Lewis James J, Van Belleghem Steven M, Papa Riccardo, Danko Charles G, Reed Robert D
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA.
Baker Institute for Animal Health, Cornell University, Ithaca, NY, USA.
Sci Adv. 2020 Sep 25;6(39). doi: 10.1126/sciadv.abb8617. Print 2020 Sep.
Characterizing the genetic complexity of adaptation and trait evolution is a major emphasis of evolutionary biology and genetics. Incongruent findings from genetic studies have resulted in conceptual models ranging from a few large-effect loci to massively polygenic architectures. Here, we combine chromatin immunoprecipitation sequencing, Hi-C, RNA sequencing, and 40 whole-genome sequences from butterflies to show that red color pattern diversification occurred via many genomic loci. We find that the red wing pattern master regulatory transcription factor Optix binds dozens of loci also under selection, which frequently form three-dimensional adaptive hubs with selection acting on multiple physically interacting genes. Many Optix-bound genes under selection are tied to pigmentation and wing development, and these loci collectively maintain separation between adaptive red color pattern phenotypes in natural populations. We propose a model of trait evolution where functional connections between loci may resolve much of the disparity between large-effect and polygenic evolutionary models.
描绘适应和性状进化的遗传复杂性是进化生物学和遗传学的一个主要重点。遗传学研究中不一致的结果导致了从少数几个大效应基因座到大量多基因结构的概念模型。在这里，我们结合了染色质免疫沉淀测序、Hi-C、RNA测序以及来自蝴蝶的40个全基因组序列，以表明红色图案多样化是通过许多基因组位点发生的。我们发现红色翅膀图案的主要调控转录因子Optix也结合了数十个同样处于选择中的位点，这些位点经常形成三维适应性枢纽，选择作用于多个物理上相互作用的基因。许多处于选择中的Optix结合基因与色素沉着和翅膀发育相关，并且这些位点共同维持了自然种群中适应性红色图案表型之间的分离。我们提出了一个性状进化模型，其中基因座之间的功能联系可能解决大效应和多基因进化模型之间的许多差异。
