The Centrality of Natural Selection

The most important extrinsic property common to all extant organisms is that they and their ancestors have passed through the filter of natural selection. As survivors, all are ‘successful’ (see below) in contemporary terms, even if they are ultimately destined for extinction: the Darwinian truth is that all have been shaped by this process of differential survival. While the process of microbial evolution differs in dynamics and detail from that of macro organisms (►Chap. 2), all life forms share an evolutionary history extending over some 3 billion years.

It could be argued that the 8.7 million or so estimated species (Mora et al. 2011) represent 8.7 million responses to natural selection. But, more interestingly, what, if any, ecological commonalities are evident among the survivors? Here is where the words of Jacob (1982 pp. 14-15) are important: “Natural selection, however, does not act merely as a sieve eliminating detrimental mutations and favoring the reproduction of beneficial ones, as is often suggested. In the long run, it integrates mutations and orders them into adaptively coherent patterns... [and] gives direction to changes, [and] orients chance." The central question that sets the unifying theme for this book is thus the extent to which the ecology of microorganisms and macro organisms has been analogously molded by differential reproductive success operating among individuals.

Since the premise is that natural selection is a major organizing principle of biology, it is worthwhile to diverge briefly to consider some important aspects and implications of Darwin’s theory. This pertains especially to the terms ‘fitness’, ‘success’, ‘optimum’, and ‘maximize, which, as common jargon in the ecological literature, are used to some extent in this book. According to Darwin (1859, p. 81) natural selection was... “this preservation of favourable [sic] variations and rejection of injurious variations.” In contemporary terminology we could say that natural selection is evolutionary change in the heritable characteristics of a population from generation to generation resulting from the differential reproductive success of genotypes.

So the first point is that natural selection is thus only one of the means by which evolution can occur and it hinges critically on the proposition that different individuals leave different numbers of descendants (and descendants is the operative word, not progeny). That, in turn, is determined both by the characteristics of the individual and those of the environment with which it interacts. Other evolutionary forces or phenomena include, but are not limited to, founder (chance) effects; archetype effects (see phylogenetic constraints, below); drift; pleiotropism and epistasis—phenomena that result in the association of multiple and apparently independent alleles or traits carried through the evolutionary process together, though not the target of selection themselves (for discussion, see Harper 1982).

In passing it should be noted that many evolutionists have cautioned against the blithe application of ‘adaptation’ to explain any seemingly beneficial trait. Williams (1966) has stressed that adaptation “. should be used only where it is really necessary. When it must be recognized, it should be attributed to no higher a level than is demanded by the evidence (p. 4) and further ...it should not be invoked when less onerous principles, such as those of physics and chemistry or that of unspecified cause and effect, are sufficient for a complete explanation ’ (p. 11).

Second, the organisms we see about us today are the outcome of natural selection acting on past organisms in past environments. Thus it has been argued by Harper (1982), somewhat facetiously, that a better term than adaptation (which implies movement toward a desired state, i.e., a teleology) is ‘abaptation’ (implying movement away from a past state; how the past has influenced the present). Equivalently, the effects of current natural selection will become manifest in the nature of organisms in the future in future environments. In other words, in actuality natural selection acts to improve fitness of descendants for the environment of their parents, not for their own environment. (The inevitable parallel here is with generals preparing their troops to fight that last war rather than how to anticipate future conflicts.) Since the environment inevitably changes (7-Chap. 7), the truly optimum state can never be reached. In essence it is pursued through time by the organism, or as van Valen (1973), Lewontin (1978) have phrased it, environments are tracked by organisms.

Third, natural selection at best can only operate on the best of what can be produced by mutation and recombination of existing genotypes: the choice is restricted to what is available at a given time and place in the gene pool. Mayr (1982, p. 490) likens natural selection to a statistical concept: possessing a superior genotype does not ensure survival; it only offers a higher probability. For reproductive success it is merely sufficient to be better (or temporarily lucky!), not perfect or optimal. Every genotype is necessarily a compromise among opposing selection forces (Dobzhansky 1956; Mayr 1982). Thus, Darwin’s theory does not predict an optimum state or perfection (although such terms are often used loosely), merely that some individuals, namely those with particular features, will leave more descendants than others (e.g., Sober 1984; Begon et al. 1996, pp. 6-7). For these reasons it is technically incorrect to say that fitness is maximized. These points are elaborated below on constraints. Nevertheless, natural selection is a potent force because, unlike the largely random process of mutation that generates the original variation (see 7Chap. 2), or random genetic drift, natural selection is nonrandom—on balance, the organisms with certain features are the ones that survive and leave relatively more descendants.

Fourth, selection operates at the level of 'the individual' (not to mention other levels; see Preface and following discussion of what is an individual in various contexts). An important corollary is that the individual cannot be meaningfully 'atomized' into adaptive traits with a view of seeking optimization for each of the dissected parts. In a now classic paper, Dobzhansky (1956) argued eloquently that “traits have no adaptive significance in isolation from the whole developmental pattern of the organism which exhibits them at certain stages of its life cycle (p. 346)... a disadvantage in some respects may be compensated by advantages in other respects (p. 339). it is the trajectory of the whole which conveys upon the genotype or the individual its fitness to survive and to reproduce” (p. 346). While this principle has been echoed and embellished over the years (e.g., see Gould and Lewontin 1979), it bears periodic re-emphasis in an era of reductionist, genomics-oriented, molecular biology.

Finally, for the sake of brevity and simplicity, and in keeping with traditional ecological terminology, expressions such as ‘choosing, ‘strategy, ‘tactic’, and so forth are used throughout the text, albeit cautiously. They carry no teleological implications for the organisms concerned. For an excellent critique of loose thinking and loose terminology, see Harper (1982).