Comprehensive Transcriptomic and Metabolomic Analysis Revealed the Functional Differences in Pigeon Lactation between Male and Female during the Reproductive Cycle

Simple Summary Lactation is an intriguing reproductive behavior in pigeons, both male and female pigeons participate in crop milk secretion and contribute to the care of their offspring through the division of labor. The question of whether the metabolism and formation of pigeon milk in both males and females follow the same mechanism is an interesting scientific question. We integrated lactation-associated metabolomic and transcriptomic data from the crop tissues of male and female pigeons during the reproductive cycles. We identified a total of 1413 metabolites across 18 crop tissues. During the reproductive cycles, the concentrations of estrone, L-ergothioneine, and L-histidine exhibited the most dynamic changes in females, while estrone, L-anserine, 1-methylhistidine, homovanillate, oxidized glutathione, and reducing glutathione showed the most dynamic changes in males. Through screening DAMs and DEGs, our findings revealed gender-specific differences in the metabolome and gene expressions, with several metabolites and pathways showing significant variations between males and females. Our findings shed light on the distinct modulation of pigeon crop milk metabolism between males and females and provide insights into the potential functions of male and female pigeon milk in the growth, development, and immunity of young pigeons.Abstract Lactation is a unique reproductive behavior in pigeons, with the crop serving as the organ responsible for secreting pigeon milk. Both male and female pigeons can produce crop milk and rear their offspring through a division of labor. Since the time of the secretion of pigeon crop milk is different in the process of feeding the young, whether the metabolism and formation of pigeon milk use the same mechanism is a very interesting scientific question. However, the metabolic dynamics and underlying genetic mechanisms involved in the formation of pigeon crop milk remain unclear, particularly during the incubation-feeding reproductive cycle. In this study, we integrated lactation-associated metabolism and transcriptome data from the crop tissues of both male and female pigeons during the brooding and feeding stages. We mapped the changes in metabolites related to milk formation in the crop tissues during these stages. Through metabolome profiling, we identified 1413 metabolites among 18 crop tissues. During the breeding cycles, the concentrations of estrone, L-ergothioneine, and L-histidine exhibited the most dynamic changes in females. In contrast, estrone, L-anserine, 1-methylhistidine, homovanillate, oxidized glutathione, and reducing glutathione showed the most dynamic changes in males. Gender-specific differences were observed in the metabolome, with several metabolites significantly differing between males and females, many of which were correlated with cytokine binding, immunity, and cytochrome P450 activity. Using this dataset, we constructed complex regulatory networks, enabling us to identify important metabolites and key genes involved in regulating the formation of pigeon milk in male and female pigeons, respectively. Additionally, we investigated gender-associated differences in the crop metabolites of pigeons. Our study revealed differences in the modulation of pigeon crop milk metabolism between males and females and shed light on the potential functions of male and female pigeon milk in the growth, development, and immunity of young pigeons, an area that has not been previously explored. In conclusion, our results provide new insights into the metabolic regulation of pigeon crop milk formation during the brooding and breeding stages. Furthermore, our findings lay the foundation for the accurate development of artificial pigeon milk.