Structure of the ovaries and follicular epithelium morphogenesis in Drosophila and its kin

Abstract

In insects, the ovarian follicular epithelium morphogenesis has been intensively studied and best characterized in the fruit fly, Drosophila melanogaster. It is well established that initially identical somatic follicular cells (FCs) form a simple epithelium overlying the germline cells, but during oogenesis, they diversify into a number of morphologically distinct subpopulations each responsible for creating specific eggshell structures. In addition, some FC subpopulations (e.g. polar cells) are indispensable in establishing antero-posterior and dorso-ventral ovarian follicle axes and patterning of the developing embryo. The morphological and molecular changes that occur during follicular epithelium morphogenesis in Drosophila are frequently considered as a paradigm of the FC diversification in all flies. However, recent comparative studies indicate that, in dipterans, the functioning of the ovarian follicles is diverse, group-specific and may significantly differ from the Drosophila model system. We discuss the similarities and differences of the ovary structure and follicular epithelium morphogenesis in different dipteran groups and put them into a phylognetic context. We suggest that the migratory activity of the FCs represents an evolutionary novelty that evolved in the ancestors of higher dipterans (Brachycera). Subsequently, during evolution of this subgroup, the number of migrating FC subpopulations has gradually increased from one (in Orthorrhapha) to four (in Cyclorrhapha).

Formation and structure of egg envelopes in Russian sturgeon Acipenser gueldenstaedtii (Acipenseriformes: Acipenseridae)

“…The classification applied here, based on envelope location on the oocyte surface and egg envelope origin, should be more useful. This type of classification has been successfully used in the description of egg envelopes in several groups of insects (Rościszewska, 1995; Zawadzka et al , 1997; Margaritis & Mazzini, 1998; Jaglarz et al , 2008). The ultrastructure of the oocyte, follicular cells and layers that build the egg envelopes and their arrangement in A. gueldenstaedtii show that the oocyte is covered by three envelopes in stage 5 of egg envelope formation.…”

“…In the investigated species, the shape of main body follicular cells changes from squamous, through rectangular and cuboid in stages 1–3–4 to cuboid (in animal region cells) or cylindrical (in the main body cells) in stages 4–5. It is commonly accepted that all changes in shape during morphogenesis of the follicular epithelium involve the cytoskeleton of cells (Zawadzka et al , 1997; Ogorzałek, 2007; Wu et al , 2008; Jaglarz et al , 2008). In the species investigated, the follicular cells remain connected with the oocyte by means of gap junctions during all stages of egg envelope formation.…”

“…It is commonly accepted that during oocyte development the follicular cells and oocyte interact. This has been thoroughly investigated in numerous insects, including the model organism genus Drosophila (Ogorzałek, 2007; Jaglarz et al , 2008; Wu et al , 2008). As a result of these interactions, the follicular cells diversify, leading to the formation of morphologically different populations of cells.…”

Fine structure and formation of the eggshell in scorpionfly Panorpa liui Hua (Mecoptera: Panorpidae)

“…In the fruit fly Drosophila melanogaster, the follicle cells initially form a uniform epithelium, but during oogenesis they diversify into several morphologically and functionally different cell subpopulations (Dobens and Raftery, 2000;Horne-Badovinac and Bilder, 2005;Jaglarz et al, 2008;Wu et al, 2008). These subpopulations of follicle cells produce different regions of the chorion (Ma et al, 2002).…”

“…Among these subpopulations, the border cells delaminate from the epithelium, surround the anterior pole cells, invade the nurse cell compartment and migrate toward the oocyte (Montell, 2003(Montell, , 2006Niewiadomska et al, 1999). When reaching the anterior pole of oocyte, they begin to form the micropylar apparatus (micropyle), which allows the sperm cells to enter and fertilize the oocyte (Jaglarz et al, 2008). The subpopulations of follicle cells are also investigated in many other insects such as Phthiraptera (Bilinski and Jankowska, 1987), Plecoptera (Rosciszewska, 1995), and Coreidae (Ogorzalek, 2007) and Hydrometridae in Heteroptera (Simiczyjew, 1999).…”