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Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2004 Nov 22;271(1555):2351–2359. doi: 10.1098/rspb.2004.2852

Thermal selection of PGM allozymes in newly founded populations of the thermotolerant vent polychaete Alvinella pompejana.

Patrice Piccino 1, Frédérique Viard 1, Pierre-Marie Sarradin 1, Nadine Le Bris 1, Dominique Le Guen 1, Didier Jollivet 1
PMCID: PMC1691873  PMID: 15556887

Abstract

Alvinella pompejana lives on the top of chimneys at deep-sea hydrothermal vents of the East Pacific Rise. It is thought to be one of the most thermotolerant and eurythermal metazoans. Our experimental approach combines methods of population genetics and biochemistry, considering temperature as a potential selective factor. Phosphoglucomutase (Pgm-1 locus) is one of the most polymorphic loci of A. pompejana and exhibits four alleles, from which alleles 90 and 100 dominate with frequencies of approximately 0.5 in populations. Results from previous studies suggested that allele 90 might be more thermostable than allele 100. Significant genetic differentiation was found by comparing contrasted microhabitats, especially the young, still hot, versus older and colder chimneys, with allele 90 being at highest frequency on young chimneys. Moreover the frequency of allele 90 was positively correlated with mean temperature at the opening of Alvinella tubes. In parallel, thermostability and thermal optimum experiments demonstrated that allele 90 is more thermostable and more active at higher temperatures than allele 100. This dataset supports an additive model of diversifying selection in which allele 90 is favoured on young hot chimneys but counterbalanced over the whole metapopulation by the dynamics of the vent ecosystem.

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Selected References

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  1. Carter P. A., Watt W. B. Adaptation at specific loci. V. Metabolically adjacent enzyme loci may have very distinct experiences of selective pressures. Genetics. 1988 Aug;119(4):913–924. doi: 10.1093/genetics/119.4.913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Dawson D. M., Jaeger S. Heterogeneity of phosphoglucomutase. Biochem Genet. 1970 Feb;4(1):1–9. doi: 10.1007/BF00484014. [DOI] [PubMed] [Google Scholar]
  3. Gaill F., Mann K., Wiedemann H., Engel J., Timpl R. Structural comparison of cuticle and interstitial collagens from annelids living in shallow sea-water and at deep-sea hydrothermal vents. J Mol Biol. 1995 Feb 17;246(2):284–294. doi: 10.1006/jmbi.1994.0084. [DOI] [PubMed] [Google Scholar]
  4. Hoffmann R. J. Properties of allelic variants of phosphoglucomutase from the sea anemone Metridium senile. Biochem Genet. 1985 Dec;23(11-12):859–876. doi: 10.1007/BF00499934. [DOI] [PubMed] [Google Scholar]
  5. Johannesson K., Johannesson B., Lundgren U. Strong natural selection causes microscale allozyme variation in a marine snail. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2602–2606. doi: 10.1073/pnas.92.7.2602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Johnson K. S., Beehler C. L., Sakamoto-Arnold C. M., Childress J. J. In situ measurements of chemical distributions in a deep-sea hydrothermal vent field. Science. 1986 Mar 7;231(4742):1139–1141. doi: 10.1126/science.231.4742.1139. [DOI] [PubMed] [Google Scholar]
  7. Karl S. A., Avise J. C. Balancing selection at allozyme loci in oysters: implications from nuclear RFLPs. Science. 1992 Apr 3;256(5053):100–102. doi: 10.1126/science.1348870. [DOI] [PubMed] [Google Scholar]
  8. McDonald J. H., Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. doi: 10.1038/351652a0. [DOI] [PubMed] [Google Scholar]
  9. Nevo E., Shimony T., Libni M. Thermal selection of allozyme polymorphisms in barnacles. Nature. 1977 Jun 23;267(5613):699–701. doi: 10.1038/267699a0. [DOI] [PubMed] [Google Scholar]
  10. Place A. R., Powers D. A. Genetic variation and relative catalytic efficiencies: lactate dehydrogenase B allozymes of Fundulus heteroclitus. Proc Natl Acad Sci U S A. 1979 May;76(5):2354–2358. doi: 10.1073/pnas.76.5.2354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Pogson G. H. Biochemical characterization of genotypes at the phosphoglucomutase-2 locus in the Pacific oyster, Crassostrea gigas. Biochem Genet. 1989 Oct;27(9-10):571–589. [PubMed] [Google Scholar]
  12. Pogson G. H. Expression of overdominance for specific activity at the phosphoglucomutase-2 locus in the Pacific oyster, Crassostrea gigas. Genetics. 1991 May;128(1):133–141. doi: 10.1093/genetics/128.1.133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Pradillon F., Shillito B., Young C. M., Gaill F. Deep-sea ecology. Developmental arrest in vent worm embryos. Nature. 2001 Oct 18;413(6857):698–699. doi: 10.1038/35099674. [DOI] [PubMed] [Google Scholar]
  14. Somero G. N. Proteins and temperature. Annu Rev Physiol. 1995;57:43–68. doi: 10.1146/annurev.ph.57.030195.000355. [DOI] [PubMed] [Google Scholar]
  15. Verrelli B. C., Eanes W. F. Clinal variation for amino acid polymorphisms at the Pgm locus in Drosophila melanogaster. Genetics. 2001 Apr;157(4):1649–1663. doi: 10.1093/genetics/157.4.1649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Verrelli B. C., Eanes W. F. Extensive amino acid polymorphism at the pgm locus is consistent with adaptive protein evolution in Drosophila melanogaster. Genetics. 2000 Dec;156(4):1737–1752. doi: 10.1093/genetics/156.4.1737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Verrelli B. C., Eanes W. F. The functional impact of Pgm amino acid polymorphism on glycogen content in Drosophila melanogaster. Genetics. 2001 Sep;159(1):201–210. doi: 10.1093/genetics/159.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Watt W. B., Carter P. A., Blower S. M. Adaptation at specific loci. IV. Differential mating success among glycolytic allozyme genotypes of Colias butterflies. Genetics. 1985 Jan;109(1):157–175. doi: 10.1093/genetics/109.1.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Watt W. B., Dean A. M. Molecular-functional studies of adaptive genetic variation in prokaryotes and eukaryotes. Annu Rev Genet. 2000;34:593–622. doi: 10.1146/annurev.genet.34.1.593. [DOI] [PubMed] [Google Scholar]

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