Evolutionary Dynamics of Nitrogen Fixation in the Legume–Rhizobia Symbiosis

The stabilization of host–symbiont mutualism against the emergence of parasitic individuals is pivotal to the evolution of cooperation. One of the most famous symbioses occurs between legumes and their colonizing rhizobia, in which rhizobia extract nutrients (or benefits) from legume plants while supplying them with nitrogen resources produced by nitrogen fixation (or costs). Natural environments, however, are widely populated by ineffective rhizobia that extract benefits without paying costs and thus proliferate more efficiently than nitrogen-fixing cooperators. How and why this mutualism becomes stabilized and evolutionarily persists has been extensively discussed. To better understand the evolutionary dynamics of this symbiosis system, we construct a simple model based on the continuous snowdrift game with multiple interacting players. We investigate the model using adaptive dynamics and numerical simulations. We find that symbiotic evolution depends on the cost–benefit balance, and that cheaters widely emerge when the cost and benefit are similar in strength. In this scenario, the persistence of the symbiotic system is compatible with the presence of cheaters. This result suggests that the symbiotic relationship is robust to the emergence of cheaters, and may explain the prevalence of cheating rhizobia in nature. In addition, various stabilizing mechanisms, such as partner fidelity feedback, partner choice, and host sanction, can reinforce the symbiotic relationship by affecting the fitness of symbionts in various ways. This result suggests that the symbiotic relationship is cooperatively stabilized by various mechanisms. In addition, mixed nodule populations are thought to encourage cheater emergence, but our model predicts that, in certain situations, cheaters can disappear from such populations. These findings provide a theoretical basis of the evolutionary dynamics of legume–rhizobia symbioses, which is extendable to other single-host, multiple-colonizer systems.

宿主-共生体互利关系抵御寄生个体出现的稳定化过程，对于合作演化而言至关重要。其中最具代表性的共生关系之一，存在于豆科植物与其定殖根瘤菌（rhizobia）之间：根瘤菌从豆科植物获取营养（即收益），同时为宿主提供经由固氮作用合成的氮资源（即成本）。然而，自然环境中广泛分布着低效根瘤菌——这类菌群仅攫取收益而不付出成本，其增殖效率远高于固氮合作型根瘤菌。关于该互利关系如何实现稳定化并在演化中持续存续的问题，学界已展开了大量讨论。

为更好地理解该共生系统的演化动力学，我们基于多参与者连续雪堆博弈（continuous snowdrift game）构建了一个简化模型，并采用适应性动力学（adaptive dynamics）与数值模拟方法对该模型进行研究。我们发现，共生演化进程取决于成本-收益平衡：当成本与收益强度相近时，欺骗者（cheaters）会广泛出现。在此场景下，共生系统的存续与欺骗者的存在并不矛盾，该结果表明共生关系对欺骗者的出现具备鲁棒性，这也可解释自然界中欺骗性根瘤菌的普遍存在。

此外，诸如伙伴忠诚反馈（partner fidelity feedback）、伙伴选择（partner choice）以及宿主制裁（host sanction）等多种稳定化机制，可通过多种途径影响共生体的适合度，从而强化共生关系。该结果提示，共生关系可通过多种机制实现合作式稳定。另有观点认为，混合根瘤种群会促进欺骗者的出现，但我们的模型预测，在特定情境下，欺骗者可从此类种群中消失。

上述发现为豆科植物-根瘤菌共生关系的演化动力学提供了理论基础，该理论框架可拓展至其他单宿主、多定殖者共生系统。