The pattern of the follicle cell diversification in ovarian follicles of the true fruit flies, Tephritidae

• Published in: Journal of anatomy 2024-10, Vol.245 (4), p.643-657
• Main Authors: Jaglarz, Mariusz K., Kuziak, Agata, Jankowska, Wladyslawa
• Format: Article
• Language: English
• Subjects: Animals; Brachycera; Cell differentiation; Cell migration; Diptera; Diversification; Drosophila; Epithelium; epithelium morphogenesis; Female; flies; follicle cells; Follicles; Insects; Morphogenesis; oogenesis; Ovarian Follicle - cytology; Ovaries; Rhagio; Tephritidae; Tephritidae - anatomy & histology; tephritids; Vitellogenesis
• ISSN: 0021-8782; 1469-7580; 1469-7580
• DOI: 10.1111/joa.14065

In flies (Diptera), the ovary displays several distinct patterns of the follicular epithelium formation and diversification. Two main patterns have been identified in the true flies or Brachycera, namely the Rhagio type and the Drosophila type. These patterns align with the traditional division of Brachycera into Orthorrhapha and Cyclorrhapha. However, studies of the follicular epithelium morphogenesis in cyclorrhaphans other than Drosophila are scarce. We characterise the developmental changes associated with the emergence of follicle cell (FC) diversity in two cyclorrhaphans belonging to the family Tephritidae (Brachycera, Cyclorrhapha). Our analysis revealed that the diversification of FCs in these species shows characteristics of both the Rhagio and Drosophila types. First, a distinct cluster of FCs, consisting of polar cells and border‐like cells, differentiates at the posterior pole of the ovarian follicle. This feature is unique to the Rhagio type and has only been reported in species representing the Orthorrhapha group. Second, morphological criteria have identified a significantly smaller number of subpopulations of FCs than in Drosophila. Furthermore, while the general pattern of FC migration is similar to that of Drosophila, the distinctive migration of the anterior‐dorsal FCs is absent. In the studied tephritids, the migration of the anterior polar cell/border cell cluster towards the anterior pole of the oocyte is followed by the posterior migration of the main body cuboidal FCs to cover the expanding oocyte. Finally, during the onset of vitellogenesis, a distinct subset of FCs migrates towards the centre of the ovarian follicle to cover the oocyte's anterior pole. Our study also highlights specific actions of some FCs that accompany the migration process, which has not been previously documented in cyclorrhaphans. These results support the hypothesis that the posterior and centripetal migrations of morphologically unique FC subsets arose in the common ancestor of Cyclorrhapha. These events appear to have occurred fairly recently in the evolutionary timeline of Diptera. The pattern of the follicular epithelium morphogenesis in tephritid flies shows similarities to both less and more evolutionary advanced dipterans. Despite similarities with the Drosophila type of follicle cell (FC) diversification, there is a significantly smaller number of FC subpopulations that can be recognised morphologically, and the distinctive migration of the anterior‐