Differentiation of follicular cells in polytrophic ovaries of Neuroptera (Insecta: Holometabola)

Mechanisms that underlie differentiation and diversification of the ovarian follicular epithelium in insects have been best characterized in a fruit fly, Drosophila melanogaster. Recent comparative analyses have shown that dipterans evolved a common, specific system of early patterning of their follicular epithelium, while some of the follicular cells acquired an ability to undertake active and invasive migrations. To gain insight into the evolution of the differentiation pathways we extended comparative analyses to Neuroptera, one of the most archaic holometabolan insects with polytrophic ovaries. Here, we show that the follicular cell differentiation pathway in neuropteran ovaries significantly differs from that observed in Drosophila and its relatives. In neuropteran ovaries differentiation of the germ line cells precedes the organization of the follicular epithelium. In consequence, at early stages of egg chamber formation germ cell clusters are not enveloped completely by the regular follicular epithelium but associate with two types of somatic cells: interstitial and prefollicular cells. Interstitial cells do not contribute to the formation of the follicular epithelium, while prefollicular cells diversify into a number of follicular cell subgroups. Some follicular cells remain in contact with the nurse cell compartment. The remaining ones associate with the lateral aspects of the oocyte and diversify into the mainbody follicular cells and the anterior and posterior centripetal cells. In the advanced stages of vitellogenesis protrusions of the anterior and posterior centripetal cells penetrate the nurse cell-oocyte interface and dragging behind their neighboring mainbody cells, eventually encapsulate the oocyte pole(s) with a confluent epithelial layer. The follicular cells in neuropteran ovaries are not migratory at all. They may only change their position relative to the germ line cells. Almost complete immobility of follicular cells in neuropteran egg chambers results in a lower number of diversified subpopulations when compared to Drosophila and other true flies.

► Follicular cell differentiation in neuropteran ovaries differs from that of Diptera. ► Neuropteran follicular cells are not migratory. ► Germ line cysts are not surrounded by a continuous epithelium until early vitellogenesis. ► Follicular cells encapsulating the oocyte do not exhibit hallmarks of active migration.