Natural selection constrains neutral diversity across a wide range of species.

Natural selection constrains neutral diversity across a wide range of species.
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DOI:
10.1371/journal.pbio.1002112
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发表时间:
2015-04
期刊:
影响因子:
9.8
通讯作者:
Sackton TB
Sackton TB
中科院分区:
生物学1区
文献类型:
--
作者:
Corbett-Detig RB;Hartl DL;Sackton TB

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分子进化的中性理论预测,一个物种中中性多态性的数量将随着人口普查规模(Nc)成比例地增加。然而,这一预测并没有在实践中得到证实:虽然Nc的范围跨越了许多数量级,但物种内的遗传多样性水平却处于相对较窄的范围内。虽然理论上的争论已经援引了自然选择在更大的群体中的效率增加来解释这种差异,但很少有人对这一假设进行直接的实证检验。在这项工作中,我们提供了一个直接的测试,这一假设使用人口基因组数据,从广泛的分类不同的物种。要做到这一点,我们依赖于这样一个事实,即自然选择对连锁中性多样性的影响取决于当地的重组环境。在相对低重组的区域,选择的变体通过连锁影响更多的中性位点,并且重组和多态性之间的相关性允许定量评估选择对连锁中性多样性的影响的大小。通过比较全基因组多态性数据和遗传图谱的结合建模框架,我们估计在何种程度上自然选择减少了40种专性真核生物的中性多样性。然后,我们表明,自然选择的影响的大小与NC呈正相关,根据身体大小和物种范围作为人口普查人口规模的代理。这些结果表明,自然选择删除了更多的变化,在链接的中性位点的物种与大NC比那些小NC,并提供了直接的经验证据表明,自然选择的约束水平的中性遗传多样性在许多物种。这意味着自然选择可以为这个长期存在的群体遗传学悖论提供一种解释。对40个物种的全基因组遗传变异数据的分析表明,自然选择不成比例地耗尽了种群规模大的物种中的中性变异,这解释了为什么中性多样性水平不随种群规模而变化。群体遗传学的一个基本目标是了解为什么不同物种和群体之间的遗传多样性水平不同。在分子进化的中性模型的假设下,群体中存在的变异量应该与群体的大小成正比。然而,这一预测并不符合现实生活中的观察:遗传多样性水平被发现比预期的要均匀得多,即使在种群规模差异很大的物种之间也是如此。因为自然选择--去除了与遗传相关的中性变异--在更大的群体中更有效,对新突变的选择提供了一个潜在的调和这一矛盾的方法。在这项工作中,我们对齐并联合分析了来自各种物种的全基因组遗传变异数据。使用这个数据集和选择对中性变异的影响的群体遗传模型,我们测试了选择将预防性地消除具有大群体大小的物种中的中性变异的预测。我们发现,自然选择的基因组特征在大多数物种中是普遍存在的,并且通过选择去除的相关中性变异的量与人口规模的代理相关。我们提出,普遍的自然选择约束中性多样性,并提供了一个解释,为什么中性多样性不按预期的规模与人口规模。
The neutral theory of molecular evolution predicts that the amount of neutral polymorphisms within a species will increase proportionally with the census population size (Nc). However, this prediction has not been borne out in practice: while the range of Nc spans many orders of magnitude, levels of genetic diversity within species fall in a comparatively narrow range. Although theoretical arguments have invoked the increased efficacy of natural selection in larger populations to explain this discrepancy, few direct empirical tests of this hypothesis have been conducted. In this work, we provide a direct test of this hypothesis using population genomic data from a wide range of taxonomically diverse species. To do this, we relied on the fact that the impact of natural selection on linked neutral diversity depends on the local recombinational environment. In regions of relatively low recombination, selected variants affect more neutral sites through linkage, and the resulting correlation between recombination and polymorphism allows a quantitative assessment of the magnitude of the impact of selection on linked neutral diversity. By comparing whole genome polymorphism data and genetic maps using a coalescent modeling framework, we estimate the degree to which natural selection reduces linked neutral diversity for 40 species of obligately sexual eukaryotes. We then show that the magnitude of the impact of natural selection is positively correlated with Nc, based on body size and species range as proxies for census population size. These results demonstrate that natural selection removes more variation at linked neutral sites in species with large Nc than those with small Nc and provides direct empirical evidence that natural selection constrains levels of neutral genetic diversity across many species. This implies that natural selection may provide an explanation for this longstanding paradox of population genetics. Analysis of whole genome genetic variation data from 40 species shows that natural selection disproportionately depletes linked neutral variation in species with large population sizes, explaining why levels of neutral diversity do not scale with population size. A fundamental goal of population genetics is to understand why levels of genetic diversity vary among species and populations. Under the assumptions of the neutral model of molecular evolution, the amount of variation present in a population should be directly proportional to the size of the population. However, this prediction does not tally with real-life observations: levels of genetic diversity are found to be substantially more uniform, even among species with widely differing population sizes, than expected. Because natural selection—which removes genetically linked neutral variation—is more efficient in larger populations, selection on novel mutations offers a potential reconciliation of this paradox. In this work, we align and jointly analyze whole genome genetic variation data from a wide variety of species. Using this dataset and population genetic models of the impact of selection on neutral variation, we test the prediction that selection will disproportionally remove neutral variation in species with large population sizes. We show that genomic signature of natural selection is pervasive across most species, and that the amount of linked neutral variation removed by selection correlates with proxies for population size. We propose that pervasive natural selection constrains neutral diversity and provides an explanation for why neutral diversity does not scale as expected with population size.
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