The cost of evolution and the imprecision of adaptation.

Abstract

Comparisons of six hypothetical cases suggest that Haldane overestimated the cost of natural selection by allele substitution. The cost is reduced if recessive alleles are advantageous, if substitutions are large and few, if selection is strong and substitutions are rapid, if substitutions are serial, and if substitutions in small demes are followed by deme-group substitutions. But costs are still so heavy that the adaptations of complex organisms in complex and changing environments are never completed. The rule probably is that most species most of the time are not fully adapted to their environments, but are just a little better than their competitors for the time being. During the "evolution" of a man-made machine, the maker of it can take it apart and eliminate inferior and substitute improved parts without throwing away whole machines. But in organic evolution, each slightest separate improvement made by natural selection in the great number of parts, processes, and behaviors in an evolving organism is made at the cost of eliminating-throwing away-all the whole individuals that lack the improvement. This is "the cost of natural selection," or of adaptive evolution. Calculation of this cost and of its consequences is one of the most important pieces of unfinished business in modern evolution theory.THEORY: THE COST OF SELECTION Haldane (1), in 1957, calculated that gene (allele) substitutions by selection cost so much that populations must (in effect) choose between evolving at low cost per generation but unadaptively slowly, or more rapidly but at a cost so high as to risk extinction. These alternatives constitute what is sometimes called "Haldane's dilemma." His conclusions have been much criticized, especially by means of complex mathematics; for partial reviews of the criticisms, see ref. 2, I shall re-examine the cost of selection in another way, by means of six hypothetical cases and simple arithmetic; the cases cannot prove generalizations but can suggest them or (sometimes) falsify them. And I shall then consider how costs limit actual, complex evolutionary processes and the precision of adaptations, including our own. Two-class, 1-episode cases Case A. Suppose that, in a population of four billion individuals, only one male and one female are homozygous for a recessive allele which allows them alone to survive an atomic holocaust which eliminates all the other individuals. (If all individuals survive, but only the two can reproduce, the others being sterilized by radiation, the effect is the same.) Then one complete allele substitution will have been made by selection (selective elimination) in one generation, at a cost of No(4 billion) -N1(2) = 3,999,999,998 individuals, and no additional selective substitutions can be made and paid for at the same time, although other, nonselective, random changes comparable to those expected of the "founder effect" may occur in the population's gene pool. 1647Case B. Now suppose that the two survivors escape other hazards and produce ten offspring of w...

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