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. 2001 Jan;157(1):317–330. doi: 10.1093/genetics/157.1.317

Nucleotide polymorphism and natural selection at the pantophysin (Pan I) locus in the Atlantic cod, Gadus morhua (L.).

G H Pogson 1
PMCID: PMC1461473  PMID: 11139512

Abstract

Molecular studies of nucleotide sequence variation have rarely attempted to test hypotheses related to geographically varying patterns of natural selection. The present study tested the role of spatially varying selection in producing significant linkage disequilibrium and large differences in the frequencies of two common alleles at the pantophysin (Pan I) locus among five populations of the Atlantic cod, Gadus morhua. Nucleotide sequences of 124 Pan I alleles showed strong evidence for an unusual mix of balancing and directional selection but no evidence of stable geographically varying selection. The alleles were highly divergent at both the nucleotide level (differing on average by 19 mutations) and at amino acid level (each having experienced three amino acid substitutions since diverging from a common ancestral allele). All six amino acid substitutions occurred in a 56-residue intravesicular loop (IV1 domain) of the vesicle protein and each involved a radical change. An analysis of molecular variation revealed significant heterogeneity in the frequencies of recently derived mutations segregating within both allelic classes, suggesting that two selective sweeps may be presently occurring among populations. The dynamic nature of the Pan I polymorphism in G. morhua and clear departure from equilibrium conditions invalidate a simple model of spatially varying selection.

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Selected References

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  1. Begun D. J., Aquadro C. F. Evolutionary inferences from DNA variation at the 6-phosphogluconate dehydrogenase locus in natural populations of drosophila: selection and geographic differentiation. Genetics. 1994 Jan;136(1):155–171. doi: 10.1093/genetics/136.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Begun D. J., Aquadro C. F. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992 Apr 9;356(6369):519–520. doi: 10.1038/356519a0. [DOI] [PubMed] [Google Scholar]
  3. Berry A., Kreitman M. Molecular analysis of an allozyme cline: alcohol dehydrogenase in Drosophila melanogaster on the east coast of North America. Genetics. 1993 Jul;134(3):869–893. doi: 10.1093/genetics/134.3.869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Braverman J. M., Hudson R. R., Kaplan N. L., Langley C. H., Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics. 1995 Jun;140(2):783–796. doi: 10.1093/genetics/140.2.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cavalli-Sforza L. L. Population structure and human evolution. Proc R Soc Lond B Biol Sci. 1966 Mar 22;164(995):362–379. doi: 10.1098/rspb.1966.0038. [DOI] [PubMed] [Google Scholar]
  6. Charlesworth B. Measures of divergence between populations and the effect of forces that reduce variability. Mol Biol Evol. 1998 May;15(5):538–543. doi: 10.1093/oxfordjournals.molbev.a025953. [DOI] [PubMed] [Google Scholar]
  7. Charlesworth B., Nordborg M., Charlesworth D. The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet Res. 1997 Oct;70(2):155–174. doi: 10.1017/s0016672397002954. [DOI] [PubMed] [Google Scholar]
  8. Cooke P. H., Oakeshott J. G. Amino acid polymorphisms for esterase-6 in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1426–1430. doi: 10.1073/pnas.86.4.1426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eanes W. F., Kirchner M., Yoon J., Biermann C. H., Wang I. N., McCartney M. A., Verrelli B. C. Historical selection, amino acid polymorphism and lineage-specific divergence at the G6pd locus in Drosophila melanogaster and D. simulans. Genetics. 1996 Nov;144(3):1027–1041. doi: 10.1093/genetics/144.3.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eanes W. F., Kirchner M., Yoon J. Evidence for adaptive evolution of the G6pd gene in the Drosophila melanogaster and Drosophila simulans lineages. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7475–7479. doi: 10.1073/pnas.90.16.7475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Excoffier L., Smouse P. E., Quattro J. M. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 1992 Jun;131(2):479–491. doi: 10.1093/genetics/131.2.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fernández-Chacón R., Südhof T. C. Genetics of synaptic vesicle function: toward the complete functional anatomy of an organelle. Annu Rev Physiol. 1999;61:753–776. doi: 10.1146/annurev.physiol.61.1.753. [DOI] [PubMed] [Google Scholar]
  13. Fu Y. X., Li W. H. Statistical tests of neutrality of mutations. Genetics. 1993 Mar;133(3):693–709. doi: 10.1093/genetics/133.3.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gaitanou M., Mamalaki A., Merkouri E., Matsas R. Purification and cDNA cloning of mouse BM89 antigen shows that it is identical with the synaptic vesicle protein synaptophysin. J Neurosci Res. 1997 Jun 15;48(6):507–514. [PubMed] [Google Scholar]
  15. Haass N. K., Kartenbeck M. A., Leube R. E. Pantophysin is a ubiquitously expressed synaptophysin homologue and defines constitutive transport vesicles. J Cell Biol. 1996 Aug;134(3):731–746. doi: 10.1083/jcb.134.3.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hasson E., Wang I. N., Zeng L. W., Kreitman M., Eanes W. F. Nucleotide variation in the triosephosphate isomerase (Tpi) locus of Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 1998 Jun;15(6):756–769. doi: 10.1093/oxfordjournals.molbev.a025979. [DOI] [PubMed] [Google Scholar]
  17. Hey J. The neutralist, the fly and the selectionist. Trends Ecol Evol. 1999 Jan;14(1):35–38. doi: 10.1016/s0169-5347(98)01497-9. [DOI] [PubMed] [Google Scholar]
  18. Hudson R. R., Bailey K., Skarecky D., Kwiatowski J., Ayala F. J. Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster. Genetics. 1994 Apr;136(4):1329–1340. doi: 10.1093/genetics/136.4.1329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hudson R. R., Kaplan N. L. The coalescent process in models with selection and recombination. Genetics. 1988 Nov;120(3):831–840. doi: 10.1093/genetics/120.3.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hudson R. R., Sáez A. G., Ayala F. J. DNA variation at the Sod locus of Drosophila melanogaster: an unfolding story of natural selection. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7725–7729. doi: 10.1073/pnas.94.15.7725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Johnston P. A., Jahn R., Südhof T. C. Transmembrane topography and evolutionary conservation of synaptophysin. J Biol Chem. 1989 Jan 15;264(2):1268–1273. [PubMed] [Google Scholar]
  22. Kaplan N. L., Hudson R. R., Langley C. H. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. doi: 10.1093/genetics/123.4.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Karotam J., Boyce T. M., Oakeshott J. G. Nucleotide variation at the hypervariable esterase 6 isozyme locus of Drosophila simulans. Mol Biol Evol. 1995 Jan;12(1):113–122. doi: 10.1093/oxfordjournals.molbev.a040180. [DOI] [PubMed] [Google Scholar]
  24. Katz L. A., Harrison R. G. Balancing selection on electrophoretic variation of phosphoglucose isomerase in two species of field cricket: Gryllus veletis and G. offnsylvanicus. Genetics. 1997 Oct;147(2):609–621. doi: 10.1093/genetics/147.2.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kliman R. M., Hey J. DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics. 1993 Feb;133(2):375–387. doi: 10.1093/genetics/133.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kreitman M., Hudson R. R. Inferring the evolutionary histories of the Adh and Adh-dup loci in Drosophila melanogaster from patterns of polymorphism and divergence. Genetics. 1991 Mar;127(3):565–582. doi: 10.1093/genetics/127.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Moriyama E. N., Powell J. R. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 1996 Jan;13(1):261–277. doi: 10.1093/oxfordjournals.molbev.a025563. [DOI] [PubMed] [Google Scholar]
  29. Pogson G. H., Mesa K. A., Boutilier R. G. Genetic population structure and gene flow in the Atlantic cod Gadus morhua: a comparison of allozyme and nuclear RFLP loci. Genetics. 1995 Jan;139(1):375–385. doi: 10.1093/genetics/139.1.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  31. Schaeffer S. W., Miller E. L. Estimates of gene flow in Drosophila pseudoobscura determined from nucleotide sequence analysis of the alcohol dehydrogenase region. Genetics. 1992 Oct;132(2):471–480. doi: 10.1093/genetics/132.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Simonsen K. L., Churchill G. A., Aquadro C. F. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics. 1995 Sep;141(1):413–429. doi: 10.1093/genetics/141.1.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stephan W., Mitchell S. J. Reduced levels of DNA polymorphism and fixed between-population differences in the centromeric region of Drosophila ananassae. Genetics. 1992 Dec;132(4):1039–1045. doi: 10.1093/genetics/132.4.1039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Strobeck C. Expected linkage disequilibrium for a neutral locus linked to a chromosomal arrangement. Genetics. 1983 Mar;103(3):545–555. doi: 10.1093/genetics/103.3.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Südhof T. C., Lottspeich F., Greengard P., Mehl E., Jahn R. A synaptic vesicle protein with a novel cytoplasmic domain and four transmembrane regions. Science. 1987 Nov 20;238(4830):1142–1144. doi: 10.1126/science.3120313. [DOI] [PubMed] [Google Scholar]
  36. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. doi: 10.1093/genetics/123.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Takahata N. A simple genealogical structure of strongly balanced allelic lines and trans-species evolution of polymorphism. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2419–2423. doi: 10.1073/pnas.87.7.2419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Takahata N., Nei M. Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics. 1990 Apr;124(4):967–978. doi: 10.1093/genetics/124.4.967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Taylor W. R. The classification of amino acid conservation. J Theor Biol. 1986 Mar 21;119(2):205–218. doi: 10.1016/s0022-5193(86)80075-3. [DOI] [PubMed] [Google Scholar]
  40. Windoffer R., Borchert-Stuhlträger M., Haass N. K., Thomas S., Hergt M., Bulitta C. J., Leube R. E. Tissue expression of the vesicle protein pantophysin. Cell Tissue Res. 1999 Jun;296(3):499–510. doi: 10.1007/s004410051310. [DOI] [PubMed] [Google Scholar]

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