Ecological drivers of the evolution of symbiosis

有益的共生现象在自然界广泛存在，是自然和人造生态系统功能的基础。此外，通过为相互作用的物种提供新的生态功能，共生是创新的重要来源，因此在地球上生命的进化中发挥了至关重要的作用。虽然有益的共生关系很重要，但它们的进化很难解释，因为它要求曾经独立的物种克服自身利益，成为一个完整的有机体。一个简单但迄今未被验证的观点是，有益共生可能进化得多稳定，它们开始是一种剥削性的相互作用，其中宿主生物捕获并利用它们的共生体来实现它们提供的有益功能。如果寄主内部的环境与寄主外部的环境有很大的不同，那么随着时间的推移，共生体将适应这个新的生态位，这样一来，由于在每种环境中生存所需的不同特征之间的权衡，它们就失去了在寄主外部茁壮成长的能力。通过这个过程，寄主和共生体物种的适应性利益变得一致，现在彼此依赖对方。在大多数共生相互作用中验证这一观点是不可能的，因为它们起源于数百万年前，现在物种不能分开来测试对自由生活环境的适应。在这个项目中，我们通过单细胞纤毛虫宿主草草虫和绿藻小球藻之间的实验处理微生物共生来克服这一挑战，小球藻既可以生活在宿主细胞内（细胞内生态位），也可以自由生活在淡水中（细胞外生态位）。我们将对来自英国湖泊的自由生活和共生藻类种群进行采样，并比较它们对细胞内和细胞外生态位之间预测变化的关键环境参数的适应性。使用比较基因组学，我们将确定共生和自由生活藻类之间的基因组分化模式，并确定对共生和自由生活方式的遗传适应。最后，我们将在实验室中在自由生活的环境条件下实验进化共生藻类，以测试这是否会通过权衡导致其共生能力的丧失。总之，这些实验将促进我们对共生生物学的理解，帮助解决共生如何以及为什么起源和进化的长期进化难题。这样做的研究也将提供深入了解共生及其在自然和人造生态系统中发挥的重要功能是如何维持的。

Beneficial symbioses are widespread in nature and underpin the function of both natural and manmade ecosystems. Moreover, by providing the interacting species with new ecological functions, symbiosis represents an important source of innovation and has thus played a crucial role in the evolution of life on Earth. Although beneficial symbioses are important, their evolution is hard to explain because it requires for once independent species to overcome their self-interest and become an integrated organism. A simple but so far untested idea for how stable beneficial symbioses might evolve is that they start off as exploitative interactions, wherein the host organism captures and exploits their symbiont for the beneficial function they provide. If the environment inside the host is sufficiently different to that experienced outside the host, the symbiont will over time adapt to this new niche and in so doing lose their ability to thrive outside the host due to trade-offs between the different traits required to survive in each environment. Through this process, the fitness interests of the host and symbiont species become aligned such that each now relies upon the other. Testing this idea in most symbiotic interactions is impossible because they originated millions of years ago and now the species cannot be separated to test for adaptation to free-living environments. In this project we overcome this challenge by using an experimentally tractable microbial symbiosis between the single-celled ciliate host Paramecium and the green alga Chlorella, which can either live inside the host cell (intracellular niche) or live freely in freshwater (extracellular niche). We will sample free-living and symbiotic algal populations from UK lakes, and compare their adaptation to key environmental parameters predicted to vary between the intracellular and extracellular niches. Using comparative genomics we will identify the patterns of genome divergence between the symbiotic and free-living algae and identify genetic adaptations to the symbiotic and free-living lifestyles. Finally, we will experimentally evolve symbiotic algae in the laboratory under free-living environmental conditions to test if this leads to the loss of their symbiotic ability through trade-offs. Together these experiments will advance our understanding of the biology of symbioses, helping to solve the long-standing evolutionary puzzle of how and why symbioses originate and evolve. In so doing the research will also provide insight into how symbioses and the important functions they perform can be maintained in natural and man-made ecosystems.