Role of pleiotropy in the evolution of a cryptic developmental variation in Caenorhabditis elegans.
Role of pleiotropy in the evolution of a cryptic developmental variation in Caenorhabditis elegans.
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DOI：
10.1371/journal.pbio.1001230
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发表时间：
2012-01
期刊：
影响因子：
9.8
通讯作者：
Félix MA
中科院分区：
文献类型：
--
作者：
Duveau F;Félix MA
作者利用秀丽隐杆线虫的外阴表型，证明了隐性遗传变异可以通过选择改变适应度的多效效应而进化，并在实验室条件下鉴定出一种赋予驯化蠕虫增强适应度的隐性变异。健壮的生物系统预计会积累隐性遗传变异，在标准条件下不影响系统输出，但一旦在强扰动下表型表达，可能会发挥进化作用。相对于健壮性状的遗传变异是隐性的，因为它不会改变表型，所以它可能会中性地积累，但如果它除了隐性效应外，还影响与适应性相关的性状，那么它也可能在选择下进化。影响外阴细胞间信号网络的隐变先前在秀丽隐杆线虫的野生分离株中被发现。使用定量遗传方法，我们确定了以前未表征的nath-10基因的非同义多态性，当系统被不同的突变致敏时，它会影响外阴表型，但在野生型菌株中不会。nath-10是一种必需的蛋白质乙酰转移酶基因，是人类NAT10的同源基因。nath-10多态性对生活史性状也有非隐性影响。N2参考菌株携带的nath-10等位基因导致产卵率和精子总数的微妙增加，这是影响雌雄同体个体生育能力和最小世代时间之间权衡的性状。我们发现这个等位基因出现在N2的早期实验室培养中，这使我们能够测试它是否在这种新环境下的选择下进化。在实验室条件下，衍生的等位基因确实强于祖先的等位基因。总之，我们确定了一个隐遗传变异的分子性质，并描述了它的进化历史。这些结果表明，隐性遗传变异不一定在整个生物体水平上中性积累，但可能通过选择改变适应度的多效效应而进化。此外，实验室培养导致参考菌株N2对实验室环境的适应性进化，这可能会改变其他感兴趣的表型。鲁棒性是生物系统的一种特性，尽管存在潜在的环境、随机和遗传变异，但它能确保产生可复制的表型。稳健性的一个结果是，潜在的功能性遗传变异可以在自然种群中自由积累，因为它在表型水平上得到了缓冲。即使这种所谓的“隐性”遗传变异在标准条件下没有明显的影响，它也可能在主要的遗传或环境扰动下表现为表型表达。在这里，我们使用模式生物秀丽隐杆线虫来鉴定野生菌株之间外阴细胞命运诱导的隐进化中涉及的遗传变异。我们发现，nath-10基因的突变不仅导致了外阴系统的隐性遗传变异，而且还影响了预期在强大选择压力下的关键生活史性状（幼崽数量、性成熟年龄、精子数量和后代产出率）。事实上，在大约50年前秀丽隐杆线虫实验室驯化过程中出现的nath-10等位基因在实验室条件下比祖先等位基因具有强大的竞争优势。因此，对于一个健壮的性状来说，一个隐性的遗传变异可以影响更敏感的表型，从而在选择下进化。
Using vulval phenotypes in Caenorhabditis elegans, the authors show that cryptic genetic variation can evolve through selection for pleiotropic effects that alter fitness, and identify a cryptic variant that has conferred enhanced fitness on domesticated worms under laboratory conditions. Robust biological systems are expected to accumulate cryptic genetic variation that does not affect the system output in standard conditions yet may play an evolutionary role once phenotypically expressed under a strong perturbation. Genetic variation that is cryptic relative to a robust trait may accumulate neutrally as it does not change the phenotype, yet it could also evolve under selection if it affects traits related to fitness in addition to its cryptic effect. Cryptic variation affecting the vulval intercellular signaling network was previously uncovered among wild isolates of Caenorhabditis elegans. Using a quantitative genetic approach, we identify a non-synonymous polymorphism of the previously uncharacterized nath-10 gene that affects the vulval phenotype when the system is sensitized with different mutations, but not in wild-type strains. nath-10 is an essential protein acetyltransferase gene and the homolog of human NAT10. The nath-10 polymorphism also presents non-cryptic effects on life history traits. The nath-10 allele carried by the N2 reference strain leads to a subtle increase in the egg laying rate and in the total number of sperm, a trait affecting the trade-off between fertility and minimal generation time in hermaphrodite individuals. We show that this allele appeared during early laboratory culture of N2, which allowed us to test whether it may have evolved under selection in this novel environment. The derived allele indeed strongly outcompetes the ancestral allele in laboratory conditions. In conclusion, we identified the molecular nature of a cryptic genetic variation and characterized its evolutionary history. These results show that cryptic genetic variation does not necessarily accumulate neutrally at the whole-organism level, but may evolve through selection for pleiotropic effects that alter fitness. In addition, cultivation in the laboratory has led to adaptive evolution of the reference strain N2 to the laboratory environment, which may modify other phenotypes of interest. Robustness is a property of biological systems that ensures the production of reproducible phenotypes in spite of underlying environmental, stochastic, and genetic variability. A consequence of robustness is that potentially functional genetic variation is free to accumulate in natural populations because it is buffered at the phenotypic level. Even if this so-called “cryptic” genetic variation has no obvious effects under standard conditions, it may become phenotypically expressed upon major genetic or environmental perturbations. Here we used the model organism Caenorhabditis elegans to identify genetic variations involved in the cryptic evolution of vulval cell fate induction between wild strains. We found that a mutation in the essential nath-10 gene not only contributes to cryptic genetic variation in the vulval system, but also affects key life history traits that are expected to be under a strong selective pressure (brood size, age at sexual maturity, sperm number and rate of progeny production). Indeed, an allele of nath-10 that emerged during the laboratory domestication of C. elegans about 50 years ago confers a strong competitive advantage over the ancestral allele under laboratory conditions. A genetic variation that is cryptic for a robust trait can therefore affect more sensitive phenotypes and thus evolve under selection.
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影响因子：
11.8
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