A non-coding region near Follistatin controls head colour polymorphism in the Gouldian finch

Discrete color morphs coexisting within a single population are common in nature. In a broad range of organisms, sympatric color morphs often display major differences in other traits, including morphology, physiology, or behavior. Despite the repeated occurrence of this phenomenon, our understanding of the genetics that underlie multi-trait differences and the factors that promote the long-term maintenance of phenotypic variability within a freely interbreeding population are incomplete. Here, we investigated the genetic basis of red and black head color in the Gouldian finch (Erythrura gouldiae), a classic polymorphic system in which naturally occurring color morphs also display differences in aggressivity and reproductive success. We show that the candidate locus is a small (~70 Kb) non-coding region mapping to the Z-chromosome near the Follistatin (FST) gene. Unlike recent findings in other systems where phenotypic morphs are explained by large inversions containing hundreds of genes (so-called ‘supergenes’), we did not identify any structural rearrangements between the two haplotypes using linked-read sequencing technology. Nucleotide divergence between the red and black alleles was high when compared to the remainder of the Z-chromosome, consistent with their maintenance as balanced polymorphisms over several million years. Our results illustrate how pleiotropic phenotypes can arise from simple genetic variation, likely regulatory in nature.

自然界中，单一种群内共存多种离散色型（discrete color morphs）的现象极为常见。在广泛的生物类群中，同域分布的不同色型往往在形态、生理或行为等其他性状上呈现显著差异。尽管该现象已被多次观测到，但我们对多性状差异背后的遗传机制，以及在自由交配种群中促进表型变异长期维持的因素仍缺乏完整认知。本研究以七彩文鸟（*Erythrura gouldiae*）这一经典多态性研究体系为对象，探究其头部红色与黑色羽色的遗传基础——该物种的自然色型在攻击性与繁殖成功率上同样存在差异。我们所鉴定的候选基因座为一段长约70 Kb的小型非编码区域，定位于Z染色体上卵泡抑素（Follistatin, FST）基因附近。与近期其他研究体系中，表型多态性由包含数百个基因的大型倒位（即所谓‘超基因’（supergenes））所调控的结论不同，我们通过连锁读长测序技术（linked-read sequencing technology）未在两种单倍型（haplotype）间检测到任何结构重排现象。相较于Z染色体的其余区域，红色与黑色等位基因间的核苷酸分歧（nucleotide divergence）水平更高，这与二者作为平衡多态性（balanced polymorphism）已维持数百万年的推论相符。本研究结果表明，多效性表型（pleiotropic phenotypes）可由简单的遗传变异产生，且该变异大概率属于调控型变异。