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

Department of Animal Developmental Biology, Zoological Institute, University of Wrocław, Wrocław, Poland.
Arthropod structure & development (Impact Factor: 1.65). 03/2012; 41(2):165-76. DOI: 10.1016/j.asd.2011.12.003
Source: PubMed


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.

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    • "As vitellogenesis proceeds, the anterior centripetal cells become hypertrophic and form a prominent anterior fold at the anterior pole of the oocyte. Eventually, the follicular cells of the anterior fold diversify into two distinct subpopulations that contribute to the micropyle formation (Kubrakiewicz et al. 2005; Garbiec and Kubrakiewicz, 2012). It has been previously demonstrated that in neuropteran insects, e.g., Euroleon nostras and Oliarces clara, micropyle canal-forming cells (MCFCs) are radially arranged, and thus the micropyle exhibits inner radial symmetry (Kubrakiewicz et al. 2005). "
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    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.
    Protoplasma 07/2015; DOI:10.1007/s00709-015-0860-z · 2.65 Impact Factor
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    • "It has been found that among many functions, in invertebrates, the follicular cells may contribute to vitellogenesis and formation of the eggshell (reviewed in Dobens and Raftery, 2000). Moreover, based on studies of insect ovaries, it has been shown that the follicular cells are able to diversify into several distinct subpopulations that differ in morphology, behavior, function and position in relation to the germline cells (Zawadzka et al., 1997; Deng and Bownes, 1998; Dobens and Raftery, 2000; Kubrakiewicz et al., 2003; Mazurkiewicz and Kubrakiewicz, 2005, 2008; Tworzyd1o et al., 2005; _ Zelazowska, 2005; Ogorza1ek, 2007; Jaglarz et al., 2008, 2009, 2010; Garbiec and Kubrakiewicz, 2012). Among chelicerates, nutrimentary, i.e. supported with nurse cells, egg development is unique for some acarine groups (Alberti and Hänel, 1986; Alberti and Zeck-Kapp, 1986; Witali nski et al., 1990; Alberti and Coons, 1999; Di Palma and Alberti, 2002). "
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    ABSTRACT: In apoikogenic scorpions, growing oocytes protrude from the gonad (ovariuterus) and develop in follicles exposed to the mesosomal (i.e. hemocoelic) cavity. During subsequent stages of oogenesis (previtellogenesis and vitellogenesis), the follicles are connected to the gonad surface by prominent somatic stalks. The aim of our study was to analyze the origin, structure and functioning of somatic cells accompanying protruding oocytes. We show that these cells differentiate into two morphologically distinct subpopulations: the follicular cells and stalk cells. The follicular cells gather on the hemocoelic (i.e. facing the hemocoel) surface of the oocyte, where they constitute cuboidal epithelium. The arrangement of the follicular cells on the oocyte surface is not uniform, moreover, the actin cytoskeleton of these cells undergoes significant modifications during oocyte growth. During initial stages of the stalk formation the stalk cells elongate and form F-actin rich cytoplasmic processes by which the stalk cells are tightly connected to each other. Additionally, the stalk cells develop microvilli directed towards the growing oocyte. Our findings indicate that the follicular cells covering hemocoelic surfaces of the oocyte and the stalk cells represent two distinct subpopulations of epithelial cells, which differ in morphology, behavior and function.
    Arthropod structure & development 12/2013; 43(4). DOI:10.1016/j.asd.2013.11.004 · 1.65 Impact Factor
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    ABSTRACT: Many male animals have evolved exaggerated traits that they use in combat with rival males to gain access to females and secure their reproductive success. But some male animals invest in nuptial gifts that gains them access to females. Both these reproductive strategies are costly in that resources are needed to produce the weapon or nuptial gift. In closely related species where both weapons and nuptial gifts are present, little is known about the potential evolutionary trade-off faced by males that have these traits. In this study, we use dobsonflies (order Megaloptera, family Corydalidae, subfamily Corydalinae) to examine the presence and absence of enlarged male weapons versus nuptial gifts within and among species. Many dobsonfly species are sexually dimorphic, and males possess extremely enlarged mandibles that they use in battles, whereas in other species, males produce large nuptial gifts that increase female fecundity. In our study, we show that male accessory gland size strongly correlates with nuptial gift size and that when male weapons are large, nuptial gifts are small and vice versa. We mapped weapons and nuptial gifts onto a phylogeny we constructed of 57 species of dobsonflies. Our among-species comparison shows that large nuptial gift production evolved in many species of dobsonfly but is absent from those with exaggerated weapons. This pattern supports the potential explanation that the trade-off in resource allocation between weapons and nuptial gifts is important in driving the diversity of male mating strategies seen in the dobsonflies, whereas reduced male-male competition in the species producing large spermatophores could be an alternative explanation on their loss of male weapons. Our results shed new light on the evolutionary interplay of multiple sexually selected traits in animals. © 2015 The Author(s) Published by the Royal Society. All rights reserved.
    Proceedings of the Royal Society B: Biological Sciences 04/2015; 282(1807):20150247. DOI:10.1098/rspb.2015.0247 · 5.05 Impact Factor