Effect of rapid environmental change on genetic diversity through space and time: selective sweeps and industrial melanism in peppered moths

对快速环境变化的适应性反应通常与极端表型的强选择有关。在最简单的情况下，当正选择的表型来自最近起源的单个突变时，它将与突变染色体的独特扩展单倍型相关联，这样当有利的等位基因传播时，它将与其亲本单倍型的大部分连锁。这种搭便车的过程预计会导致选择目标两侧区域遗传变异的丧失。受影响的染色体区域的大小，以及其中核苷酸多样性下降的速率，取决于与可选单倍型重组的机会，因此取决于可选单倍型的局部频率，发生重组的世代数，种群大小和交叉率。在19世纪的英国，由于烟雾污染影响了这两种变种对鸟类捕食者的相对可见度，在40代之内，黑炭黑变种取代了典型的斑蛾白桦（Biston betularia），预计会产生强烈的搭便车效应。在英格兰西北部的城市制造业地区和邻近的北威尔士农村地区之间，沿炭黑菌频率曲线，与其他单倍型重组的机会可能在空间上有所不同。在英格兰北部的工业中心地带，炭黑菌几乎固定了大约70代，炭黑菌单倍型的多样性应该变化相对较小。相比之下，在1970年后炭黑菌数量下降期间（可能在很大程度上是由来自西部农村的典型移民推动的），预测是炭黑菌位点两侧的连锁不平衡随着时间的推移逐渐被侵蚀，遗传多样性至少部分得到了恢复。最近，我们已经分离出了含有炭黑菌开关位点的基因组区域，现在我们可以很好地研究炭黑菌形态的上升和随后下降的遗传后果。本研究的一个特别之处在于，进化动态将从空间和时间两方面进行分析，通过整合遗传信息，不仅从沿着cline的一系列位置收集的样本中，而且从昆虫学收藏品中保存的历史材料中。这种方法的价值是双重的。首先，它允许对选择和扩散的相互作用过程进行更有力的解剖，其对遗传多样性和连锁不平衡的影响预计会在空间和时间上变化。其次，它提供了临床选择性扫描的文献证据，而不是纯粹基于当代快照的历史重建。100个DNA多态性跨越以炭黑菌位点为中心的3Mb区域，将在大约1000个蛾子的样本中进行分析，这些蛾子代表了沿着cline样带的种群，包括最近几代以及追溯到19世纪的祖先世代。对这些数据的分析将揭示原始突变单倍型的年龄和身份，并确定炭黑菌表型是否只有一个或多个突变起源。遗传多样性的模式将从选择、迁移和时间等方面进行解释，并将炭黑菌与典型单倍型进行对比。通过提供迄今为止最详细的临床选择性扫描重建，我们的研究将对科学的理解做出重大贡献。除了进化生物学家之外，这与公众和环境政策制定者都有关系，前者已经熟悉了胡椒蛾的工业黑化故事，后者需要认识到环境变化的进化后果。

Adaptive responses to rapid environmental change are typically associated with strong selection for extreme phenotypes. In the simplest case, when the positively selected phenotype derives from a single mutation of recent origin, it will be associated with a unique extended haplotype for the mutant chromosome, such that when the favoured allele spreads, it will do so in linkage with a large part of its parent haplotype. This hitch-hiking process is expected to lead to loss of genetic variation in the region flanking the target of selection. The size of the chromosomal region affected, and the rate at which nucleotide diversity declines within it, depends on the opportunity for recombination with alternative haplotypes, and therefore upon the local frequency of alternative haplotypes, the number of generations for recombination to occur, the population size and the crossover rate. The replacement of the typical morph of the peppered moth, Biston betularia, by the black carbonaria morph within 40 generations in 19th c. England, driven by the effects of smoke pollution on the relative visibility of the two morphs to bird predators, is predicted to have generated a strong hitch-hiking effect. The opportunity for recombination with alternative haplotypes is likely to have varied spatially along the carbonaria frequency cline between urban manufacturing areas in northwest England and adjacent rural North Wales. In the industrial heartlands of northern England, where carbonaria was near fixation for about 70 generations, the diversity of carbonaria haplotypes should have changed relatively little. By contrast, during the post-1970 decline of carbonaria, probably fuelled in large part by typical immigrants from the rural west, the prediction is for linkage disequilibrium either side of the carbonaria locus to have been progressively eroded over time, and for genetic diversity to have been at least partially restored. Having recently isolated the genomic region containing the carbonaria switch locus, we are now ideally positioned to examine the genetic consequences of the rise and subsequent fall of the carbonaria morph. A special feature of this study is that the evolutionary dynamics will be analysed with respect to both space and time, by integrating genetic information not only from samples collected at a series of positions along the cline but also from historical material preserved in entomological collections. The value of this approach is twofold. Firstly, it allows for more powerful dissection of the interacting processes of selection and dispersal, whose impacts on genetic diversity and linkage disequilibrium are expected to vary in space and time. Secondly, it provides documentary evidence of a clinal selective sweep, as opposed to a historical reconstruction based purely on a contemporary snapshot. One hundred DNA polymorphisms spanning a 3Mb region centred around the carbonaria locus will be assayed in a sample of about 1000 moths representing the population along the cline transect, in recent generations as well as ancestral generations going back to 19th c. Analysis of these data will reveal the age and identity of the original mutant haplotype, and establish whether the carbonaria phenotype has just one or multiple mutational origins. Patterns in genetic diversity will be explained with respect to selection, immigration and time, and contrasted between carbonaria and typical haplotypes. By providing the most detailed reconstruction to date of a clinal selective sweep our study will make a substantial contribution to the understanding of science. Beyond evolutionary biologists, this is relevant both to the general public, who are already familiar with the story of industrial melanism in peppered moths, and to environmental policy makers who need to appreciate the evolutionary ramifications of environmental change.