The Ascent of the Abundant: How Mutational Networks Constrain Evolution

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Abstract
Evolution by natural selection is fundamentally shaped by the fitness landscapes in which it occurs. Yet fitness landscapes are vast and complex, and thus we know relatively little about the long-range constraints they impose on evolutionary dynamics. Here, we exhaustively survey the structural landscapes of RNA molecules of lengths 12 to 18 nucleotides, and develop a network model to describe the relationship between sequence and structure. We find that phenotype abundance—the number of genotypes producing a particular phenotype—varies in a predictable manner and critically influences evolutionary dynamics. A study of naturally occurring functional RNA molecules using a new structural statistic suggests that these molecules are biased toward abundant phenotypes. This supports an “ascent of the abundant” hypothesis, in which evolution yields abundant phenotypes even when they are not the most fit. Evolutionary biology tells us much about the immediate fate of a mutation once it appears, but relatively little about its long-term evolutionary implications. Major evolutionary transitions from one trait to another may depend on a long sequence of interacting mutations, each arising by chance and surviving natural selection. In this study, we characterize the network of mutations that connect diverse molecular structures, and find that this network biases evolution toward traits that are readily produced by one or a short sequence of mutations. This bias may prevent the evolution of optimal traits, a phenomenon they call the “ascent of the abundant.”

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