Natural Selection as the Common Denominator

As noted in Chap. 1, a general property uniting organisms is that all are shaped by evolutionary pressures. The major evolutionary process underpinning comparisons in this book has been natural selection. This is as opposed to other forces or phenomena such as founder effects, archetype (phylogenetic) effects, genetic drift, or pleiotropic effects (for insightful discussion of these and others, see Harper 1982). Many genes or gene families (e.g., histone, cytochrome, etc.) have been conserved in widely divergent organisms through a vast evolutionary history.

Thus, it should not surprise us that analogous responses or ‘strategies’ to similar fundamental challenges or ‘problems’ also have emerged in the ecology of organisms, regardless of their size (Table 8.1). By virtue of sharing fundamental biological attributes and being extant, all have passed thus far the endless sifting and winnowing of natural selection. It is therefore an unfortunate mistake that demarcation based on size, implicitly or explicitly, has acted to compartmentalize so much of the thinking in ecology (and biology in general).

The Principle of Trade-Offs as a Universal Currency.The general model presented at the outset (Fig. 1.2 and Chap. 1) as a common basis for ecological comparisons is the organism as an input/output system. The organism is viewed as a black box with an input and an output: it acquires various resources and produces progeny. The challenge for all organisms is, and always has been, the same: Each life history is of necessity a compromise to multiple demands on limited time, resources, and options. Stearns (1992, his Chap. 4) identifies “at least 45 trade-offs” (p. 72), particularly those between current reproduction and survival, current reproduction and future reproduction, reproduction and growth, number and quality of offspring, among others. In a world where no compromises were necessary, under natural selection every organism would operate at its optimum phylogenetic limits—an observation obviously inconsistent with a wealth of evidence from both microbial ecology and plant and animal ecology (see especially Chaps. 1, 3, 5, and 7; also Stearns 1989, 1992). This, arguably the most fundamental ecological tenet at the organism level, might be called the Principle of Trade-Offs.

Natural selection should favor organisms that are cost-efficient overall in resource acquisition, allocation, and expenditure. As such, they should be competitively superior and leave more descendants. (Note that while the principle of allocation is intuitively acceptable, it is usually not clear to what extent any particular allocation pattern translates ultimately into numbers of descendants; Chap. 3.) The activities of an organism on which selection acts can be subdivided for convenience into five arbitrary categories (Southwood 1988): (i) tolerance of the physical environment; (ii) defense; (iii) foraging; (iv) reproduction; (v) escape in time or space. Although the input/output scheme, as a simplistic model, does not explicitly recognize the functional categories (i), (ii) and (v), they are implicitly a part of it. Costs assignable to these categories will have a negative impact on foraging and a positive or negative effect on reproduction. For instance, with respect to defense, time spent by a bird avoiding predators or, with respect to escape, time spent by a fungus ensconced as a resistant, quiescent sclerotium, in both instances is time lost, for example, to feeding. Modifications in these diversions may or may not prove to increase the number of descendants (Chaps. 3, 7, and Andrews 1992). Natural selection is the ultimate arbiter.

Various levels of ecological generality and comparability can be recognized for each of the above categories in comparisons among taxa. Take, for example, adjustment to the physical environment. The most general comparison entails only a slight restatement of the principle of trade-offs, viz., microorganisms as well as macroorganisms must compromise allocations to physiological adjustment with other demands on their time and resources. This is a valid generality, but being a universal statement conveys nothing of specific value in any particular context. A second, more specific level of comparison could be that, in the short term, bacteria respond rapidly to a rapidly changing environment by altering metabolic pathways, whereas plants respond primarily by a system of cues and hormonal controls triggered by environmental change. The two organisms do so in part by analogous mechanisms of phenotypic plasticity (Chap. 7).

In fact, as we saw, at least some bacteria even exhibit circadian rhythm. For both creatures this implies costs as well as benefits. Being a more specific statement than the first, it carries useful predictions, though these predictions may mostly pertain to bacteria and plants. Finally, at the third and most specific level, one could postulate that bacterium species A copes with stochastic adversity by segregating a tolerant subpopulation (for example, of ‘persisters’; Chap. 7) prepositioned on ‘standby’ as it were, while plant species B responds to seasonal adversity by shedding its leaves. At this level a given response does not necessarily apply even to fairly closely related taxa, much less from microorganism to macroorganism.

A different genus of bacterium may form spores; a different plant species might cope with the environmental change by employing apical dormancy. In our context and across this spectrum from very general to quite specific, a very interesting and productive analogy is at the level of evolution of phenotypic plasticity: what forms does it take in microorganisms versus macroorganisms; to what extent does plasticity shape the respective life cycles; what is the genetic/epigenetic basis; and do some of the genes involved even have a common evolutionary origin? Parenthetically, it is noteworthy that such plasticity is among the most ancient of organism traits, having evolved in primitive bacteria, and in some form being phylogeneti- cally universal. Clearly it appears to have been a seminal evolutionary event.