Histological and global gene expression analysis of the 'lactating' pigeon crop

Abstract

BackgroundBoth male and female pigeons have the ability to produce a nutrient solution in their crop for the nourishment of their young. The production of the nutrient solution has been likened to lactation in mammals, and hence the product has been called pigeon 'milk'. It has been shown that pigeon 'milk' is essential for growth and development of the pigeon squab, and without it they fail to thrive. Studies have investigated the nutritional value of pigeon 'milk' but very little else is known about what it is or how it is produced. This study aimed to gain insight into the process by studying gene expression in the 'lactating' crop.ResultsMacroscopic comparison of 'lactating' and non-'lactating' crop reveals that the 'lactating' crop is enlarged and thickened with two very obvious lateral lobes that contain discrete rice-shaped pellets of pigeon 'milk'. This was characterised histologically by an increase in the number and depth of rete pegs extending from the basal layer of the epithelium to the lamina propria, and extensive proliferation and folding of the germinal layer into the superficial epithelium. A global gene expression profile comparison between 'lactating' crop and non-'lactating' crop showed that 542 genes are up-regulated in the 'lactating' crop, and 639 genes are down-regulated. Pathway analysis revealed that genes up-regulated in 'lactating' crop were involved in the proliferation of melanocytes, extracellular matrix-receptor interaction, the adherens junction and the wingless (wnt) signalling pathway. Gene ontology analysis showed that antioxidant response and microtubule transport were enriched in 'lactating' crop.ConclusionsThere is a hyperplastic response in the pigeon crop epithelium during 'lactation' that leads to localised cellular stress and expression of antioxidant protein-encoding genes. The differentiated, cornified cells that form the pigeon 'milk' are of keratinocyte lineage and contain triglycerides that are likely endocytosed as very low density lipoprotein (VLDL) and repackaged as triglyceride in vesicles that are transported intracellularly by microtubules. This mechanism is an interesting example of the evolution of a system with analogies to mammalian lactation, as pigeon 'milk' fulfils a similar function to mammalian milk, but is produced by a different mechanism.

Biology of the Gastrointestinal Tract in Poultry

“…Crop "milk" is sloughed off epithelial cells containing very high levels of lipid and protein together with very low unconjugated carbohydrates (Shetty et al, 1994). The histological and changes in global gene expression have been characterised by Gillespie et al (2011).…”

A toxic diet: transfer of contaminants to offspring through a parental care mechanism

“…Male and female pigeons, for example Columba livia, produce a rich curd-like substance containing nutrients and antibodies in the crop during breeding that is regurgitated and fed to their offspring (Vandeputte-Poma, 1980;Gillespie et al, 2011). Similar crop-feeding of offspring is observed in flamingos, Phoenicopterus spp., and male emperor penguins, Aptenodytes forsteri (Lang, 1963;Prévost and Vilter, 1963).…”

Proceedings of the 2015 National Toxicology Program Satellite Symposium

“…What exactly signals this in either the male or the female is unknown, but prolactin is certainly important in both sexes (Silver 1984). Global gene expression profiling showed that gene expression patterns were also distinctly different in the ‘lactating’ crop as compared to the non-‘lactating’ crop, including a pigeon ‘milk’ growth factor with biological activity similar to epidermal growth factor, transferrin, and lactoferrin (Gillespie et al, 2011). …”