Just as drift causes changes in allele frequencies, it also changes multilocus gamete frequencies. Genetic drift tends to create linkage disequilibrium and associations between loci by chance alone. As we consider more and more loci simultaneously, we subdivide any finite gene pool into more and more gametic categories, thereby tending to make any one particular gamete type more rare. Sampling error is a strong force of evolutionary change for any gamete type that is rare in a gene pool, so in general genetic drift is a more powerful force for altering gamete frequencies at the multilocus level than at the single-locus level.
The increased sensitivity of linkage disequilibrium to drift compared to allele frequencies is illustrated by a study of 34 X-linked microsatellite loci in the United Kingdom and in 10 regions in Scotland (Vitart et al. 2005)—the urban region of Edinburgh and 9 rural regions. The rural regions had smaller populations sizes (but still in the tens of thousands or above) and less gene flow. There was little overall differentiation among these subpopulations in allele frequencies, but these areas showed large differences in the amount of linkage disequilibrium. Because several X-linked loci were available, one convenient measure of overall disequilibrium is the map distance in centimorgans at which the linkage disequilibrium on the X chromosome is half the difference between its maximum and minimum values, called the LD half distance. These are plotted in Figure 4.8. The large populations in the United Kingdom and in Edinburgh had no overall linkage disequilibrium by this measure, but several of the rural regions did have significant overall disequilibrium. Thus, differentiation could be observed at the level of linkage disequilibrium even though it was absent in terms of single-locus allele frequencies.
Founder and bottleneck effects are particularly effective in creating linkage disequilibrium and chance associations. If the loci are closely linked, the specific associations created by a founder or bottleneck episode can persist for many generations. For example, linkage disequilibrium occurs in a human population living in southern Italy west of the Apennine mountain range (Filosa et al. 1993). A 3-Mb telomeric region of the human X chromosome contains the genes for the enzyme glucose-6-phosphate dehydrogenase (G6PD) and red/green color vision. Nearly 400 distinct mutants are known at the G6PD locus that result in a deficiency of G6PD activity, which in turn can cause hemolytic anemia in individuals hemizygous or homozygous for a deficient allele. This population west of the Apennines has a unique deficiency allele (Medl), indicating both a founder effect and the relative genetic isolation of this area. Most remarkably, all Medl G6PD-deficient males also had red/green color blindness (which is controlled by a small complex of tightly linked genes). Interestingly, on the nearby island of Sardinia, there is also remarkable homogeneity for G6PD-deficient alleles (Frigerio et al. 1994), consistent with a founder effect most likely due to Phoenician contact with the island in the fifth century BCE (Filippi et al. 1977). But
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