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

红皇后和蛭形轮虫：如何在长期缺乏有性生殖的情况下跟上共同进化的寄生虫

• 批准号: NE/J01933X/1
• 负责人: Christopher Wilson
• 金额: $ 35.76万
• 依托单位: Imperial College London
• 依托单位国家: 英国
• 项目类别: Fellowship
• 财政年份: 2013
• 资助国家: 英国
• 起止时间: 2013 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FJ01933X%2F1
• 关键词: Red; Queen; bdelloid; rotifers; how

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 However, asexual hosts have no way to change their outdated defences, and are doomed to be overtaken and exterminated.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.

对于进化生物学家来说，性是令人尴尬的，他们几十年来一直在努力解释为什么几乎所有的动物和植物都参与了这种低效的活动。原则上，雌性可以通过产生完全相同的克隆子代来100%有效地传递她们的基因。相比之下，有性行为将雌性在每个后代中的基因赌注降低到50%，其余的由分担很少生产成本的雄性提供。考虑到有性雌性的双重劣势，为什么不是所有的生物都是无性的呢？一个主要的观点是，缺乏基因变异会使无性恋者群体容易患上疾病。在这一观点中，寄生虫和病原体不断进化，以克服宿主的免疫防御。有性寄主可以通过每一代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与寄生虫保持同步。然而，无性宿主无法改变他们过时的防御，注定要被赶超和灭绝。与这一观点一致的是，完全放弃性行为的血统几乎不可避免地在不久后灭绝，而证据表明疾病起到了一定作用。然而，有一个值得注意的和提供信息的例外。蜈蚣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，但一直存在并多样化，形成了450多个物种。他们的成功被称为“进化丑闻”，因为性爱被认为是不可或缺的。它们似乎驳斥了红皇后假说，因为它们患有一系列致命的真菌寄生虫，但并没有像预测的那样被赶尽杀绝。我们应该放弃这个原本很有希望的假设吗？如果蜈蚣类轮虫找到了处理寄生虫的不寻常的替代方法，那该怎么办？如果是这样的话，它们的无性性实际上可能会加强，而不是挑战红皇后的假设。我正在调查蜈蚣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领先于寄生虫。这些动物可以忍受完全的干燥，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，它们会形成微小的颗粒，可以被风吹走数百米。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，从原则上讲，蜈蚣克隆体可以将其共同适应的寄生虫留在身后，并分散到当地寄生虫适应较差的新栖息地。如果这些迁徙发生得足够频繁，任何补丁中的寄生虫都会暴露在一系列不断变化的宿主基因中，就像蜈蚣有性行为一样。我的目标是直接测试这个有趣的场景。我将使用遗传“条形码”来识别和跟踪在英国林地的苔藓丛中迁徙的蜈蚣克隆。我将测试来自同一地区的蜈蚣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竞争中处于领先地位。我将在田野中设置无菌的、隆起的苔藓斑块，看看它们被风吹来的蜈蚣克隆人殖民的速度有多快。其中一些新的补丁将被植入寄生虫的种子，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，这些理论工作描述了蜈蚣是否真的与它们的寄生虫玩着一场“捉迷藏”的生态游戏。如果得到证实，这将是一个令人着迷的、史无前例的解决普遍问题的方案，为扩散在共同进化动力学中的作用提供了新的认识。这也将使“丑闻”的蜈蚣类轮虫与红皇后假说相一致。或者，如果这一有希望的假设被驳斥，蜈蚣的成功将变得更加神秘和耐人寻味，迫使人们认真重新考虑所谓的无性恋者对寄生虫的脆弱性。

项目成果

Comparative genomics of bdelloid rotifers: evaluating the effects of asexuality and desiccation tolerance on genome evolution

蛭形轮虫的比较基因组学：评估无性和耐干燥性对基因组进化的影响

• DOI: 10.1101/226720
• 发表时间: 2017
• 作者: Nowell R

Evidence for "inter- and intraspecific horizontal genetic transfers" between anciently asexual bdelloid rotifers is explained by cross-contamination

交叉污染解释了古代无性蛭形轮虫之间“种间和种内水平遗传转移”的证据

• DOI: 10.1101/150490
• 发表时间: 2017
• 作者: Wilson C

Comparative genomics of bdelloid rotifers: Insights from desiccating and nondesiccating species.

• DOI: 10.1371/journal.pbio.2004830
• 发表时间: 2018-04
• 期刊: PLoS biology
• 影响因子: 9.8
• 作者: Nowell RW;Almeida P;Wilson CG;Smith TP;Fontaneto D;Crisp A;Micklem G;Tunnacliffe A;Boschetti C;Barraclough TG
• 通讯作者: Barraclough TG

Spatial and temporal escape from fungal parasitism in natural communities of anciently asexual bdelloid rotifers

古代无性蛭形轮虫自然群落中真菌寄生的空间和时间逃逸

• DOI: 10.1098/rspb.2013.1255
• 发表时间: 2013
• 期刊: Biological Sciences
• 作者: Wilson C

Comparative genomics of Alexander Fleming's original Penicillium isolate (IMI 15378) reveals sequence divergence of penicillin synthesis genes.

• DOI: 10.1038/s41598-020-72584-5
• 发表时间: 2020-09-24
• 期刊: Scientific reports
• 影响因子: 4.6
• 作者: Pathak A;Nowell RW;Wilson CG;Ryan MJ;Barraclough TG
• 通讯作者: Barraclough TG