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. 1988 Aug;119(4):913–924. doi: 10.1093/genetics/119.4.913

Adaptation at Specific Loci. V. Metabolically Adjacent Enzyme Loci May Have Very Distinct Experiences of Selective Pressures

P A Carter 1, W B Watt 1
PMCID: PMC1203474  PMID: 2970419

Abstract

The polymorphic phosphoglucomutase (PGM) and glucose-6-phosphate dehydrogenase (G6PD) loci have been studied in parallel to experimental work on the phosphoglucose isomerase (PGI) polymorphism in Colias butterflies. PGI, PGM and G6PD are also autosomal in Colias. PGM and G6PD are loosely linked (and represent the first identified autosomal linkage group in Colias); they assort independently from PGI. Recombination occurs in both sexes. Neither PGM nor G6PD shows large, consistent differences in flight capacity through the day among its genotypes, as PGI does. PGM shows some change of allele frequencies, and match to Hardy-Weinberg expectation, with air temperature in middle and latter parts of the season, but not early in the season. G6PD may show some heterozygote excess over Hardy-Weinberg expectation early in the day, but more testing is needed. No evidence for differential survivorship was seen at PGM or G6PD, in contrast to PGI. At the PGM and G6PD loci, male heterozygotes are advantaged in mating with females, but without the evidence of female choice which occurs for PGI. These effects are not correlated among the three loci. There is no assortative mating at G6PD (nor at PGI). There is minor positive assortative mating of PGM heterozygotes, but it is too weak to account for the PGM-genotype-specific male mating advantage. No trends of multilocus genotype frequencies involving PGI are seen. Certain PGM-G6PD two-locus genotypes are over-represented, and others under-represented, in wild adult samples, particularly among males and uniformly among successfully mating males. Our results emphasize that enzyme loci sharing a substrate need not have common experience of the existence or strength of natural selection, and suggest initial food-resource processing and allocation as a possible context for fitness-related effects of the PGM and G6PD polymorphisms.

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Selected References

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  1. Asmussen M. A., Clegg M. T. Dynamics of the Linkage Disequilibrium Function under Models of Gene-Frequency Hitchhiking. Genetics. 1981 Oct;99(2):337–356. doi: 10.1093/genetics/99.2.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bijlsma R. Polymorphism at the G6PD and 6PGD loci in Drosophila melanogaster. II. Evidence for interaction in fitness. Genet Res. 1978 Jun;31(3):227–237. doi: 10.1017/s0016672300018012. [DOI] [PubMed] [Google Scholar]
  3. Bijlsma R. Polymorphism at the G6pd and 6Pgd loci in Drosophila melanogaster. IV. Genetic factors modifying enzyme activity. Biochem Genet. 1980 Aug;18(7-8):699–715. doi: 10.1007/BF00484587. [DOI] [PubMed] [Google Scholar]
  4. Bijlsma R., van der Meulen-Bruijns C. Polymorphism at the G6pd and 6Pgd loci in Drosophila melanogaster. III. Developmental and biochemical aspects. Biochem Genet. 1979 Dec;17(11-12):1131–1144. doi: 10.1007/BF00504350. [DOI] [PubMed] [Google Scholar]
  5. Cavener D. R., Clegg M. T. Dynamics of correlated genetic systems. IV. Multilocus effects of ethanol stress environments. Genetics. 1978 Nov;90(3):629–644. doi: 10.1093/genetics/90.3.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cavener D. R., Clegg M. T. Evidence for biochemical and physiological differences between enzyme genotypes in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4444–4447. doi: 10.1073/pnas.78.7.4444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cavener D. R. The Response of Enzyme Polymorphisms to Developmental Rate Selection in DROSOPHILA MELANOGASTER. Genetics. 1983 Sep;105(1):105–113. doi: 10.1093/genetics/105.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Charlesworth B., Charlesworth D. A study of linkage disequilibrium in populations of Drosophila melanogaster. Genetics. 1973 Feb;73(2):351–359. doi: 10.1093/genetics/73.2.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Clegg M. T., Kidwell J. F., Horch C. R. Dynamics of Correlated Genetic Systems. V. Rates of Decay of Linkage Disequilibria in Experimental Populations of DROSOPHILA MELANOGASTER. Genetics. 1980 Jan;94(1):217–234. doi: 10.1093/genetics/94.1.217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eanes W. F., Bingham B., Hey J., Houle D. Targeted selection experiments and enzyme polymorphism: negative evidence for octanoate selection at the G6PD locus in Drosophila melanogaster. Genetics. 1985 Feb;109(2):379–391. doi: 10.1093/genetics/109.2.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Eanes W. F., Hey J. IN VIVO Function of Rare G6pd Variants from Natural Populations of DROSOPHILA MELANOGASTER. Genetics. 1986 Jul;113(3):679–693. doi: 10.1093/genetics/113.3.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Epperson B. K., Allard R. W. Linkage Disequilibrium between Allozymes in Natural Populations of Lodgepole Pine. Genetics. 1987 Feb;115(2):341–352. doi: 10.1093/genetics/115.2.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Giles N. H., Case M. E., Baum J., Geever R., Huiet L., Patel V., Tyler B. Gene organization and regulation in the qa (quinic acid) gene cluster of Neurospora crassa. Microbiol Rev. 1985 Sep;49(3):338–358. doi: 10.1128/mr.49.3.338-358.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gillespie J. H., Kojima K. The degree of polymorphisms in enzymes involved in energy production compared to that in nonspecific enzymes in two Drosophila ananassae populations. Proc Natl Acad Sci U S A. 1968 Oct;61(2):582–585. doi: 10.1073/pnas.61.2.582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hochachka P. W. Action of temperature on branch points in glucose and acetate metabolism. Comp Biochem Physiol. 1968 Apr;25(1):107–118. doi: 10.1016/0010-406x(68)90917-1. [DOI] [PubMed] [Google Scholar]
  16. Laurie-Ahlberg C. C. Genetic variation affecting the expression of enzyme-coding genes in Drosophila: an evolutionary perspective. Isozymes Curr Top Biol Med Res. 1985;12:33–88. [PubMed] [Google Scholar]
  17. Prakash S., Lewontin R. C. A molecular approach to the study of genic heterozygosity in natural populations. 3. Direct evidence of coadaptation in gene arrangements of Drosophila. Proc Natl Acad Sci U S A. 1968 Feb;59(2):398–405. doi: 10.1073/pnas.59.2.398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Prakash S., Lewontin R. C. A molecular approach to the study of genic heterozygosity in natural populations. V. Further direct evidence of coadaptation in inversions of Drosophila. Genetics. 1971 Nov;69(3):405–408. doi: 10.1093/genetics/69.3.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Riddle R. A., Iverson V., Dawson P. S. Dietary Effects on Fitness Components at the PGM-1 Locus of TRIBOLIUM CASTANEUM. Genetics. 1983 Jan;103(1):65–73. doi: 10.1093/genetics/103.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Snyder L. R. Evolutionary conservation of linkage groups: additional evidence from murid and cricetid rodents. Biochem Genet. 1980 Apr;18(3-4):209–220. doi: 10.1007/BF00484237. [DOI] [PubMed] [Google Scholar]
  21. Thomson G. The effect of a selected locus on linked neutral loci. Genetics. 1977 Apr;85(4):753–788. doi: 10.1093/genetics/85.4.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Turner J. R., Sheppard P. M. Absence of crossing-over in female butterflies (Heliconius). Heredity (Edinb) 1975 Apr;34(Pt 2):265–269. doi: 10.1038/hdy.1975.29. [DOI] [PubMed] [Google Scholar]
  23. Watt W. B. Adaptation at Specific Loci. II. Demographic and Biochemical Elements in the Maintenance of the Colias Pgi Polymorphism. Genetics. 1983 Apr;103(4):691–724. doi: 10.1093/genetics/103.4.691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Watt W. B. Adaptation at specific loci. I. Natural selection on phosphoglucose isomerase of Colias butterflies: Biochemical and population aspects. Genetics. 1977 Sep;87(1):177–194. doi: 10.1093/genetics/87.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Watt W. B. Allelic isozymes and the mechanistic study of evolution. Isozymes Curr Top Biol Med Res. 1985;12:89–132. [PubMed] [Google Scholar]
  26. Watt W. B., Boggs C. L. Allelic isozymes as probes of the evolution of metabolic organization. Isozymes Curr Top Biol Med Res. 1987;15:27–47. [PubMed] [Google Scholar]
  27. 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]
  28. Watt W. B., Carter P. A., Donohue K. Females' choice of "good genotypes" as mates is promoted by an insect mating system. Science. 1986 Sep 12;233(4769):1187–1190. doi: 10.1126/science.3738528. [DOI] [PubMed] [Google Scholar]
  29. Watt W. B., Cassin R. C., Swan M. S. Adaptation at Specific Loci. III. Field Behavior and Survivorship Differences among Colias Pgi Genotypes Are Predictable from IN VITRO Biochemistry. Genetics. 1983 Apr;103(4):725–739. doi: 10.1093/genetics/103.4.725. [DOI] [PMC free article] [PubMed] [Google Scholar]

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