The Red Queen and the bdelloid rotifers: how to keep up with co-evolving parasites in the long-term absence of sexual reproduction

对于进化生物学家来说，性是一件令人尴尬的事情，几十年来，他们一直在努力解释为什么几乎所有的动物和植物都从事这样一种效率低下的活动。原则上，雌性可以通过产生完全相同的克隆女儿来以100%的效率传递它们的基因。相比之下，性行为将雌性在每个后代中的基因股份减少到50%，其余的由雄性提供，雄性分担很少的生产成本。既然有性生殖的雌性动物有这样的双重劣势，为什么不是所有的生物都是无性生殖的呢？一个主要的观点是，缺乏遗传变异使无性繁殖的种群容易受到疾病的影响。在这个被称为“红皇后假说”的观点中，寄生虫和病原体不断进化以克服宿主的免疫防御。有性宿主每一代都可以用新的防御基因组合进行反击，使它们能够在无休止的共同进化竞赛中跟上寄生虫。然而，无性繁殖的寄主无法改变其过时的防御，注定要被超越和灭绝。与这种观点相一致的是，完全放弃性的血统几乎不可避免地在不久之后灭绝，证据表明疾病起了作用。然而，有一个值得注意的例外，蛭形轮虫是一种微小的淡水无脊椎动物，在3000多万年前放弃了性别和雄性，但仍然存在并多样化为450多个物种。他们的成功被称为“进化的丑闻”，因为性被认为是必不可少的。他们似乎反驳了红皇后的假设，因为他们遭受了一系列致命的真菌寄生虫，但并没有像预测的那样灭绝。我们是否应该放弃这个原本很有希望的假设呢？如果蛭形轮虫找到了对付寄生虫的不寻常的替代方法呢？如果是这样的话，它们的无性恋可能实际上会加强，而不是挑战红皇后假设。我正在调查蛭形目生物生活方式的独特方面是否有助于它们在不需要性行为的情况下保持领先于寄生虫。这些动物可以忍受完全干燥，使它们能够在微小的，短暂的苔藓和雨水中茁壮成长。当干燥时，它们形成微小的颗粒，可以被风带到数百米外。然而，至关重要的是，它们的寄生真菌无法承受这一过程。因此，原则上讲，蛭形虫克隆体可以将与它共同适应的寄生虫抛在身后，分散到一个新的栖息地，在那里，当地的寄生虫适应性较差。如果这种迁移发生得足够频繁，任何一个小块中的寄生虫都会暴露在一系列不断变化的宿主基因型中，就像蛭形类在交配一样。我将使用遗传“条形码”来识别和跟踪蛭形虫克隆，因为它们在英国林地的苔藓斑块中迁移。我将测试来自同一地区的蛭形轮虫对真菌寄生虫的抵抗力是否不同，并确定轮虫或它们的敌人是否在比赛中领先。我将在田野里设置无菌的、高出地面的苔藓块，看看它们被风吹来的蛭形虫克隆体殖民的速度有多快。其中一些新的斑块将被寄生虫播种，以确定它们的存在是否有利于具有特定遗传免疫力的轮虫。研究结果将与理论工作进行比较，理论工作描述了蛭形类昆虫是否真的在与它们的寄生虫玩“捉迷藏”的生态游戏。如果得到证实，这将是一个有趣的、前所未有的解决方案，可以解决一个普遍性问题，为传播在共同进化动力学中的作用提供新的视角。这也将调和“可耻的”蛭形轮虫与红皇后假说。或者，如果这个充满希望的假设被推翻，蛭形动物的成功将变得更加神秘和有趣，迫使人们认真地重新考虑无性繁殖者对寄生的脆弱性。

Sex is embarrassing for evolutionary biologists, who have struggled for decades to explain why almost all animals and plants engage in such an inefficient activity. In principle, females could transmit their genes with 100% efficiency by producing identical clonal daughters. Sex, by contrast, reduces a female's genetic stake in each offspring to 50%, with the remainder supplied by a male who shares few of the production costs. Given this twofold disadvantage to sexual females, why aren't all organisms asexual?One leading idea is that a lack of genetic variation leaves asexual populations vulnerable to diseases. In this view, colourfully named the 'Red Queen hypothesis', parasites and pathogens are constantly evolving to overcome the immune defenses of their hosts. Sexual hosts can fight back with new combinations of defensive genes each generation, allowing them to keep up with parasites in an endless co-evolutionary race. However, asexual hosts have no way to change their outdated defences, and are doomed to be overtaken and exterminated. Consistent with this view, lineages that completely abandon sex almost inevitably go extinct soon after, and evidence suggests that disease plays a role. However, there is one remarkable and informative exception.Bdelloid rotifers are microscopic freshwater invertebrates that abandoned sex and males more than 30 million years ago, but have persisted and diversified into more than 450 species. Their success has been called 'an evolutionary scandal,' because sex was believed to be indispensable. They appear to refute the Red Queen hypothesis, as they suffer from a range of deadly fungal parasites, but have not been driven extinct as predicted. Should we abandon this otherwise promising hypothesis? What if bdelloid rotifers have found unusual alternative ways of dealing with parasites? If so, their asexuality may actually strengthen, rather than challenge the Red Queen hypothesis.I am investigating whether unique aspects of the bdelloids' lifestyle help them stay ahead of parasites without needing sex. These animals can tolerate complete desiccation, allowing them to thrive in tiny, ephemeral patches of moss and rainwater. When dry, they form miniscule particles that can be transported by wind for hundreds of metres. Crucially, however, their parasitic fungi cannot withstand this process. In principle, therefore, a bdelloid clone could leave its co-adapted parasites behind, and disperse to a new habitat patch where the local parasites are less well-adapted. If these migrations happen often enough, parasites in any patch will be exposed to a constantly changing array of host genotypes, just as if the bdelloids were having sex.I aim to test this intriguing scenario directly. I will use genetic 'barcodes' to identify and track bdelloid clones as they migrate among patches of moss in UK woodland. I will test whether bdelloids from the same area differ in their resistance to fungal parasites, and determine whether the rotifers or their enemies are 'ahead' in the race. I will set up sterile, elevated patches of moss in the field, to see how quickly they are colonised by windblown bdelloid clones. Some of these new patches will be seeded with parasites, to determine whether their presence favours rotifers with specific genetic immunities. Results will be compared with theoretical work that describes the patterns to expect if bdelloids are indeed playing an ecological game of "hide-and-seek" with their parasites.If confirmed, this would be a fascinating and unprecedented solution to a universal problem, throwing new light on the role of dispersal in co-evolutionary dynamics. It would also reconcile the 'scandalous' bdelloid rotifers with the Red Queen hypothesis. Alternatively, if this promising scenario is refuted, the bdelloids' success would become even more mysterious and intriguing, forcing a serious reconsideration of the supposed vulnerability of asexuals to parasitism.