期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：36
DOI：10.1073/pnas.2123152119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
Through variation in fitness, selection accumulates and maintains information in the genomes of organisms. This process takes place over many generations, in populations that evolve stochastically due to finite size and random mutation. The information, which we quantify in bits, corresponds to the degree to which selection shapes the population composition, the DNA sequence, and the phenotype. We prove a general bound on the rate at which information can accumulate per generation. We find that both accumulation and maintenance of information are most efficient (require the least fitness variation per bit) when individual loci experience weak selection. This is relevant for selection on traits influenced by many small-effect loci—a common genetic architecture according to genome-wide association studies.
Selection accumulates information in the genome—it guides stochastically evolving populations toward states (genotype frequencies) that would be unlikely under neutrality. This can be quantified as the Kullback–Leibler (KL) divergence between the actual distribution of genotype frequencies and the corresponding neutral distribution. First, we show that this population-level information sets an upper bound on the information at the level of genotype and phenotype, limiting how precisely they can be specified by selection. Next, we study how the accumulation and maintenance of information is limited by the cost of selection, measured as the genetic load or the relative fitness variance, both of which we connect to the control-theoretic KL cost of control. The information accumulation rate is upper bounded by the population size times the cost of selection. This bound is very general, and applies across models (Wright–Fisher, Moran, diffusion) and to arbitrary forms of selection, mutation, and recombination. Finally, the cost of maintaining information depends on how it is encoded: Specifying a single allele out of two is expensive, but one bit encoded among many weakly specified loci (as in a polygenic trait) is cheap.
