From adaptation to molecular evolution

Abstract

There have been an increasing number of calls in recent years for a ‘post-modern' synthesis of evolutionary biology, extending the modern synthesis of the 40–50's by including molecular aspects of development (evo–devo), phenotypic plasticity driving genetic evolution, or epigenetic inheritance (for example, Pigliucci, 2007). This illustrates an infusion of evolutionary thinking into all aspects of modern biology, creating a need for integrative approaches and increased exchange between complementary fields. These calls often go along with a healthy questioning of orthodoxy in the light of current empirical evidence. However, alternatives should be scrutinized with as much skepticism as the mainstream theory they aim to replace or improve. We need to ask whether each theory—Neo-Darwinism or the proposed alternative—is sufficient to explain observed patterns, not whether it is necessary. That some observed patterns could be due to another process does not argue against Neo-Darwinism, if this other process is not a sufficient explanation in other situations. As an analogy, relativity theory is not always necessary to explain the motion of particles, but it is sufficient to account for all known mechanics, whereas Newton's theory is not. Interpreting the enormous amount of emerging molecular data requires such an integrative approach. To use these data to infer population processes behind patterns of adaptation, we need models that describe how natural selection operates on traits, how this translates into changes in nucleotide sequences, and whether unique molecular signatures can be detected under alternative, plausible scenarios. In a recent paper in this journal, Hughes (2011) argues that, because current statistical approaches fail to reliably detect strong evidence of positive selection at the molecular level (while they reveal substantial evidence of purifying selection), we need to explain the origin of adaptation at the phenotypic level by a process other than the Neo-Darwinian one, that is, cumulative substitutions of beneficial mutations. Specifically, he proposes that adaptation may arise when ancestral phenotypic plasticity in a variable environment is lost in a more homogeneous environment by the accumulation of deleterious mutations under relaxed selection (the plasticity–relaxation–mutation hypothesis, or PRM). He suggests that most evolutionists have overlooked this alternative explanation, because it does not fit their Neo-Darwinian understanding of adaptation. We hold that the PRM hypothesis is neither a more parsimonious hypothesis, nor one more consistent with data, than the Neo-Darwinian mode of adaptation. Patterns of molecular evolution can agree well with predictions from the Neo-Darwinian view of adaptation, provided we use more explicit models for phenotypic selection in a new environment and for the genetic architecture of adaptive traits.