Asymmetry in structure of the eggshell in Osmylus fulvicephalus (Neuroptera: Osmylidae): an exceptional case of breaking symmetry during neuropteran oogenesis

Abstract

Ovaries of neuropterans are of meroistic-polytrophic type. The ovarian tubes, the ovarioles, are divided into two major parts: a germarium, comprised of newly formed germ cell clusters; and a vitellarium, housing linearly arranged ovarian follicles. Each ovarian follicle consists of the germ cell cluster diversified into different number of nurse cells, and the oocyte enclosed by follicular epithelium. In Osmylus fulvicephalus, a representative of Neuroptera, during consecutive stages of oogenesis, the follicular cells undergo a multistep process of diversification which leads to the appearance of several follicular cell subpopulations i.e., the main-body follicular cells, the stretched cells, the anterior centripetal cells, and posterior centripetal cells. The anterior centripetal cells occupy the anterior pole of the oocyte and in advanced oogenesis due to hypertrophy that transform into anterior fold cells. Initially, the anterior fold cells form a symmetric fold, but in advanced oogenesis, quite different from other neuropterans studied so far, they undergo uneven hypertrophic growth which results in breaking symmetry of the anterior fold that becomes shifted to the ventral side of the oocyte. Since the anterior fold cells participate in the production of the specialized chorion structure, the micropyle, asymmetric structure of the anterior fold, is reflected both in its asymmetric position and in the asymmetric construction of the micropyle. As a consequence of breaking symmetry of the anterior fold, Osmylus eggshell gains dorso-ventral polarity, which is unusual for neuropterans.

Differentiation of follicular epithelium in polytrophic ovaries of Pieris napi (Lepidoptera: Pieridae)—how far to Drosophila model

“…In contrast, in all investigated lower and higher dipterans (Nematocera and Brachycera), the micropyle apparatus is produced by the highly specialized follicular cells of the anterior pole of the egg chamber (in Drosophila defined as the border cells) (Kubrakiewicz et al 2003; Mazurkiewicz and Kubrakiewicz 2005, 2008; Tworzydlo et al 2005; Jaglarz et al 2008, 2009, 2010; Mazurkiewicz-Kania et al 2012). In many nondipteran insects with the polytrophic type of ovary (including butterflies) (Zelazowska 2005; Tworzydlo and Kisiel 2011; Garbiec and Kubrakiewicz 2012; Garbiec et al 2016; and the present study), these specialized cells do not exist.…”

“…In some insects, e.g., lower Diptera (Nematocera) (Mazurkiewicz and Kubrakiewicz 2005, 2008) and Neuroptera (Garbiec and Kubrakiewicz 2012; Garbiec et al 2016), none of the follicular cell subgroups display ability to active migration. In Nematocera, some of the follicular cells (micropyle forming cells) alter their position within the egg chambers solely by planar migration (dislocations within the epithelium).…”

Two phases for centripetal migration of Drosophila melanogaster follicle cells: initial ingression followed by epithelial migration

“…Centripetal migration appears to vary across insects; for example, lower brachycerans exhibit cellular rearrangements similar to infolding ( Garbiec and Kubrakiewicz, 2012 ; Garbiec et al, 2016 ; Tworzydlo and Kisiel, 2011 ). We assessed whether D. melanogaster centripetal migration might involve infolding of squamous stretch FCs and columnar FCs, as suggested by Tran and Berg (2003) .…”

The structural and functional modularity of ovarian follicle epithelium in the pill-millipedeHyleoglomeris japonica(Myriapoda: Diplopoda: Pentazonia: Glomerida) and the morphological reconsideration of somatic tissues around oocytes in Myriapoda

“…The structural and functional modularity within a somatic tissue covering the oocyte has been known from the follicle cells of many insects such as Diptera (Büning, 1994, Mazurkiewicz and, Lepidoptera Yoshitake, 1984a, b, Mazurkiewicz-Kania et al, 2019), Neuroptera (Kubrakiewicz et al, 2005, Garbiec et al, 2016, Psocodea (Zawadzka et al, 1997), Hemiptera (Büning, 1994), Dermaptera (Tworzydlo and Kisiel, 2011), and Mantophasmatodea (Tsutsumi et al, 2005). Over a century, many histological and ultrastructural studies have uncovered the morphological features of myriapod ovaries and oogenesis (e.g., Tönniges, 1902, Tiegs, 1940, 1945, 1947a, b, Jangi, 1957, Herbaut, 1974, Knoll, 1974, Biliński, 1979, Sareen and Adiyodi, 1983, Kubrakiewicz, 1991a, b, Yahata and Makioka, 1994, Fontanetti et al, 2010, Miyachi and Yahata, 2012, Yahata, 2012, Yahata et al, 2018, Chikami and Yahata, 2019a.…”