Constraints on Natural Selection: Phylogenetic, Ontogenetic, and Allometric

Natural selection does not operate on a uniform or blank slate but within the context of many interacting factors and processes such as chance, historical precedent, habitat complexity, and inherent biological constraint. In general, three major, interrelated constraints have been recognized: phylogenetic (taxa-related), ontogenetic (development-related), and allometric (size-related). Unlike the trade-off concept, which underlies most of the examples in this book and is discussed later, evolutionary constraints are absolute and cannot be moved to-and-fro by changing an opposing selection force (Stearns 1977, 1982, 1992).

Thus, one way to look at any organism is “as a mosaic of relatively new adaptations embedded in a framework of relatively old constraints” (Stearns 1982, p. 249). Stearns (1992) has further noted that not only are certain traits fixed within lineages but they constrain within limits those that do vary (only those varying are involved in trade-offs). Moreover, since each lineage is constrained uniquely, each has its own trade-off structure, e.g., for plants, see Niklas (2000). For these reasons, organisms cannot technically be ‘optimal’ entities (whatever an author may mean by that expression) and optimality models in ecology have to operate within the boundaries discussed below (see discussion and caveats in Stearns 1992).

The constraints placed on a species by its evolutionary pedigree are phylogenetic, also termed historical. Organisms evolve in lineages of ancestral and descendant populations. No lineage begins with a blank slate; each is constrained by its legacy. A specific pattern of development for each species is both characteristic of and similar to the ancestral form. McKitrick (1993) has likened this to a game of scrabble where players are limited in spelling words by the letters they receive at the outset. There are many excellent examples in biology: Humans, unlike millipedes, have only two legs and lack the power of regenerating amputated appendages. Starfish and their relatives all show five-point symmetry.

All plants are modular in growth form; all higher animals are unitary. In every instance, limitations as well as opportunities are bestowed on the organism by its birthright. So, given a particular design, certain things are impossible or, though possible are strongly selected against, or both (Stearns 1983). Buss (1987) has discussed the different evolutionary directions of the plant, animal, and fungal kingdoms preordained by the different ancestral features of the three clades. These are described later (7-Chaps. 4 and 5) and in Andrews (1995).

Second, selection also can be limited in what it can do at any point in the life cycle by what has gone before in the developmental program (Bonner 1982b; see especially pp. 1-16). Such limitations are termed ontogenetic or developmental. One would expect that more complex organisms and more complex life cycles would be particularly vulnerable to this constraint (7 Chaps. 4 and 6). It is considerably more complicated to build the Space Shuttle than a Volkswagen Beetle. In biological terms, the complicated ontogeny of a mammal tends to preclude radical changes because early occurring mutations would likely be lethal, whereas microorganisms are relatively free from these constraints (Bonner 1982a, b).

Changes in the timing of events in the life cycle (heterochrony) may occur (events speeded up, as in larvae that are sexually mature; slowed down, as in development of the large brain in humans), but critical phases or structures cannot be eliminated. This is true even when functionally useless vestigial structures (gill arches in vertebrates; appendices in humans; tails in birds and mammals) appear in the fetus or adult. Such structures persist as a consequence of engineering size-increase by the building block method (Dobzhansky 1956; Chap. 4 in Bonner 1988). What is important is not the particular item so much as the overall process and the end product. A cautionary note in interpreting such constraints in some contexts, however, is that simply because one character state precedes another (ancestral condition) in a phylogeny, it is unwarranted to conclude that the presence of the second state necessarily depends on the occurrence of the first (Herron and Michod 2008).

Third, allometric limitations relating to size include associated changes in chemistry, physiology, and morphology. Evolution is limited by physical and chemical laws, a key example of which is surface-to-volume relationships that affect all sorts of fundamental processes such as biomechanics and diffusion. Carroll (2001) has asked the provocative question ... “are there universal rules to the shapes of life?” This and related issues are explored in 7Chap. 4.

One example is that a geometrical consequence of increasing size (volume) is decreasing surface area (S), dictated by the relationship S a V^2/3 (the “surface area law” or the “2/3-power law”). Metabolically important surfaces, however, scale not by the two-thirds power but directly in proportion to volume—we see this rule manifested as convolutions or sheets in the living world in the form of structural accommodations like villi, alveoli, capillaries, leaves, roots, and root hairs (7-Chap. 4). Metabolic and energetic ground rules set another form of constraint at the level of cell physiology (Lehninger 1970; Feldgarden et al. 2003). Size differences and the attendant allometric relationships can be examined during the course of development of an organism (ontogenetic comparisons) or across taxa at arbitrarily selected stages (phylogenetic comparisons) in an historical or contemporary context.

We are considering here and later in detail (7Chap. 4) the extent to which microorganisms and macroorganisms see the world differently and the ecological implications of this size differential. Such considerations must allow for not only differences of the conventional allometric sort applicable to organisms of similar geometry, but acknowledge also the pronounced differences in shape as well as size of the microorganisms versus macroorganisms. There are no spherical cows to compare with coccoid bacteria! Even if there were, the types of environments and the scale on which the organisms would interact with these environments would be entirely different.