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1947 Measuring selection and drift in a natural population
CHAPTER TWELVE
1947 Measuring selection and drift in a natural population The concept Using six consecutive years of allele frequency changes and population size estimates in the moth Panaxia dominula, Ronald A. Fisher and Edmund B. Ford (1947) tested the relative importance of selection and drift on allele frequency variation. While they found that the variation in allele frequencies was greater than expected from drift alone, their research marks the first of many efforts to sort out the evolutionary importance of drift and selection in natural populations.
The explanation Sewell Wright (1931) emphasized the important role of random genetic drift in the evolutionary process. He suggested that in moderate-size populations drift would act to change allele frequencies in a direction that might not be favored by natural selection but could allow the population to explore the fitness landscape and possibly evolve to a higher fitness plateau. Fisher was not sympathetic to this view and the data collected by E. B. Ford allowed a direct comparison of the impact of selection and drift on allele frequency variation. Ford had worked with a single locus wing color polymorphism in the moth Panaxia dominula. From 1941 to 1946, collections made at Oxford, UK provided yearly estimates of the frequency of the medionigra allele. The adult moths were mostly active during the month of July for 12e23 days. During this time, individual moths would be marked and then the frequency of recaptures would be recorded. These data allowed Fisher and Ford to estimate the size of the adult population. Fisher realized that the estimated frequency of the medionigra allele would vary due to two different sampling processes; the finite breeding population (e.g. drift) and the number of adults sampled to estimate the medionigra allele frequency. Fisher then devised a statistical test to see if the allele frequency variation over a six year sampling period was about what was expected from Conceptual Breakthroughs in Evolutionary Ecology ISBN: 978-0-12-816013-8 https://doi.org/10.1016/B978-0-12-816013-8.00012-0
© 2020 Elsevier Inc. All rights reserved.
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Conceptual Breakthroughs in Evolutionary Ecology
drift and allele frequency estimation or if it was greater than this, as might be expected if selection was acting on this polymorphisms but changing direction over time. The estimates of population size were crude, so Fisher and Ford (1947) set the effective population size to be constant and at the lowest number seen over their six-year sample. They found that the observed variation was significantly greater than expected by drift and sampling alone. Fisher and Ford (1947) then concluded “Thus our analysis, the first in which the relative parts played by random survival and selection in a wild population can be tested, does not support the view that chance fluctuations in gene-ratios, such as may occur in very small isolated populations, can be of any significance in evolution.” The last part of this statement is a little strong given that at best this study was on a single population. Nevertheless, this work showed the power of combining evolutionary theory, statistics, and detailed field observation in an evolutionary study. Thirty years later, as many more datasets of allele frequency time-series in natural populations became available, Schaffer et al. (1977) published an improved version of Fisher and Ford’s test. However, both Schaffer et al. (1977) and Fisher and Ford (1947) only had estimates of the census population size. Mueller et al. (1985) made actual estimates of effective population size from demographic and census data of butterfly populations and used computer simulations to derive drift and sampling-only expectations.
Impact: 8 This work is a pioneering application of modern statistical techniques to analyze the two major evolutionary forces of drift and natural selection in a natural population. The fact that a similar study did not happen for another 30 years shows how far ahead of its time Fisher and Ford’s work was.
References Fisher, R.A., Ford, E.B., 1947. The spread of a gene in natural conditions in a colony of the moth Panaxia dominula L. Heredity 1, 143e174. Mueller, L.D., Wilcox, B.A., Ehrlich, P.R., Heckel, D.G., Murphy, D.D., 1985. A direct assessment of the role of genetic drift in determining allele frequency variation in populations of Euphydryas editha. Genetics 110, 495e511. Schaffer, H.E., Yardley, D., Anderson, W.W., 1977. Drift or selection: a statistical test of gene frequency variation over generations. Genetics 87, 371e379. Wright, S., 1931. Evolution in mendelian populations. Genetics 16, 97e159.
1947 Measuring selection and drift in a natural population The concept Using six consecutive years of allele frequency changes and population size estimates in the moth Panaxia dominula, Ronald A. Fisher and Edmund B. Ford (1947) tested the relative importance of selection and drift on allele frequency variation. While they found that the variation in allele frequencies was greater than expected from drift alone, their research marks the first of many efforts to sort out the evolutionary importance of drift and selection in natural populations.
The explanation Sewell Wright (1931) emphasized the important role of random genetic drift in the evolutionary process. He suggested that in moderate-size populations drift would act to change allele frequencies in a direction that might not be favored by natural selection but could allow the population to explore the fitness landscape and possibly evolve to a higher fitness plateau. Fisher was not sympathetic to this view and the data collected by E. B. Ford allowed a direct comparison of the impact of selection and drift on allele frequency variation. Ford had worked with a single locus wing color polymorphism in the moth Panaxia dominula. From 1941 to 1946, collections made at Oxford, UK provided yearly estimates of the frequency of the medionigra allele. The adult moths were mostly active during the month of July for 12e23 days. During this time, individual moths would be marked and then the frequency of recaptures would be recorded. These data allowed Fisher and Ford to estimate the size of the adult population. Fisher realized that the estimated frequency of the medionigra allele would vary due to two different sampling processes; the finite breeding population (e.g. drift) and the number of adults sampled to estimate the medionigra allele frequency. Fisher then devised a statistical test to see if the allele frequency variation over a six year sampling period was about what was expected from Conceptual Breakthroughs in Evolutionary Ecology ISBN: 978-0-12-816013-8 https://doi.org/10.1016/B978-0-12-816013-8.00012-0
© 2020 Elsevier Inc. All rights reserved.
29
j
30
Conceptual Breakthroughs in Evolutionary Ecology
drift and allele frequency estimation or if it was greater than this, as might be expected if selection was acting on this polymorphisms but changing direction over time. The estimates of population size were crude, so Fisher and Ford (1947) set the effective population size to be constant and at the lowest number seen over their six-year sample. They found that the observed variation was significantly greater than expected by drift and sampling alone. Fisher and Ford (1947) then concluded “Thus our analysis, the first in which the relative parts played by random survival and selection in a wild population can be tested, does not support the view that chance fluctuations in gene-ratios, such as may occur in very small isolated populations, can be of any significance in evolution.” The last part of this statement is a little strong given that at best this study was on a single population. Nevertheless, this work showed the power of combining evolutionary theory, statistics, and detailed field observation in an evolutionary study. Thirty years later, as many more datasets of allele frequency time-series in natural populations became available, Schaffer et al. (1977) published an improved version of Fisher and Ford’s test. However, both Schaffer et al. (1977) and Fisher and Ford (1947) only had estimates of the census population size. Mueller et al. (1985) made actual estimates of effective population size from demographic and census data of butterfly populations and used computer simulations to derive drift and sampling-only expectations.
Impact: 8 This work is a pioneering application of modern statistical techniques to analyze the two major evolutionary forces of drift and natural selection in a natural population. The fact that a similar study did not happen for another 30 years shows how far ahead of its time Fisher and Ford’s work was.
References Fisher, R.A., Ford, E.B., 1947. The spread of a gene in natural conditions in a colony of the moth Panaxia dominula L. Heredity 1, 143e174. Mueller, L.D., Wilcox, B.A., Ehrlich, P.R., Heckel, D.G., Murphy, D.D., 1985. A direct assessment of the role of genetic drift in determining allele frequency variation in populations of Euphydryas editha. Genetics 110, 495e511. Schaffer, H.E., Yardley, D., Anderson, W.W., 1977. Drift or selection: a statistical test of gene frequency variation over generations. Genetics 87, 371e379. Wright, S., 1931. Evolution in mendelian populations. Genetics 16, 97e159.