Differing strategies of patterning of follicular cells in higher and lower brachycerans (Diptera: Brachycera)

Abstract

In all higher dipterans (Brachycera), including the fruitfly, Drosophila melanogaster, each egg chamber (ovarian follicle) consists of a group (clone) of germ cells (one oocyte and 15 accompanying nurse cells) that is surrounded by a layer of somatic mesodermal follicular cells (FCs). As oogenesis progresses the initially uniform FCs diversify into several morphologically and functionally distinct subpopulations. In D. melanogaster some of these subpopulations, e.g., border, centripetal, and dorsolateral cells, undertake coordinated migration or rearrangement over the surface of the germ cells. During the final stages of oogenesis these subpopulations participate in the formation of a complex, regionally specialized eggshell. In representatives of lower brachycerans (Orthorrhapha), only FCs that undertake active, directed migration are the border cells. These cells originate at the anterior pole of the ovarian follicle and migrate between the nurse cells to the anterior pole of the oocyte. Reduced motility of FCs in lower brachycerans results in the absence of certain FC subpopulations in their egg chambers and subsequent simplicity of their eggshells. We found that the lack of some FC subpopulations coincided with the appearance of lamellipodium-like protrusions of the oocyte. These protrusions penetrated between the apposing membranes of nurse and FCs and partially enveloped the nurse cell compartment. Analysis of whole-mount preparations stained with rhodamine-conjugated phalloidin revealed that the protrusions contained microfilaments and that their tips were equipped with actin-rich filopodium-like processes. We also found that in some lower brachycerans (representatives of the family Rhagionidae), the FCs located at the posterior pole of the oocyte, became enlarged and morphologically similar to the anterior border cells. These findings indicate that in higher dipterans the processes leading to the formation of a functional egg are variable and often markedly different from those in the model organism, D. melanogaster.

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

“…The ovarian follicles of the species investigated in this study (see Table 1) were processed for the light, fluorescent and electron microscopy analysis as previously described (see Tworzydlo et al 2005 for details). In each species, FC diversification has been examined in two to four ovarian follicles at the same stage of development.…”

Follicular cell differentiation in polytrophic ovaries of a moth midge, Tinearia alternata

“…In contrast, in the egg chambers of lower brachycerans, the border cells migration is facilitated by the progressive degradation of the nurse cell complex. No other translocations of FCs have been described in lower brachycerans (Kubrakiewicz et al, 2003, Tworzydlo et al, 2005. Their FCs neither stretch nor migrate centripetally, but rather maintain their position within the epithelium throughout oogenesis.…”

“…Their FCs neither stretch nor migrate centripetally, but rather maintain their position within the epithelium throughout oogenesis. Tworzydlo et al (2005) reported that the FCs in lower brachycerans may change their relative position within the epithelium. This change, however, does not result from the FCs migratory activity, but depends on the specific behaviour of the oocyte.…”

“…The FCs with centripetally expanded processes have also been found in the egg chambers of lower brachycerans (Kubrakiewicz et al, 2003;Tworzydlo et al, 2005) and were regarded as the anteriormost mainbody FCs. The origin of FCs with centripetally oriented extensions in Tinearia is presently unclear.…”

“…In order to gain insight into the evolution of mechanisms of FCs to FCs' differentiation within Brachycera (Kubrakiewicz et al, 2003;Tworzydlo et al, 2005 (Oosterbroek and Courtney, 1995). Within the Nematocera four distinct evolutionary lineages are distinguished: (Tanyderomorpha + Psychodomorpha), Neoneura, Polyneura and Anisoneura (Krzeminski and Krzeminska, 2003).…”