Adaptive inertia caused by hidden pleiotropic effects (Q1369201)

The focus of this study is a simple model for the evolution of complex organisms. It is based on three assumptions which capture some of the features characteristic of organismic evolution: (1) The first assumption is that pleiotropic effects are extensive and universal. It is thus based on Wright's universal pleiotropy hypothesis. (2) Only one character (or a linear combination of characters) is under directional selection at any time. This assumption is in line with the pattern of mosaic evolution, which means that complex organisms do not change all their characteristics at the same time. (3) While some of the characters are under directional selection, most of the others are either neutral or under stabilizing selection. This is a corollary of the mosaic evolution assumption. Hence it is expected that a combination of directional and stabilizing selection is a common pattern. Explicit genetic models are considered for the evolution of a quantitative polygenic character under directional selection. It is assumed that the character is coupled to an uncorrelated quantitative character via ''hidden'' pleiotropic effects. The term ''hidden pleiotropic effects'' means that the pleiotropic effects do not contribute to genetic correlations between the characters. It is shown that the evolution of the mean value is influenced by selection on a pleiotropically coupled character even in the absence of genetic correlations. This effect is due to apparent stabilizing selection caused by deleterious pleiotropic effects. Dynamically, the effect is mediated through an association between the mean value of one character and the genetic variance of the pleiotropically linked character. The main results have been shown analytically for two as well as for more loci. In the case of more than two genes, additional terms than the ones discussed above appear in the equation for the evolution of the first character which slightly mitigate the Pooh effect. Selection creates a linkage disequilibrium in favor of gametes hiding some of the pleiotropic effects (the so-called Bulmer effect). But this effect is small in the range investigated so far \((n\leq 8)\). The main difference in this model is that deleterious effects are not unconditionally deleterious. Deleterious pleiotropic effects are modeled as additive effects on a character which is under stabilizing selection. Additive effects of one gene can be compensated by additive effects of the opposite sign at another locus. This is to say that the pleiotropic effects are epistatic with respect to fitness. Whether a pleiotropic effect increases or decreases fitness depends on the current breeding value for the second character of the genotype. If the breeding value of the second character is at the optimum for this character, every pleiotropic effect is deleterious. However, if the breeding value of the second character does not coincide with its optimum, the fitness effect might be positive or negative. If the pleiotropic effect brings the breeding value closer to the optimum of the second character, fitness increases; if it leads away from the optimum, the fitness decreases. The effect on asymptotic rates of evolution in finite populations of hidden pleiotropic effects was investigated by stochastic simulations. It was found that the asymptotic rate of evolution is reduced by stabilizing selection on hidden pleiotropic effects. The magnitude of the reduction depends on the strength of the directional selection as compared to the stabilizing selection. If this ratio is below the limit for the Pooh effect, predicted by the deterministic theory, then the rate of evolution is more than 50 \% of the rate predicted by the standard one-character theory. Under these conditions the influence on the rate of evolution is moderate. Considerable influence is found once the apparent stabilizing selection dominates over directional selection and can then be as low as 5 \% of the value predicted by one character theory. The biological implications of these results can be divided into two main topics: the potential of the Pooh effect to happen in real populations, and the implications for long-term selection response. Without pleiotropic effects the asymptotic rate of evolution under sustained directional selection has been shown to be proportional to the effective population size, the mutational variance, and the selection intensity \(2\sigma N_e V_m\). The results in this paper show that this prediction is a good upper limit to the rate of evolution under most circumstances. The analysis suggests that apparent stabilizing selection induced by hidden pleiotropic effects is also causing adaptive inertia to weak directional selection. If the basic assumptions of the presented model are true (i.e., extensive pleiotropy and mosaic evolution) one can expect adaptive inertia to be a common phenomenon of phenotypic evolution.