Genetic and ecological drivers of molt in a migratory bird

The ability of animals to sync the timing and location of molting (the replacement of hair, skin, exoskeletons or feathers) with peaks in resource availability has important implications for their ecology and evolution. In migratory birds, the timing and location of pre-migratory feather molting, a period when feathers are shed and replaced with newer, more aerodynamic feathers, can vary within and between species. While hypotheses to explain the evolution of intraspecific variation in the timing and location of molt have been proposed, little is known about the genetic basis of this trait or the specific environmental drivers that may result in natural selection for distinct molting phenotypes. Here we take advantage of intraspecific variation in the timing and location of molt in the iconic songbird, the Painted Bunting (Passerina ciris) to investigate the genetic and ecological drivers of distinct molting phenotypes. Specifically, we use genome-wide genetic sequencing in combination with stable isotope analysis to determine population genetic structure and molting phenotype across thirteen breeding sites. We then use genome-wide association analysis (GWAS) to identify a suite of genes associated with molting and pair this with gene-environment association analysis (GEA) to investigate potential environmental drivers of genetic variation in this trait. Associations between genetic variation in molt-linked genes and the environment are further tested via targeted SNP genotyping in 25 additional breeding populations across the range. Together, our integrative analysis suggests that molting is in part regulated by genes linked to feather development and structure (GLI2 and CSPG4) and that genetic variation in these genes is associated with seasonal variation in precipitation and aridity. Overall, this work provides important insights into the genetic basis and potential selective forces behind phenotypic variation in what is arguably one of the most important fitness-linked traits in a migratory bird.

动物可将换蜕皮（毛发、皮肤、外骨骼或羽毛的更替）的时间与位置与资源可获得性峰值同步，该能力对其生态学与进化学研究具有重要意义。在候鸟类群中，迁徙前羽毛换羽期（即旧羽脱落并被更全新、空气动力学性能更优的新羽替代的阶段）的时间与位置，在物种内部及物种间均存在变异。尽管已有研究提出假说，用以解释换羽时间与位置的种内变异的演化机制，但学界对该性状的遗传基础，以及可能促使自然选择形成不同换羽表型的具体环境驱动因素仍知之甚少。本研究以标志性鸣禽丽彩鹀（Passerina ciris）为研究对象，利用其换羽时间与位置的种内变异，探究不同换羽表型的遗传与生态驱动因素。具体而言，本研究结合全基因组遗传测序与稳定同位素分析，对13个繁殖地的种群遗传结构与换羽表型进行测定。随后，我们通过全基因组关联分析（Genome-Wide Association Study, GWAS）筛选出与换羽相关的一系列基因，并结合基因-环境关联分析（Gene-Environment Association Analysis, GEA），探究该性状遗传变异的潜在环境驱动因素。我们进一步通过对分布范围内另外25个繁殖种群的靶向单核苷酸多态性（Single Nucleotide Polymorphism, SNP）基因分型，对换羽相关基因的遗传变异与环境之间的关联进行验证。综合本次研究的所有分析结果表明，换羽过程部分受到与羽毛发育及结构相关的基因（GLI2与CSPG4）调控，且这些基因的遗传变异与降水和干旱程度的季节变化存在关联。总体而言，本研究为换羽这一可以说是候鸟最为重要的适合度相关性状之一的表型变异背后的遗传基础与潜在选择压力提供了重要见解。