Eighty million years without sex: the role of genome structure in bdelloid rotifers

蜈蚣类轮虫是一种数量丰富、无害的微型动物，大多数生活在临时的淡水池或潮湿的栖息地。它们有两个显著的特征：1)它们在没有性行为的情况下存活了大约8000万年。没有男性被发现，分子证据与长期的无性繁殖进化史相一致。虽然其他无性生物是已知的，但它们在进化史上是最近才出现的，通常被认为是进化的死胡同，很快就会灭绝。因此，杰出的进化学家、已故的约翰·梅纳德·史密斯教授称其为“进化丑闻”。2)它们可以在几乎完全失水的情况下存活。生物大多是水，需要保留这些水才能生存。然而，蜈蚣是一类可以干燥但不会死亡的有机体；它们是“耐干燥”的。随着周围环境的干涸，蜈蚣进入一种暂停生命的状态，在这种状态下，生命过程变得不可察觉，但当重新补充水分时，它们会恢复生命，就像什么都没有发生过一样。更值得注意的是，它们可以在干燥状态下保持多年，没有明显的不良影响，而且在干燥时，对极端温度和压力具有高度的抵抗力。在这项建议中，将探索这些特征之间的潜在联系，涉及蜈蚣如何使用基因拷贝。在二倍体生物中，所有的“单拷贝”基因实际上都以两个拷贝的形式存在，每个拷贝都在一个同源染色体上。现有证据表明，蜈蚣与二倍体相似，因为它们分析了大多数基因的两个副本。然而，对于某些基因，可能有15%，它们有四个拷贝。因此，有人认为蜈蚣是退化的四倍体，是拥有四个所有基因副本的祖先的后代，但其中许多已经在进化过程中丢失了。有性生物体在生殖细胞(卵子和精子)的产生过程中经历了基因交换的过程，这导致种群中的同源基因拷贝(等位基因)在序列上非常相似。因为蜈蚣是无性繁殖的，所以这种情况不会发生，因此相应的基因拷贝(前等位基因)会随着时间的推移而累积变化(突变)。因此，以前的等位基因将有本质上不同的DNA序列：这被称为梅塞尔森效应，以第一个发现它的科学家的名字命名。我们最近在蜈蚣类中已经表明，一对基因拷贝之间的这种序列差异也可以导致功能上的差异，这一点可能被蜈蚣利用来提高它们在干燥中生存的能力。这种基因功能的进化不可能发生在有性生物身上，因此只有无性恋者才能利用这一点。然而，还有另一种关于蜈蚣如何使用基因拷贝的建议。梅塞尔森和他的同事们提出，它们被用来修复受损的基因。干燥的一个可能的结果是DNA被破坏，梅塞尔森提出蜈蚣类动物使用完整的基因拷贝来取代那些受损的基因。这个过程应该与上面提到的序列差异相反，从而消除相关基因拷贝的任何功能差异，以及随之而来的任何进化优势。因此，这项提议将检验这两个对立的想法，并试图发现蜈蚣类轮虫是使用基因拷贝来使其基因功能多样化，还是保持基因功能。

Bdelloid (pronounced with a silent 'b') rotifers are abundant, harmless, microscopic animals, most of which live in temporary freshwater pools or damp habitats. They have two remarkable characteristics: 1) They have survived without sex for perhaps 80 million years. No males have ever been found, and molecular evidence is consistent with a long evolutionary history of asexual reproduction. Although other asexual organisms are known, they have arisen recently in evolutionary history and are usually thought to be evolutionary dead ends which will rapidly become extinct. As a result, bdelloids were called 'an evolutionary scandal' by the late Prof John Maynard Smith, a prominent evolutionist. 2) They can survive almost complete water loss. Living creatures are mostly water and need to retain this water to stay alive. However, bdelloids are one group of organisms which can dry but not die; they are 'desiccation tolerant'. As their surroundings dry out, bdelloids enter a state of suspended animation in which life processes become undetectable, but when rehydrated, they come back to life as if nothing had happened. Even more remarkably, they can remain in the dry state for many years without apparent ill effects and, while dry, are highly resistant to extremes of temperature and pressure. In this proposal, potential links between these characteristics will be explored relating to how bdelloids use gene copies. In diploid organisms, all 'single copy' genes are in fact present in two copies, each on a homologous chromosome. The available evidence suggests that bdelloids resemble diploids, in that they have two copies of most genes analysed. However, for some genes, perhaps 15%, they have four copies. It has therefore been suggested that bdelloids are degenerate tetraploids, descending from an ancestor with four copies of all genes, but that many of these have been lost during evolution. Sexual organisms undergo a process of genetic exchange during the generation of germ cells (eggs and sperm) which leads to homologous gene copies ('alleles') in a population being very similar in sequence. Because bdelloids reproduce asexually, this does not happen and therefore corresponding gene copies ('former alleles') will accumulate changes ('mutations') over time. So former alleles will have substantially different DNA sequences: this has been called the Meselson effect after the scientist who first discovered it. We have shown recently in bdelloids that such sequence divergence between one pair of gene copies can also result in functional differences, and that this can potentially be exploited by bdelloids to increase their ability to survive desiccation. Evolution of gene function in this way can't happen in sexual organisms, and it is therefore something that only asexuals can exploit. There is another proposal for how bdelloids use gene copies, however. Meselson and colleagues have suggested that they are used for repairing damaged genes. One likely outcome of drying out is that DNA becomes broken, and Meselson proposes that bdelloids employ intact gene copies to replace those which are damaged. This process should work in the opposite direction to the sequence divergence noted above, and thereby eliminate any functional divergence of related gene copies, and with it any evolutionary advantage it confers. This proposal will therefore test these two opposing ideas and attempt to discover whether bdelloid rotifers use gene copies to diversify the function of their genes, or to maintain gene function.