Ecological drivers of the evolution of symbiosis

有益的共生体在自然界中广泛存在，并支撑着自然和人造生态系统的功能。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。关于稳定的有益共生体如何进化的一个简单但迄今尚未经过验证的想法是，它们开始时是剥削性的相互作用，其中宿主生物体捕获并利用它们的共生体提供的有益功能。如果宿主内部的环境与宿主外部的环境完全不同，共生体将随着时间的推移而适应这个新的生态位，并且由于在每个环境中生存所需的不同特性之间的权衡而失去在宿主外部茁壮成长的能力。通过这个过程，宿主和共生体物种的适应性利益变得一致，以至于现在彼此依赖。在大多数共生相互作用中测试这一想法是不可能的，因为它们起源于数百万年前，现在物种无法分离以测试对自由生活环境的适应。在这个项目中，我们克服了这一挑战，通过使用一个实验听话的微生物之间的共生单细胞纤毛虫宿主草履虫和绿色小球藻，它可以生活在宿主细胞内（细胞内生态位）或生活在淡水中（细胞外生态位）。我们将从英国湖泊中采集自由生活和共生的藻类种群样本，并将其适应预测在细胞内和细胞外小生境之间变化的关键环境参数进行比较。利用比较基因组学，我们将确定共生和自由生活的藻类之间的基因组分歧的模式，并确定共生和自由生活的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性地进化共生藻类，以测试这是否会导致它们通过权衡失去共生能力。这些实验将共同推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。在这样做的过程中，研究还将深入了解共生体及其所发挥的重要功能如何在自然和人造生态系统中得以维持。

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.