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Repeatability of evolution on epistatic landscapes.

ABSTRACT: Evolution is a dynamic process. The two classical forces of evolution are mutation and selection. Assuming small mutation rates, evolution can be predicted based solely on the fitness differences between phenotypes. Predicting an evolutionary process under varying mutation rates as well as varying fitness is still an open question. Experimental procedures, however, do include these complexities along with fluctuating population sizes and stochastic events such as extinctions. We investigate the mutational path probabilities of systems having epistatic effects on both fitness and mutation rates using a theoretical and computational framework. In contrast to previous models, we do not limit ourselves to the typical strong selection, weak mutation (SSWM)-regime or to fixed population sizes. Rather we allow epistatic interactions to also affect mutation rates. This can lead to qualitatively non-trivial dynamics. Pathways, that are negligible in the SSWM-regime, can overcome fitness valleys and become accessible. This finding has the potential to extend the traditional predictions based on the SSWM foundation and bring us closer to what is observed in experimental systems.

SUBMITTER: Bauer B

PROVIDER: S-EPMC5386189 | biostudies-literature | 2015 May

REPOSITORIES: biostudies-literature

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Repeatability of evolution on epistatic landscapes.

Bauer Benedikt B Gokhale Chaitanya S CS

Scientific reports 20150505

Evolution is a dynamic process. The two classical forces of evolution are mutation and selection. Assuming small mutation rates, evolution can be predicted based solely on the fitness differences between phenotypes. Predicting an evolutionary process under varying mutation rates as well as varying fitness is still an open question. Experimental procedures, however, do include these complexities along with fluctuating population sizes and stochastic events such as extinctions. We investigate the ...[more]

PMID: 25939695

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Project description:BackgroundUnderstanding interactions between mutations and how they affect fitness is a central problem in evolutionary biology that bears on such fundamental issues as the structure of fitness landscapes and the evolution of sex. To date, analyses of fitness landscapes have focused either on the overall directional curvature of the fitness landscape or on the distribution of pairwise interactions. In this paper, we propose and employ a new mathematical approach that allows a more complete description of multi-way interactions and provides new insights into the structure of fitness landscapes.ResultsWe apply the mathematical theory of gene interactions developed by Beerenwinkel et al. to a fitness landscape for Escherichia coli obtained by Elena and Lenski. The genotypes were constructed by introducing nine mutations into a wild-type strain and constructing a restricted set of 27 double mutants. Despite the absence of mutants higher than second order, our analysis of this genotypic space points to previously unappreciated gene interactions, in addition to the standard pairwise epistasis. Our analysis confirms Elena and Lenski's inference that the fitness landscape is complex, so that an overall measure of curvature obscures a diversity of interaction types. We also demonstrate that some mutations contribute disproportionately to this complexity. In particular, some mutations are systematically better than others at mixing with other mutations. We also find a strong correlation between epistasis and the average fitness loss caused by deleterious mutations. In particular, the epistatic deviations from multiplicative expectations tend toward more positive values in the context of more deleterious mutations, emphasizing that pairwise epistasis is a local property of the fitness landscape. Finally, we determine the geometry of the fitness landscape, which reflects many of these biologically interesting features.ConclusionA full description of complex fitness landscapes requires more information than the average curvature or the distribution of independent pairwise interactions. We have proposed a mathematical approach that, in principle, allows a complete description and, in practice, can suggest new insights into the structure of real fitness landscapes. Our analysis emphasizes the value of non-independent genotypes for these inferences.

Project description:BackgroundGenes that encode proteins associated with sperm competition, fertilization, and sexual conflicts of interest are often among the most rapidly evolving parts of animal genomes. One family of sperm-expressed genes (Zp3r, C4bpa) in the mammalian gene cluster called the regulator of complement activation (RCA) encodes proteins that bind eggs and mediate reproductive success, and are therefore expected to show high relative rates of nonsynonymous nucleotide substitution in response to sexual selection in comparison to other genes not involved in gamete binding at fertilization. We tested that working hypothesis by using phylogenetic models of codon evolution to identify episodes of diversifying positive selection. We used a comparative approach to quantify the evidence for episodic diversifying selection acting on RCA genes with known functions in fertilization (and sensitivity to sexual selection), and contrast them with other RCA genes in the same gene family that function in innate immunity (and are not sensitive to sexual selection).ResultsWe expected but did not find evidence for more episodes of positive selection on Zp3r in Glires (the rodents and lagomorphs) or on C4BPA in Primates, in comparison to other paralogous RCA genes in the same taxon, or in comparison to the same orthologous RCA gene in the other taxon. That result was not unique to RCA genes: we also found little evidence for more episodes of diversifying selection on genes that encode selective sperm-binding molecules in the egg coat or zona pellucida (Zp2, Zp3) in comparison to members of the same gene family that encode structural elements of the egg coat (Zp1, Zp4). Similarly, we found little evidence for episodic diversifying selection acting on two other recently discovered genes (Juno, Izumo1) that encode essential molecules for sperm-egg fusion.ConclusionsThese negative results help to illustrate the importance of a comparative context for this type of codon model analysis. The results may also point to other phylogenetic contexts in which the effects of selection acting on these fertilization proteins might be more readily discovered and documented in mammals and other taxa.

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Repeatability of evolution on epistatic landscapes.

Publications

Repeatability of evolution on epistatic landscapes.

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