Singh Prerna, Bruijning Marjolein, Carver Gavriela D, Donia Mohamed S, Metcalf Charlotte Jessica E
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, United States.
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands.
Evol Lett. 2024 Oct 20;9(1):105-114. doi: 10.1093/evlett/qrae052. eCollection 2025 Feb.
The evolution and maintenance of symbiotic systems remains a fascinating puzzle. While the coevolutionary dynamics of bipartite (host-symbiont) systems are well-studied, the dynamics of more complex systems have only recently garnered attention with increasing technological advances. We model a tripartite system inspired by the marine symbiotic relationship between the alga sp., its intracellular defensive bacterial symbiont " Endobryopsis kahalalidifaciens," which produces a toxin that protects the alga against fish herbivores, and the sea-slug (Zan et al., 2019), which is not deterred by the toxin. We disentangle the role of selection on different actors within this system by investigating evolutionary scenarios where defense evolves as (i) a host-controlled trait that reduces algal reproductive ability; (ii) a symbiont-controlled trait that impacts symbiont transmission; and (iii) a trait jointly controlled by both host and symbiont. Optimal investment in defensive toxins varies based on the characteristics of the host, symbiont, and sea slug; and evolutionary trajectories are modulated by trade-off shape, i.e., a strongly decelerating trade-off between defense and symbiont transmission can drive symbiont diversification via evolutionary branching. Increasing slug herbivory reduces host investment in defense to favor reproduction, while symbiont investment in defense first declines and then increases as host density declines to the degree that horizontal symbiont transmission is no longer beneficial. Increasing vertical transmission selects for reduced defense by the host when it evolves as a jointly controlled trait, as a result of investment by the symbiont. Our theoretical exploration of the evolution of defensive symbiosis in scenarios involving interactions with multiple herbivores provides a first window into the origin and maintenance of the sp. system, and adds another piece to the puzzle of the evolution of symbiotic systems.
共生系统的演化与维持仍是一个引人入胜的谜题。虽然二元（宿主 - 共生体）系统的协同进化动态已得到充分研究，但随着技术进步，更复杂系统的动态直到最近才受到关注。我们构建了一个三方系统模型，其灵感来源于藻类、其细胞内防御性细菌共生体“Endobryopsis kahalalidifaciens”（该细菌产生一种毒素，可保护藻类免受草食性鱼类侵害）以及海蛞蝓之间的海洋共生关系（Zan等人，2019年），海蛞蝓不受该毒素影响。我们通过研究防御作为以下几种情况进化时的演化场景，来剖析选择对该系统中不同参与者的作用：（i）一种宿主控制的性状，会降低藻类繁殖能力；（ii）一种共生体控制的性状，会影响共生体传播；（iii）一种由宿主和共生体共同控制的性状。对防御性毒素的最优投入因宿主、共生体和海蛞蝓的特征而异；进化轨迹由权衡形状调节，即防御与共生体传播之间强烈减速的权衡可通过进化分支驱动共生体多样化。海蛞蝓草食作用的增加会降低宿主在防御上的投入，转而有利于繁殖，而共生体在防御上的投入最初会下降，然后随着宿主密度下降到水平共生体传播不再有益的程度而增加。当防御作为一种共同控制的性状进化时，由于共生体的投入，垂直传播的增加会选择宿主降低防御投入。我们对涉及与多种草食动物相互作用的防御性共生进化的理论探索，为 sp. 系统的起源与维持提供了首个窗口，并为共生系统进化之谜增添了另一块拼图。
