Genomic evolution in real time: causes and consequences of an adaptive mutation in the wild

表型变异是进化的原材料，也是自然选择和性选择的目标。然而，进化只能通过DNA水平上基因频率的变化来实现。我们的建议利用最近发现的适应性形态突变，明确地将基因组水平的变化转化为表型水平的变化，然后在野生种群中进行快速和可量化的进化变化。我们将研究太平洋田野蟋蟀Teleogryllus oceanicus的一种突变，这种突变会消除雄性翅膀上产生声音的结构。雄性通常通过唱歌来吸引雌性交配，但在这样做的同时，它们也吸引了一种致命的、靠声音定向的寄生蝇。沉默突变，平翅，出现在2003年的野生种群，并迅速蔓延到近固定在大约20代的过程中，因为它保护男性免受苍蝇的攻击。沉默的平翅雄鸟似乎充当了种群中剩余呼叫者的卫星，通过拦截和与响应的雌鸟交配。平翅突变的迅速传播代表了有史以来野生动物进化速度最快的一次。这种突变是性染色体上遗传的简单孟德尔特征。我们建议的主要目标是（1）确定突变位于基因组的哪个区域，以及潜在的遗传变化，（2）表征平翅和正常翅雄性蟋蟀之间基因表达的大规模差异，以及经历过不同社会环境的蟋蟀之间的差异，这些差异是由于沉默雄性的存在或不存在造成的。这些目标将使进化生物学界更好地理解野生选择所针对的基因组变异类型（例如编码基因与调控基因）。我们的研究结果还将证明一个重大的进化事件如何对其他基因的调控和表达产生连锁效应，从而使新的表型性状受到选择。霸王oceanicus研究系统提供了一个极好的机会来展示进化是如何在真实的时间，在野外，以及如何在一个单一的性状的变化引发了一系列的影响，改变基因表达，表型性状，和选择压力。

Phenotypic variation is the raw material of evolution and the target of natural and sexual selection. However, evolution can only occur through changes in gene frequencies at the level of DNA. Our proposal capitalizes on a recently discovered adaptive morphological mutation to explicitly link how changes at the genomic level translate into changes at the phenotypic level, which are then subject to rapid and quantifiable evolutionary change in a wild population. We will study a mutation in the Pacific field cricket, Teleogryllus oceanicus, that erases sound-producing structures on male wings. Males ordinarily sing to attract females for mating, but in doing so, they also attract a deadly, acoustically-orienting parasitoid fly. The silencing mutation, flatwing, arose in a wild population in 2003 and rapidly spread to near-fixation over the course of approximately 20 generations because it protects males from attack by the fly. Silent flatwing males appear to act as satellites to the remaining callers in the population by intercepting and mating with responding females. The rapid spread of the flatwing mutation represents one of the fastest rates of evolution ever recorded in the wild. The mutation is a simple Mendelian trait inherited on the sex chromosome. The main goals of our proposal are to (1) identify in what region of the genome the mutation resides, and the underlying genetic changes, and (2) characterize broad-scale differences in gene expression between flatwing and normal-wing male crickets, and between crickets that have experienced different social environments resulting from the presence or absence of silent males. These goals will provide the evolutionary biology community with a better understanding of the type of genomic variation targeted by selection in the wild (e.g. coding genes vs. regulatory genes). Our results will also demonstrate how a major evolutionary event has knock-on effects on the regulation and expression of other genes, thereby exposing new phenotypic traits to selection. The T. oceanicus study system provides an excellent opportunity to demonstrate how evolution works in real time, in the wild, and how change in a single trait initiates a cascade of effects that alter gene expression, phenotypic traits, and selection pressure.