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

蛭形轮虫（发音不发音的“b”）是数量众多、无害的微型动物，大多数生活在临时的淡水水池或潮湿的栖息地。它们有两个显著的特点：1)它们在没有交配的情况下存活了大约8000万年。没有发现雄性，分子证据与无性繁殖的漫长进化历史相一致。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，蛭形虫被已故的著名进化论者约翰·梅纳德·史密斯教授称为“进化的丑闻”。它们能在几乎完全失水的情况下存活。生物大部分是水，它们需要水来维持生命。然而，蛭形虫是一类可以干燥但不会死亡的生物；它们“耐干燥”。当它们周围的环境变干时，蛭形生物进入一种假死状态，在这种状态下，生命过程变得无法察觉，但当它们重新水化后，它们就会恢复生命，就像什么都没发生过一样。更值得注意的是，它们可以在干燥状态下保持多年而没有明显的不良影响，而且在干燥的情况下，它们对极端的温度和压力具有很强的抵抗力。在本提案中，这些特征之间的潜在联系将探讨与蛭形生物如何使用基因拷贝有关。在二倍体生物中，所有的“单拷贝”基因实际上存在于两个拷贝中，每个拷贝在同源染色体上。现有的证据表明，蛭形体与二倍体相似，因为它们具有大多数被分析基因的两个副本。然而，对于某些基因，也许是15%，它们有四个拷贝。因此，有人提出，蛭形体是退化的四倍体，从具有所有基因的四个拷贝的祖先遗传而来，但其中许多基因在进化过程中丢失了。有性生物在生殖细胞（卵子和精子）的产生过程中经历了一个遗传交换的过程，这导致种群中同源基因拷贝（“等位基因”）的序列非常相似。由于蛭形虫无性繁殖，这不会发生，因此相应的基因拷贝（“前等位基因”）会随着时间的推移而积累变化（“突变”）。因此，先前的等位基因会有本质上不同的DNA序列：这被称为梅塞尔森效应，以第一位发现它的科学家的名字命名。我们最近在蛭形体中表明，一对基因拷贝之间的这种序列差异也会导致功能差异，并且这可能被蛭形体利用来提高它们在干燥环境中生存的能力。以这种方式进化的基因功能不会发生在有性生物中，因此只有无性生物才能利用它。然而，对于蛭形生物如何利用基因拷贝，还有另一种说法。Meselson和他的同事们认为它们是用来修复受损基因的。干燥的一个可能的结果是DNA被破坏，Meselson提出，蛭形生物利用完整的基因拷贝来取代那些受损的基因拷贝。这个过程应该与上面提到的序列分化方向相反，从而消除相关基因拷贝的任何功能分化，以及由此带来的任何进化优势。因此，这一提议将检验这两种相反的观点，并试图发现蛭形轮虫是利用基因拷贝来使基因功能多样化，还是维持基因功能。

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.