molecular systematics (ed. D.M., Hillis and C., Moritz), pp. 373–410. Sunderland: Sinauer Associates.Google Scholar
Weir, B.S. & Cockerham, C.C., 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.Google Scholar
Williams, N.A., Dixon, D.R., Southward, E.C. & Holland, P.W.H., 1993. Molecular evolution and diversification of the vestimentiferan tube worms. Journal of the Marine Biological Association of the United Kingdom, 73, 437–452.CrossRefGoogle Scholar
Williams, S.M., Desalle, R. & Strobeck, C., 1985. Homogenization of geographical variants at the non-transcribed spacer of rDNA in Drosophila mercatorum. Molecular Biology and Evolution, 2, 338–346.Google Scholar
Wright, S., 1965. The interpretation of population structure by F-statistics with regard to systems of mating. Evolution, 19, 395–420.Google Scholar
Zal, F., Desbruyères, D. & Jouin-Toulmond, C., 1994. Sexual dimorphism in Paralvinella grasslei, a polychaete annelid from deep-sea hydrothermal vents. Compte Rendus de I'Académie des Sciences de Paris, série III, 317, 42–48.Google Scholar
Zal, F., Jollivet, D., Chevaldonné, P. & Desbruyères, D., 1995. Population structure and reproductive biology of Paralvinella grasslei, a polychaete annelid from deep-sea hydrothermal vents. Marine Biology, 122, 637–648.CrossRefGoogle Scholar