Recent progress has been made in identifying genomic regions implicated in trait evolution on a microevolutionary scale in many species, but whether these are relevant over macroevolutionary time remains unclear. Here, we directly address this fundamental question using bird beak shape, a key evolutionary innovation linked to patterns of resource use, divergence, and speciation, as a model trait. We integrate class-wide geometric-morphometric analyses with evolutionary sequence analyses of 10,322 protein-coding genes as well as 229,001 genomic regions spanning 72 species. We identify 1434 protein-coding genes and 39,806 noncoding regions for which molecular rates were significantly related to rates of bill shape evolution. We show that homologs of the identified protein-coding genes as well as genes in close proximity to the identified noncoding regions are involved in craniofacial embryo development in mammals. They are associated with embryonic stem cell pathways, including BMP and Wnt signaling, both of which have repeatedly been implicated in the morphological development of avian beaks. This suggests that identifying genotype-phenotype association on a genome-wide scale over macroevolutionary time is feasible. Although the coding and noncoding gene sets are associated with similar pathways, the actual genes are highly distinct, with significantly reduced overlap between them and bill-related phenotype associations specific to noncoding loci. Evidence for signatures of recent diversifying selection on our identified noncoding loci in Darwin finch populations further suggests that regulatory rather than coding changes are major drivers of morphological diversification over macroevolutionary times.

中文翻译：

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非编码区在宏观进化尺度上支撑着禽类票据的多样化。

在许多物种的微进化尺度上，鉴定与性状进化有关的基因组区域已取得了最新进展，但是，这些在宏观进化时期是否相关仍不清楚。在这里，我们直接使用鸟嘴形状来解决这个基本问题，鸟嘴形状是与资源利用，分化和物种形成模式相关的关键进化创新，作为模型特征。我们将全类别的几何形态分析与10,322个蛋白质编码基因以及229,001个基因组区域（涵盖72个物种）的进化序列分析相结合。我们确定了1434个蛋白质编码基因和39806个非编码区域，这些区域的分子速率与票据形状演化的速率显着相关。我们表明，已鉴定的蛋白质编码基因以及与已鉴定的非编码区非常接近的基因的同源物都参与了哺乳动物的颅面胚胎发育。它们与胚胎干细胞途径有关，包括BMP和Wnt信号传导，这两种途径都已反复涉及鸟类喙的形态发育。这表明，在宏观进化时间内，在全基因组范围内鉴定基因型-表型关联是可行的。尽管编码和非编码基因集与相似的途径相关，但实际基因却截然不同，它们与非编码基因座特有的票据相关表型关联之间的重叠大大减少。