Biology Department, Queens College of The City University of New York, New York City, New York, USA.
Department of Electrical and Computer Engineering, University of Delaware, Newark, Delaware, USA.
mBio. 2022 Jun 28;13(3):e0359321. doi: 10.1128/mbio.03593-21. Epub 2022 Apr 25.
Optimality models have a checkered history in evolutionary biology. While optimality models have been successful in providing valuable insight into the evolution of a wide variety of biological traits, a common objection is that optimality models are overly simplistic and ignore organismal genetics. We revisit evolutionary optimization in the context of a major bacteriophage life history trait, lysis time. Lysis time refers to the period spanning phage infection of a host cell and its lysis, whereupon phage progenies are released. Lysis time, therefore, directly determines phage fecundity assuming progeny assembly does not exhaust host resources prior to lysis. Noting that previous tests of lysis time optimality rely on batch culture, we implemented a quasi-continuous culture system to observe productivity of a panel of isogenic phage λ genotypes differing in lysis time. We report that under our experimental conditions, λ phage productivity is maximized around optimal lysis times ranging from 60 to 100 min, and λ wildtype strain falls within this range. It would appear that natural selection on phage λ lysis time uncovered a set of genetic solutions that optimized progeny production in its ecological milieu relative to alternative genotypes. We discuss this finding in light of recent results that lysis time variation is also minimized in the strains with lysis times closer to the λ wild-type strain. Optimality theory presents the idea that natural selection acts on organismal traits to produce genotypes that maximize organismal survival and reproduction. As such, optimality theory is a valuable tool in guiding our understanding of the genetic constraints and tradeoffs organisms experience as their genotypes are selected to produce optimal solutions to biological problems. However, optimality theory is often critiqued as being overly simplistic and ignoring the roles of chance and history in the evolution of organismal traits. We show here that the wild-type genotype of a popular laboratory model organism, the bacteriophage λ, produces a phenotype for a major life history trait, lysis time, that maximizes the reproductive success of bearers of that genotype relative to other possible genotypes. This result demonstrates, as is rarely shown experimentally, that natural selection can achieve optimal solutions to ecological challenges.
优化模型在进化生物学中有着复杂的历史。虽然优化模型在提供对广泛的生物特征进化的有价值的见解方面取得了成功，但一个常见的反对意见是，优化模型过于简单化，忽略了生物体的遗传学。我们重新审视了进化优化在一个主要噬菌体生活史特征——裂解时间中的作用。裂解时间是指噬菌体感染宿主细胞到其裂解的时间段，在此期间噬菌体后代被释放。因此，裂解时间直接决定了噬菌体的繁殖力，假设在裂解之前，后代的组装不会耗尽宿主资源。我们注意到，以前对裂解时间最优性的测试依赖于分批培养，因此我们实施了准连续培养系统来观察一组在裂解时间上不同的同源噬菌体 λ 基因型的生产力。我们报告说，在我们的实验条件下，λ噬菌体的生产力在最佳裂解时间范围（60-100 分钟）内达到最大值，而 λ野生型菌株落在这个范围内。似乎噬菌体 λ裂解时间的自然选择揭示了一组遗传解决方案，这些解决方案相对于其他基因型优化了其生态环境中的后代产生。我们根据最近的结果讨论了这一发现，即裂解时间变化在接近 λ野生型菌株的裂解时间的菌株中也最小化。优化理论提出了这样的观点，即自然选择作用于生物体的特征，以产生最大限度地提高生物体生存和繁殖的基因型。因此，优化理论是指导我们理解生物体经历的遗传限制和权衡的有价值的工具，因为它们的基因型被选择以产生生物问题的最佳解决方案。然而，优化理论经常被批评为过于简单化，忽略了机会和历史在生物体特征进化中的作用。我们在这里表明，一种流行的实验室模式生物噬菌体 λ 的野生型基因型产生了一个主要生活史特征——裂解时间的表型，相对于其他可能的基因型，该表型使该基因型携带者的繁殖成功率最大化。这一结果表明，就像很少在实验中展示的那样，自然选择可以为生态挑战实现最佳解决方案。
