Interaction-based evolution: how natural selection and nonrandom mutation work together
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Abstract Background The modern evolutionary synthesis leaves unresolved some of the mostfundamental, long-standing questions in evolutionary biology: What is therole of sex in evolution? How does complex adaptation evolve? How canselection operate effectively on genetic interactions? More recently, themolecular biology and genomics revolutions have raised a host of criticalnew questions, through empirical findings that the modern synthesis fails toexplain: for example, the discovery of de novo genes; the immenseconstructive role of transposable elements in evolution; genetic varianceand biochemical activity that go far beyond what traditional naturalselection can maintain; perplexing cases of molecular parallelism; andmore. Presentation of the hypothesis Here I address these questions from a unified perspective, by means of a newmechanistic view of evolution that offers a novel connection betweenselection on the phenotype and genetic evolutionary change (while relying,like the traditional theory, on natural selection as the only source offeedback on the fit between an organism and its environment). I hypothesizethat the mutation that is of relevance for the evolution of complexadaptation—while not Lamarckian, or “directed” to increasefitness—is not random, but is instead the outcome of a complex andcontinually evolving biological process that combines information frommultiple loci into one. This allows selection on a fleeting combination ofinteracting alleles at different loci to have a hereditary effect accordingto the combination’s fitness. Testing and implications of the hypothesis This proposed mechanism addresses the problem of how beneficial geneticinteractions can evolve under selection, and also offers an intuitiveexplanation for the role of sex in evolution, which focuses on sex as thegenerator of genetic combinations. Importantly, it also implies that geneticvariation that has appeared neutral through the lens of traditional theorycan actually experience selection on interactions and thus has a muchgreater adaptive potential than previously considered. Empirical evidencefor the proposed mechanism from both molecular evolution and evolution atthe organismal level is discussed, and multiple predictions are offered bywhich it may be tested. Reviewers This article was reviewed by Nigel Goldenfeld (nominated by Eugene V.Koonin), Jürgen Brosius and W. Ford Doolittle.
- BioMed Central