The frailty of adaptive hypotheses for the origins of organismal complexity

Abstract

The vast majority of biologists engaged in evolutionary studies interpret virtually every aspect of biodiversity in adaptive terms. This narrow view of evolution has become untenable in light of recent observations from genomic sequencing and population-genetic theory. Numerous aspects of genomic architecture, gene structure, and developmental pathways are difficult to explain without invoking the nonadaptive forces of genetic drift and mutation. In addition, emergent biological features such as complexity, modularity, and evolvability, all of which are current targets of considerable speculation, may be nothing more than indirect by-products of processes operating at lower levels of organization. These issues are examined in the context of the view that the origins of many aspects of biological diversity, from gene-structural embellishments to novelties at the phenotypic level, have roots in nonadaptive processes, with the population-genetic environment imposing strong directionality on the paths that are open to evolutionary exploitation.

Fig. 1.

The long-term probability that an allele residing at a biallelic locus will be of the selectively advantageous type, given a selective advantage s, an effective population number of gene copies of N_g, and a mutation rate to the beneficial allele m times that in the reverse direction. The red line (2N_gs = 0.0) denotes neutrality, whereas the green line (2N_gs = ∞) denotes an effectively infinite population, such that genetic drift is a negligible force.

Fig. 2.

The passive emergence of specialized gene functions via nonadaptive processes of duplication, degenerative mutation, and random genetic drift. (Left) Regulatory elements (transcription-factor binding sites) are depicted, with each regulatory element color-coded according to the transcription factor that binds to it. (Right) Allele-specific utilizations of transcription factors are depicted. Transcription factors denoted by black and white are ubiquitously expressed, whereas those denoted by green and red are each expressed in single, nonoverlapping tissues. For this particular gene, within their respective tissues, the green and red transcription factors are redundant with respect to the white factor, but the additional black factors are essential for complete expression. Three hypothetical phases of gene architectural modification are shown. (Top) Accretion and degeneration of transcription-factor binding sites. The initial allele (a) is expressed in an identical manner in both tissues, but the regulatory region sequentially acquires the green and red elements. The redundant white element is then vulnerable to loss by degenerative mutation, yielding a descendant allele with a semiindependent mode of expression, as the black element is still essential to expression in both tissues. At this stage all four alleles (a–d) are interchangeable, as each of them achieves the same pattern of phenotypic expression. (Middle) Regulatory-region duplication, degeneration, and complementation. The entire enhancer region is tandemly duplicated, with each component then losing a complementary (red/green) element. The resultant allele has become modularized in the sense that it harbors two independently mutable subfunctions denoted by the green and red open boxes; a mutation in either region has effects confined to a single tissue. (Bottom) Gene duplication and subfunctionalization by degenerative mutation. The entire gene is duplicated, with each copy becoming silenced by degenerative mutation for a complementary subfunction. The expression of each copy is now confined to a single tissue.

Fig. 3.

A series of allelic states for locus A, defined by the ability to self-express and/or be activated by an upstream transcription factor B. Mutational rates of gain and loss of regulatory abilities are denoted by u_g and u_l, here for simplicity assumed to be the same for both self-activation and upstream activation. The redundantly regulated allele is invulnerable to single-loss mutations.