Parmenides Center for the Conceptual Foundations of Science, 82049 Pullach/Munich, Germany.
Department of Plant Systematics, Ecology and Theoretical Biology, Institute of Biology, Eötvös Loránd University, 1117 Budapest, Hungary.
Biol Rev Camb Philos Soc. 2018 Feb;93(1):505-528. doi: 10.1111/brv.12355. Epub 2017 Jul 26.
We propose an evolutionary perspective to classify and characterize the diverse systems of adaptive immunity that have been discovered across all major domains of life. We put forward a new function-based classification according to the way information is acquired by the immune systems: Darwinian immunity (currently known from, but not necessarily limited to, vertebrates) relies on the Darwinian process of clonal selection to 'learn' by cumulative trial-and-error feedback; Lamarckian immunity uses templated targeting (guided adaptation) to internalize heritable information on potential threats; finally, shotgun immunity operates through somatic mechanisms of variable targeting without feedback. We argue that the origin of Darwinian (but not Lamarckian or shotgun) immunity represents a radical innovation in the evolution of individuality and complexity, and propose to add it to the list of major evolutionary transitions. While transitions to higher-level units entail the suppression of selection at lower levels, Darwinian immunity re-opens cell-level selection within the multicellular organism, under the control of mechanisms that direct, rather than suppress, cell-level evolution for the benefit of the individual. From a conceptual point of view, the origin of Darwinian immunity can be regarded as the most radical transition in the history of life, in which evolution by natural selection has literally re-invented itself. Furthermore, the combination of clonal selection and somatic receptor diversity enabled a transition from limited to practically unlimited capacity to store information about the antigenic environment. The origin of Darwinian immunity therefore comprises both a transition in individuality and the emergence of a new information system - the two hallmarks of major evolutionary transitions. Finally, we present an evolutionary scenario for the origin of Darwinian immunity in vertebrates. We propose a revival of the concept of the 'Big Bang' of vertebrate immunity, arguing that its origin involved a 'difficult' (i.e. low-probability) evolutionary transition that might have occurred only once, in a common ancestor of all vertebrates. In contrast to the original concept, we argue that the limiting innovation was not the generation of somatic diversity, but the regulatory circuitry needed for the safe operation of amplifiable immune responses with somatically acquired targeting. Regulatory complexity increased abruptly by genomic duplications at the root of the vertebrate lineage, creating a rare opportunity to establish such circuitry. We discuss the selection forces that might have acted at the origin of the transition, and in the subsequent stepwise evolution leading to the modern immune systems of extant vertebrates.
我们提出了一种进化视角，以对在所有主要生命领域发现的多样化适应性免疫系统进行分类和特征描述。我们根据免疫系统获取信息的方式提出了一种新的基于功能的分类：达尔文式免疫（目前已知存在于但不限于脊椎动物中）依赖于克隆选择的达尔文过程，通过累积的试错反馈来“学习”；拉马克式免疫利用模板靶向（引导适应）内化潜在威胁的遗传信息；最后，散弹枪式免疫通过无反馈的体细胞靶向机制运作。我们认为，达尔文式（但非拉马克式或散弹枪式）免疫的起源代表了个体和复杂性进化中的一个根本性创新，并提议将其添加到主要进化转变的列表中。虽然向更高层次的单元的转变需要抑制较低层次的选择，但达尔文式免疫在多细胞生物中重新开启了细胞水平的选择，受指导而非抑制细胞水平进化的机制控制，以个体的利益为导向。从概念上讲，达尔文式免疫的起源可以被视为生命史上最激进的转变，在这种转变中，自然选择的进化实际上已经自我重塑。此外，克隆选择和体细胞受体多样性的结合使从有限的抗原环境信息存储能力转变为几乎无限的能力成为可能。因此，达尔文式免疫的起源既包括个体性的转变，也包括新信息系统的出现——这是主要进化转变的两个标志。最后，我们提出了脊椎动物达尔文式免疫起源的进化情景。我们提出了重新审视脊椎动物免疫“大爆炸”概念的建议，认为其起源涉及一个“困难”（即低概率）的进化转变，这种转变可能只发生过一次，即在所有脊椎动物的共同祖先中。与最初的概念相反，我们认为，限制创新的不是体细胞多样性的产生，而是安全操作具有体细胞靶向的可扩增免疫反应所需的调节回路。脊椎动物谱系起源处的基因组重复增加了调节复杂性，为建立这种调节回路创造了一个难得的机会。我们讨论了可能在转变起源时起作用的选择力，以及随后导致现存脊椎动物现代免疫系统的逐步进化。
