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Accelerated crossing of fitness valleys through division of labor and cheating in asexual populations.

ABSTRACT: Complex traits can require the accumulation of multiple mutations that are individually deleterious. Their evolution requires a fitness valley to be crossed, which can take relatively long time spans. A new evolutionary mechanism is described that accelerates the emergence of complex phenotypes, based on a "division of labor" game and the occurrence of cheaters. If each intermediate mutation leads to a product that can be shared with others, the complex type can arise relatively quickly as an emergent property among cooperating individuals, without any given individual having to accumulate all mutations. Moreover, the emergence of cheaters that destroy cooperative interactions can lead to the emergence of individuals that have accumulated all necessary mutations on a time scale that is significantly faster than observed in the absence of cooperation and cheating. Application of this mechanism to somatic and microbial evolution is discussed, including evolutionary processes in tumors, biofilms, and viral infections.

SUBMITTER: Komarova NL

PROVIDER: S-EPMC3512085 | biostudies-other | 2012

REPOSITORIES: biostudies-other

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Accelerated crossing of fitness valleys through division of labor and cheating in asexual populations.

Komarova Natalia L NL Urwin Erin E Wodarz Dominik D

Scientific reports 20121203

Complex traits can require the accumulation of multiple mutations that are individually deleterious. Their evolution requires a fitness valley to be crossed, which can take relatively long time spans. A new evolutionary mechanism is described that accelerates the emergence of complex phenotypes, based on a "division of labor" game and the occurrence of cheaters. If each intermediate mutation leads to a product that can be shared with others, the complex type can arise relatively quickly as an em ...[more]

PMID: 23209877

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Project description:BackgroundSingle nucleotide substitutions in protein-coding genes can be divided into synonymous (S), with little fitness effect, and non-synonymous (N) ones that alter amino acids and thus generally have a greater effect. Most of the N substitutions are affected by purifying selection that eliminates them from evolving populations. However, additional mutations of nearby bases potentially could alleviate the deleterious effect of single substitutions, making them subject to positive selection. To elucidate the effects of selection on double substitutions in all codons, it is critical to differentiate selection from mutational biases.ResultsWe addressed the evolutionary regimes of within-codon double substitutions in 37 groups of closely related prokaryotic genomes from diverse phyla by comparing the fractions of double substitutions within codons to those of the equivalent double S substitutions in adjacent codons. Under the assumption that substitutions occur one at a time, all within-codon double substitutions can be represented as "ancestral-intermediate-final" sequences (where "intermediate" refers to the first single substitution and "final" refers to the second substitution) and can be partitioned into four classes: (1) SS, S intermediate-S final; (2) SN, S intermediate-N final; (3) NS, N intermediate-S final; and (4) NN, N intermediate-N final. We found that the selective pressure on the second substitution markedly differs among these classes of double substitutions. Analogous to single S (synonymous) substitutions, SS double substitutions evolve neutrally, whereas analogous to single N (non-synonymous) substitutions, SN double substitutions are subject to purifying selection. In contrast, NS show positive selection on the second step because the original amino acid is recovered. The NN double substitutions are heterogeneous and can be subject to either purifying or positive selection, or evolve neutrally, depending on the amino acid similarity between the final or intermediate and the ancestral states.ConclusionsThe results of the present, comprehensive analysis of the evolutionary landscape of within-codon double substitutions reaffirm the largely conservative regime of protein evolution. However, the second step of a double substitution can be subject to positive selection when the first step is deleterious. Such positive selection can result in frequent crossing of valleys on the fitness landscape.

Dataset Information

Accelerated crossing of fitness valleys through division of labor and cheating in asexual populations.

Publications

Accelerated crossing of fitness valleys through division of labor and cheating in asexual populations.

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