Bilateral BBSRC-FAPESP: A genome wide view of the evolutionary processes shaping genetic variation in natural populations

达尔文的“适者生存”思想是我们理解这个星球上生命多样性的核心。然而，如果只有最适合的生存和繁殖，那么为什么我们看到个体之间在与适合度相关的特征上有这么多差异呢？这个问题在社会系统中尤为突出，在社会系统中，合作的个体会采取某种代价高昂的行为来帮助他人。因此，合作行为对个体及其互动对象（通常是其亲属）的适应性有重要影响。此外，合作的个体面临着被破坏性骗子入侵的风险，这些骗子从合作行为中获益，但却没有支付公平的成本份额。在这种情况下，我们会期望出现“最佳”策略：要么作弊，要么合作。然而，令人惊讶的是，对自然种群的研究常常揭示出个体在合作和欺骗的程度上存在差异。如果欺骗或合作是更好的策略，那么为什么在合作-欺骗连续体上存在差异呢？为了更好地理解这个问题，我们认为重要的是不仅要描述种群中实际存在的变异的本质，还要描述产生这种变异的基因以及形成这种变异的过程。这是因为，尽管进化论可能提出了最好的策略，但所需的基因变化可能是不可能的。例如，一些策略可能不存在，因为任何收益可能被其他适合度成本抵消。另外，合作特征可能很少被表达，或者欺骗的机会有限，因此达尔文选择的行为可能效率太低，无法塑造变异来实现最优或最有利的策略。我们建议用一个简单的系统来解决这个基本问题，这个系统用于研究合作行为，即居住在土壤中的社会性变形虫盘齿龙。在有利条件下，盘状变形虫以单细胞个体的形式存在，以细菌为食生长和分裂。然而，在饥饿的情况下，多达10万只变形虫聚集并合作形成多细胞子实体，由死亡的茎细胞支持的耐寒孢子组成。柄细胞因此牺牲自己来帮助孢子的传播。这样的牺牲是受欢迎的，因为他们通常帮助亲属，但当非亲属互动时，个人的牺牲可能会帮助非亲属。至关重要的是，像其他系统一样，我们发现盘状棘球蚴在许多特征上表现出巨大的多样性，包括不同个体的合作程度，从而为我们提供了一个简单的系统来研究这种差异存在的原因。为了实现这一目标，我们将采用一种新颖的方法组合来分析盘状棘球龙的合作行为和其他特征的遗传和进化。我们将使用大量自然发生的菌株来识别基因的自然变异，这些变异解释了我们观察到的性状的多样性。我们将描述在社会特征中产生自然多样性的基因类型，并询问这些基因是否也影响其他类型的非社会特征，这可能表明它们受到非社会过程的约束或塑造。我们将能够确定似乎对种群变异的维持或持续负责的进化过程的类型。最后，我们将把这些结果与进化模型结合起来，以更好地从理论上理解遗传多样性是如何维持的，以及进化结果是如何受到限制的。因此，这项工作将导致我们对自然种群表型多样性的变异类型和形成这种变异的进化过程的理解取得根本性的进展。

The Darwinian idea of 'survival of the fittest' is central to our understanding of the diversity of life on this planet. However, if only the fittest survive and reproduce, then why do we see so much variation among individuals in traits that are tied to fitness? This problem is especially striking in social systems where cooperating individuals perform some sort of costly act that helps others. Cooperative behaviour therefore has important effects on the fitness of individuals and those that they interact with (often their relatives). Furthermore, cooperating individuals run the risk of invasion by disruptive cheaters that reap the benefits of cooperative behaviours, but do not pay their fair share of the cost. In such situations, we would expect the 'best' strategy to emerge: either cheating or cooperating. Surprisingly, however, studies of natural populations often reveal variation in the degree to which individuals appear to cooperate and cheat. If either cheating or cooperating is the better strategy, then why is there variation along a cooperator-cheater continuum? To better understand this problem, we believe that it is important to not only describe the nature of the variation that is actually present in populations, but also the genes that generate this variation and the processes shaping their variation. This is because, although evolutionary theory may suggest the best strategy, the genetic changes required may not be possible. For example, some strategies may not exist because any gains may be offset by other fitness costs. Alternatively, cooperative traits may be expressed rarely, or there may be limited opportunities to cheat, and as a result the action of Darwinian selection may simply be too inefficient to mould variation to achieve the optimal or favoured strategy.We propose to address this fundamental question using a simple system for the study of cooperative behaviour, the soil dwelling social amoeba Dictyostelium discoideum. Under favourable conditions, D. discoideum amoebae exist as single celled individuals that grow and divide by feeding on bacteria. Upon starvation, however, up to 100,000 amoebae aggregate and cooperate to make a multicellular fruiting body consisting of hardy spores supported by dead stalk cells. Stalk cells thus sacrifice themselves to help the dispersal of spores. Such sacrifices can be favoured because they typically help relatives, but when non-relatives interact, the sacrifices of an individual may help non-relatives. Crucially, like other systems, we have discovered that D. discoideum show enormous diversity in a wide array of traits, including the degree to which different individuals cooperate, thus providing us with a simple system to investigate why such variation exists. To achieve this goal, we will employ a novel combination of approaches in D. discoideum that allow the genetics and evolution of cooperative behaviour and other traits to be analysed with great power. We will use a large panel of naturally occurring strains to identify natural variation in genes that account for the diversity in the traits we observe. We will characterize the types of genes that produce natural diversity in social traits and ask whether those genes also affect other types of non-social traits, which could suggest that they are constrained or shaped by non-social processes. We will be able to determine the types of evolutionary processes that appear to be responsible for the maintenance or persistence of variation in populations. Finally, we will integrate these results with models of evolution to develop a better theoretical understanding of how genetic diversity is maintained and evolutionary outcomes constrained. This work will therefore lead to a fundamental advance in our understanding of the types of variation underlying phenotypic diversity in natural populations and the evolutionary processes shaping that variation.