Formation of the proventriculus in the foregut during metamorphosis of the honey bee Apis mellifera Linnaeus, 1758 (Hymenoptera: Apidae).

Abstract

In adult bees, the foregut-midgut transition is marked by the proventriculus, which consists of an anterior muscular bulb extending into the crop lumen and a posterior stomodeal valve in the midgut lumen. In larvae, the proventricular bulb is absent and forms only during metamorphosis, a process that remains poorly understood. This study aimed to describe the cellular events involved in the formation and differentiation of the honey bee Apis mellifera proventriculus during metamorphosis. The foregut-midgut transition of larvae, pupae, and newly emerged adults was analyzed using histology and immunohistochemistry to detect apoptosis, autophagy, cell proliferation, and differentiation. In larvae, the proventriculus consists solely of the stomodeal valve, which disappears in prepupae as the foregut-midgut passage closes. The proventricular bulb precursor emerges in prepupae as a thick epithelium, differentiating alongside the muscle layer until the brown-eyed pupal stage. The stomodeal valve forms in brown-eyed pupae through epithelial invagination towards the foregut lumen and everts in the end of black-eyed pupae stage, projecting into the midgut. Apoptosis was frequent in prepupae but rare in later stages. Autophagy occurred in white- and brown-eyed pupae but was absent in black-eyed pupae. Cell proliferation was observed in prepupae, white- and brown-eyed pupae but not in pink-eyed pupae, where differentiation predominated. No cellular events were detected in black-eyed pupae, marking the end of proventriculus remodeling. The morphogenesis of the A. mellifera proventriculus involves extensive tissue remodeling, with apoptosis, proliferation, and differentiation driving its transformation during metamorphosis.