First, evolution is a population-level feature. Thus, if an organismal feature that modifies the ability to evolve is to be advanced directly by adaptive mechanisms, selection must operate efficiently at a higher level of organization than the individual. This requires a significantly subdivided population structure, with levels of evolvability being positively correlated with population longevity and/or productivity. Because populations survive longer than individuals, such group selection is expected to be a much weaker force than individual selection, and necessarily operates on much longer time scales. If evolvability is to be subject to selective advancement, at least three stringent conditions must be met: (i) the group advantages of the genomic attribute that enhances evolvability must exceed any conflicting pressures operating at the individual level; (ii) the enhanced capacity for rapid evolutionary change must persist over the time scale of group selection; and (iii) while en route to fixation at the population level, the alleles that promote evolvability must remain tightly linked to the loci whose evolution is advantageous. Do such conditions ever exist in nature? The evidence for individual-level selection is overwhelming (Endler, 1986; Kingsolver et al., 2001), but aside from the matter of kin selection in behavioral evolution (Hamilton, 1964a,b; Wilson, 1975), the evidence for the operation of group selection is weak, although some investigators remain more optimistic than others (Coyne et al., 2000; Goodnight and Wade, 2000).
Second, it is by no means clear that an enhanced ability to evolve is generally advantageous. The dynamics of genetic variance for quantitative traits is complex, with selection modifying allele frequencies at epistatically interacting loci in ways that can either increase or decrease heritabilities, regardless of the advantage of the traits under selection (Carter et al., 2005). In addition, one can just as easily point to a long list of pathologies that can arise from an overly rapid proliferation of a new phenotype, and such scenarios have motivated a completely alternative, and equally speculative, view, that selection can favor mechanisms that suppress evolvability (Altenberg, 2005). Furthermore, theoretical studies have shown that the kinds of complexities that are often focused on by those enamored with evolvability (e.g., increased dimensionality and modularity) can actually inhibit the rate of adaptive evolution (Orr, 2000; Welch and Waxman, 2003; Haygood, 2006). Although the arguments are technical, they are no more abstract than the verbal reasoning of the evolvability school.
Third, there is no evidence that phylogenetic variation in evolutionary features reflects anything more than diversity in variation-generating factors that exist for purely physical reasons. For example, the biological features most likely to influence the ability to evolve, recombination and mutation rates, vary by orders of magnitude among species, with no