Multidimensional Epistasis and the Transitory Advantage of Sex

Identifying and quantifying the benefits of sex and recombination is a long-standing problem in evolutionary theory. In particular, contradictory claims have been made about the existence of a benefit of recombination on high dimensional fitness landscapes in the presence of sign epistasis. Here we present a comparative numerical study of sexual and asexual evolutionary dynamics of haploids on tunably rugged model landscapes under strong selection, paying special attention to the temporal development of the evolutionary advantage of recombination and the link between population diversity and the rate of adaptation. We show that the adaptive advantage of recombination on static rugged landscapes is strictly transitory. At early times, an advantage of recombination arises through the possibility to combine individually occurring beneficial mutations, but this effect is reversed at longer times by the much more efficient trapping of recombining populations at local fitness peaks. These findings are explained by means of well-established results for a setup with only two loci. In accordance with the Red Queen hypothesis the transitory advantage can be prolonged indefinitely in fluctuating environments, and it is maximal when the environment fluctuates on the same time scale on which trapping at local optima typically occurs.

甄别与量化有性生殖及重组的演化优势，是演化理论领域长期存在的经典难题。具体而言，针对存在符号上位性（sign epistasis）的高维适应度景观（fitness landscape）上，重组是否具备演化优势这一问题，学界一直存在相互矛盾的论断。本研究针对强选择条件下、可调控崎岖度的模型景观中的单倍体有性与无性演化动力学开展对比数值分析，重点关注重组演化优势的时间演化特征，以及种群多样性与适应速率之间的内在关联。研究表明，静态崎岖景观上重组的适应性优势仅具有暂时性。演化初期，重组可通过整合独立产生的有益突变形成优势；但随着时间推移，重组种群更易陷入局部适应峰，这一效应会发生反转。上述结论可通过仅含两个基因座（locus）的经典模型的已有成熟研究结论得到合理解释。根据红皇后假说（Red Queen hypothesis），在波动环境中，重组带来的暂时性优势可被无限延长；且当环境波动的时间尺度与种群陷入局部最优的典型时间尺度相匹配时，该优势将达到峰值。