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Genic Variability and Strategies of Adaptation in Animals (Allozymes/Heterozygosity/Polymorphism/Environmental Grain) ROBERT K

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Genic Variability and Strategies of Adaptation in Animals (Allozymes/Heterozygosity/Polymorphism/Environmental Grain) ROBERT K Proc. Nat. Acad. Sci. USA Vol. 70, No. 6, pp. 1875-1877, June 1973 Genic Variability and Strategies of Adaptation in Animals (allozymes/heterozygosity/polymorphism/environmental grain) ROBERT K. SELANDER AND DONALD W. KAUFMAN Department of Zoology, University of Texas, Austin, Tex. 78712 Communicated by Verne Grant, April 6, 1973 ABSTRACT Levels of genie heterozygosity, as mea- averaging 15%. [In Table 1, values for horseshoe crab, sured by surveys of allozymic variation, are much lower in sparrow, and two rodent genera (Dipodomys and Sigmodon) populations of large, mobile animals (most vertebrates) than in those of small, relatively immobile animals (most have been increased by 70% over observed values to com- invertebrates). This difference is not consistent with pensate for the fact that esterases, which are highly poly- theories relating variability to population size (species morphic enzymes (5), were not included in the samples of number) or dispersal ability (gene flow), but it is predicted loci assessed.] As a rule, local populations of vertebrates have by Levins' theory of adaptive strategies in relation to no more than four alleles at frequencies greater than 1% per environmental uncertainty ("grain"). Mobility and de- for gree of homeostatic control apparently are important locus, and over half the polymorphic loci are segregating factors influencing levels ofgenic heterozygosity in natural only two common alleles. In contrast, the smaller inverte- populations. The results argue indirectly that at least a brates have one more allele per polymorphic locus on the major proportion of allozymic variation is maintained by natural selection. TABLE 1. Estimates of genic heterozygosity per population Although classical research on viability and morphologic characters had suggested the existence of much cryptic genic variation in plants and animals (1), the concept of a high level No. of No. of Heterozygosity of polymorphism as the usual condition in populations was Organism* species loci Mean Range not firmly established until 1966, when surveys of allozymic Invertebrates estimates of genic heterozygosity variation yielded direct Drosophila 19 11-33 0.145 0.05-0.22 (mean proportion of loci in heterozygous state per individual) Field cricket 1 20 0.145 for Drosophila pseudoobscura (2) and the British human Land snails 3 17 0.207 0.14-0.25 population (3). Extrapolations from these and other surveys Horseshoe crab 1 25 0.097 of electrophoretically demonstrable variation in proteins lead 24 0.1507 to the conclusion that most diploid organisms are polymorphic Total at thousands of structural gene loci and that every individual Vertebrates has a unique protein complement (4, 5). Fish (Tetra) 1 17 0.112 - The rationale behind the approach of estimating total Lizards 4 15-29 0.058 0.05-0.07 genic heterozygosity in genomes by electrophoretic analysis Sparrow 1 15 0.059 - of randomly selected samples of loci encoding enzymes and Rodents 14 18-41 0.056 0.01-0.09 other proteins is discussed by Hubby and Lewontin (6). Seal 1 19 0.030 Because of our profound ignorance of the composition of Man (European) 1 70 0.067 genomes and, particularly, the number and proportion of Total 22 0.0584 structural genes (7), the degree of confidence to be attached to extrapolations from small samples of loci is uncertain. Ad- * Species and references: Drosophila pseudoobscura, D. per- ditionally, the contribution of individual loci to estimates of similis, D. obscura, D. subobscura, D. willistoni, D. equinoxialis, overall heterozygosity is so variable (5, 8-10) that sampling D. paulistorum (23), D. tropicalis (10), D. melanogaster, D. simu- error among loci undoubtedly is an important source of varia- lans (8), and nine species of the D. virilis group (L. H. Throck- tion. Yet the general consistency of estimates for very different morton and J. L. Hubby, in preparation); Gryllus integer (Selan- types of organisms suggests that they index some basic param- der, in preparation); Helix aspersa, Mesodon roemeri, and Rab- eter of genetic variability. This idea is supported by recent dotus mooreanus (Kaufman and Selander, in preparation); demonstrations of positive correlations between degrees of Limulus polyphemus (24); Astyanax mexicanus (25); Uta stans- caro- morphologic and allozymic variability in some plants and buriana, Sceloporus graciosus, S. grammicus, and Anolis animals (11). linensis (26); Zonotrichia capensis (27); Dipodomys ordii and D. merriami (16), Eutamias panamintinus Mus musculus, based on samples of Estimates of genic heterozygosity, Sigmodon hispidus, S. arizonae, Thom'omys bottae, T. umbrinus, 11-70 loci, are available for 46 species of animals having large Peromyscus polionotus, and P. floridanus (28), P. leucopus and continental or marine distributions (Table 1). For tetrapods, P. gossypinus (Smith, Selander & Johnson, in preparation), including man, the estimates are surprisingly consistent at Geomys personatus, and G. arenarius (Kaufman et al., in prepara- around 6%, but those for invertebrates are much higher, tion); Mirounga leonina (29); Homo sapiens (30). 1875 Downloaded by guest on September 24, 2021 1876 Zoology: Selander and Kaufman Proc. Nat. Acad. Sci. USA 70 (1978) average, and- it is not unusual to find 10 or more alleles seg- spatial and temporal changes. And for temperature and some regating at esterase loci (12). Proportions of polymorphie other factors, larger size, itself, may increase homeostasis. loci range generally from 10 to 20% in vertebrates and from Moreover, because the fitness set (an expression of individual 25 to 50% in invertebrates. Thus, several indices demonstrate developmental and functional tolerance relative to a range of a major difference in level of genie variability between verte- environmental conditions) becomes more convex as homeo- brates and invertebrates. stasis increases, there is a decreasing probability that adapta- Clearly this difference cannot be related to dispersal ability, tion will involve the maintenance of differentially adapted since both snails and flying insects are highly polymorphic. morphs. [Using a diffusion-model approach to explore rela- Nor is it likely that the difference can be related to total tionships between genetic variability and environmental species number, following the argument of Kimura and Ohta patchiness, J. Gillespie (in preparation) also has predicted that (13), because the endemic Hawaiian species of Drosophila, the likelihood of polymorphism in organisms decreases with which have numbers several orders of magnitude smaller increasing homeostatic control.] than those of continental species, are on the average no less Vertebrates, with generally larger body size, greater mo- polymorphic (studies of 23 species by W. E. Johnson, personal bility, and greater homeostatic control, are expected to pursue communication). Even for the continental species of Droso- a different adaptive strategy than invertebrates when the phila, serious difficulties are encountered in attempting to tolerance of the individual genotype is exceeded by the range explain observed levels of heterozygosity and the general of environmental conditions likely to be experienced ("con- geographic uniformity of allele frequencies in terms of genetic cave fitness set" in Levins' terminology). For a population of drift of neutral or nearly neutral alleles (14). For snails, with organisms experiencing the environment as fine-grained, the severely limited migration, the effective population size can- optimum strategy is more often a single phenotype special- not be equivalent to the total species number or any signif- ized to the most frequently encountered set of conditions. icant part of it. In urban populations of Helix aspersa, for But a coarse-grained environment more often dictates a example, there is essentially no migration between colonies strategy in which specialized morphs occur in proportions de- on adjacent city blocks (Selander and Kaufman, in prepara- pendent upon the frequencies of the different environmental tion). If we exclude small insular populations and those having patches. Thus, Levins' model predicts that the probability of recently experienced severe reductions in numbers, there is no the optimum adaptive strategy involving alternate or multiple apparent relationship between level of genic variability and phenotypic and genotypic equilibria decreases with increasing population size or extent of range (5, 15, 16). size and mobility, and that genetic polymorphism occurs less The idea that types and levels of genetic variation in frequently in large, mobile organisms than in small, immobile populations can be related to temporal and spatial patterns ones. The estimates of genic heterozygosity in Table 1 are of environmental variation has been a persistent theme in consistent with this prediction not only between vertebrates evolutionary biology (17), although only recently have and invertebrates, but also within each group. The horseshoe rigorous, quantitative statements and analyses of the problem crab, an unusually large invertebrate that is highly mobile been attempted. The theory of strategies of adaptation de- both in developmental stages and as an adult, has an unusually veloped by Levins (18) in analyzing the effects of environ- low level of heterozygosity; and the very small fish (Astyanax) mental uncertainty provides a general explanation for the is more heterozygous than other, larger vertebrates. Appar- observed variation in genic heterozygosity levels
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