Transcriptomic dynamics control rapid transition of core crop functions in 'lactating' pigeon

Pigeons (Columba livia) are widely kept as domesticated pets worldwide, and may have adapted to captivity through the evolutionarily specialized ability to produce ‘milk’ in the crops of both male and female parents via rapid proliferation and shedding of lipid- and protein-enriched epithelial cells. Given the implications for understanding evolution in atricial species, a comprehensive transcriptomic perspective of the pigeon crop spanning the complete breeding cycle is warranted. Here, we generated a de novo pigeon genome assembly to construct a high resolution spatio-temporal transcriptomic landscape of the crop epithelium across the entire breeding cycle. This multi-omics analysis identified a set of ‘lactation’-related genes involved in lipid and protein metabolism that are highly expressed in the crop. Spatial transcriptomics analysis revealed extensive reorganization of long-range promoter-enhancer interactions linked to the dynamic expression of these ‘lactation’-related genes between stages. Moreover, their expression is spatially localized in specific epithelial layers, and can be correlated with phenotypic changes in the crop. This study thus illustrates the preferential de novo synthesis of ‘milk’ lipids and proteins in the crop epithelium prior to shedding from the lumen, and provides candidate enhancer loci for further investigation of the regulatory elements controlling pigeon ‘lactation’. Furthermore, these comprehensive datasets provide a foundational resource for avian and evolutionary biology research, especially relevant to atricial reproductive biology.