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Population Size, Natural Selection and the Genetic Load

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Population Size, Natural Selection and the Genetic Load 700 NATURE. VOL. 218. MAY 18. 1968 GENERAL density-dependent selection. In general the fitness of any genotype can be described by the equation Population Size, Natural Selection and the Genetic Load How great a genetic load can a population tolerate? This where the ks are constants, j(q) is a function of gene (or 1 subject has recently been discussed by several authors - o• genotype) frequency, j(d) is a function of population We believe that a most important point can be stated density, and i and c indicate, respectively, that the function briefly: because most organisms produce far more offspring is unique to that genotype or is shared by all genotypes than are necessary to maintain a constant population in the population. (To make the equation completely density, and because population densities remain, very general, we should include all the products of the j( ) roughly, constant, many individuals die before they are terms.) Then k; is the loaded selection, j;(q), j;(d) and mature; it does not matter whether they die of starvation, j;(q,d) are the frequency-dependent, density-dependent and accidents or from genetic ailments; the population can population-dependent parts of selection, jdd) represents still maintain itself. It is not so much that there is a density-dependent population control andjc(q) represents genetic load which might threaten the species, but that gene-frequency-dependent population control (which will there is an ecological load, resulting from density probably often be zero). regulation, which because it must, as Darwin noted, The great increase in variability observed in the produce natural selection, gives rise to the apparent butterfly Melitaea aurinia while the population was genetic load. A population will be able to tolerate what expandinglO was probably, as Ford suggests, an indication seems to us a considerable genetic load, without being, that density or population-dependent selection had been on that account, in any danger of extinction. The genetic much reduced, allowing survival of extreme phenotypes load is, for the most part, merely an expression of the and an increase in numbers. The viability of bar genotypes fact that not all genotypes are equally viable when the in Drosophila varies with popUlation densityll. Harding population becomes crowded. Many individuals have to et al." have shown selection in Phaseolus lunatus which die in the process of density regulation, and if those is certainly frequency-dependent and may also be density­ which die differ genetically from those which survive, we dependent. will observe a "genetic load". This is the crux of the Selection which is frequency-dependent produces little Malthus-Darwin concept of selection. This does not of or no genetic load at equilibrium, but does produce a course apply to genetic conditions which are markedly genetic load at other gene frequencies. Density-dependent disabling at all population densities; there must be a selection never produces a "genetic load" in the ecological decided limit (although a fairly high one, for the dead sense (although it will do so in terms of human values), individuals simply leave more food or space for others, for selection acts only when the population has to be which otherwise would die) to the number of these which "thinned" in any case because it is becoming too dense. a population can contain. We suggest the term "loaded" Although other forms of selection no doubt maintain some for this last kind of selection. polymorphisms, we suggest that the majority must be It is quite possible that many of the biochemical maintained by population-dependent selection, with a polymorphisms of Drosophila pseudoobscura1 are main­ small residue of "loaded" selection, and that this is how tained by density-dependent natural selection-some Drosophila pseudoobscura, and no doubt other species, genotypes, probably homozygotes, are less viable than can be polymorphic. The populations would be in no others when the population is crowded, and it has been danger if they became inbred. shown2- 4 that this could maintain polymorphisms at Loaded selection, frequency density and population­ perhaps a thousand loci. dependent selection do not, ipso jacto, maintain poly. We must distinguish between density-dependent and morphism; but all of them can do so, in complete accord frequency-dependent selection. If the organism con­ with the facts of genetics and ecology. In saying this, we l3 l4 taminates its environment and if the contaminant is are re-stating the arguments of Cain and Sheppard • removed at a constant rate, then the denser the population and of Darwin. In view of the mounting importance of the greater the amount of contaminant. If some geno­ eugenic as well as demographic problems for man as a types suffer more than others from the contaminant, then species, we think it of great importance to understand this component of natural selection is purely density­ the relations between these various causes of death. dependent. If the fitness of a genotype depends entirely We thank all those who discussed these problems at the on its frequency relative to other genotypes, irrespective meeting of the Population Genetics Group at Birmingham of popUlation density (as with assortative mating or in January 1968. Batesian mimicry within moderate limits of population density), then selection is purely frequency-dependent. J. R. G. TURNER 7 Both kinds of selection can maintain polymorphism-. • M. H. WILLIAMSON It is probably commoner for selection to be both frequency and density-dependent. If the densities of Department of Biology, different genotypes are limited by different factors in the University of York. environment, then the fitness (rate of survival and repro· duction) of a genotype will depend on its density. The Received ]'ebruary 26. 1968. density of a genotype is a direct function of its frequency and of the density of the population, so that selection is 1 Lewontin. R. C.. and Hubby. J. L., Genet;cs, 54, 595 (1966). dependent on both these two variables. Kojima and • Sved, J. A., Reed, T. E., and Bodmer, W. F., (Jenetics, 55, 469 (1987). 8 • King, J. L., Genetics, 55, 483 (1967). Yarbrough misleadingly call this type of selection • Milkman, R. D., Genetics, 55, 493 (1967). "frequency-dependent". Perhaps it should be called popu­ • Feller, W. B .. Genet. Res., Oambridge, 9, 1 (1967). lation-dependent. • Williamson, M. H., Nature, 180, 422 (1957). Levene's· much quoted model of differential selection 1 Turner, J. R. G .• Proc. Roy. Soc., B, 169, 31 (1967). 'Kojima, K., and Yarhrough, K. M., Proc. US Nat. Acad. Sci., 57. 645 in different "niches" can be conceived as an elaborate (1967). kind of population-dependence. Models have been • Levene, H., Amer. Naturalist, 87, 257 (1953). suggested in which a certain percentage of the population 10 Ford, E. B., Ecological Genetics, chap. 2 (Methuen, London, 1964). survives'-4 ; if the survivors tend to be heterozygous at n Bentvelzen, P., Genetica, 34, 229 (1963). 12 Harding, J., Allard, R. W .• and Smeltzer, D. G., Proc. US Nat. Acad. Sci., more loci than are those which die, these loci remain 56. 99 (1966). polymorphic. Because the percentage surviving depends is Cain. A. J., and Sheppard, P. M .• Amer. Naturatist, 88, 321 (1954). on population density, these models correspond with our "Cain. A. J., and Sheppard, P. M., Amer. Naturatist, 90, 202 (1956). © 1968 Nature Publishing Group.
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