Endocrine factors modulating vitellogenesis and oogenesis in insects: An update

The large populations and great variety of insects, with over a million species known, are related to their high rates of reproduction (Adler and Foottit, 2009). In adult insect females, successful reproduction requires five main steps: vitellogenesis, oogenesis, ovulation, fertilization, and oviposition (Fig. 1). Vitellogenesis is characterized by a massive synthesis of yolk protein precursors (YPPs), mainly vitellogenin (Vg), by the fat body, and to a lesser extent, by the ovaries (Raikhel and Dhadialla, 1992). The fat body is a multifunctional organ, distributed throughout the body of the animal, and remotely integrated with different tissues such as the midgut, corpora allata (CA) and central nervous system (CNS), to regulate vitellogenesis by sensing nutritional, hormonal, and neuropeptide signals (S. Li et al., 2019). The CA, situated in the retrocerebral complex, synthesizes juvenile hormone (JH). In conjunction with ecdysteroids produced by the ovaries, JH plays a crucial role in ensuring successful reproduction across various insect species (Khalid et al., 2021). The CNS contains neuroendocrine cells that produce neuropeptides; small proteins (typically 5–80 amino acids) serving as neurohormones, neurotransmitters, or neuromodulators, several of them with direct or indirect gonadoregulatory activities (Lenaerts et al., 2019a; Orchard and Lange, 2024). Upon synthesis, YPPs are released into the circulation and accumulated in oocytes through receptor-mediated endocytosis within specialized organelles called yolk granules (Raikhel and Dhadialla, 1992) (Fig. 1). The yolk, rich in nutrient precursors and energy, serves as a vital resource for embryogenesis (Ramos et al., 2022a). Oogenesis occurs in the ovaries, each containing multiple ovarioles depending on the insect species. The germarium, at the ovariole tip, contains undifferentiated oogonia. Oogenesis is initiated as an oogonial cell commits to becoming an oocyte. The oocytes are then surrounded by follicular cells, forming follicles arranged in a linear progression of increasingly developed stages, with the terminal follicle being in the most advanced stage of development (Nagoshi, 2004). The accumulation of yolk proteins (YPs) by developing oocytes occurs in the vitellarium (Fig. 1). Ovarioles are categorized into two types based on the presence and arrangement of specialized cells that provide trophic support to the oocyte: panoistic ovarioles, where all oogonia eventually transform into oocytes (found in Orthoptera and Blattodea); and meroistic ovarioles, where oogonia can develop into both oocytes and nurse cells. Meroistic ovarioles further classify into polytrophic, with nurse cells and oocytes alternating along the ovariole (found in Diptera and Lepidoptera), and telotrophic, with nurse cells localized in the germarium and connected to oocytes by nutritive or trophic cords (found in Hemiptera and Coleoptera) (Nagoshi, 2004; Trauner and Büning, 2007) (Fig. 1). Following egg formation, ovulation begins with the exit of the egg from the ovariole, making it available for fertilization (if the female has copulated). The sperm is transferred from the spermatheca; storage organs attached to the common oviduct or the bursa. Eggs are deposited synchronously or asynchronously, depending on the species, adding further diversity to the physiological requirements for egg production (Fig. 1).

The endocrine system plays a crucial role in shaping each of the steps of the reproductive process, modulating a series of interconnected events dependent on external and internal signals, such as nutrition, mating, and interactions with other biological functions. Although a few generalizations can be made, the endocrine control has evolved into a complex and coordinated network, unique to an insect species, or sometimes shared within a group of species (Roy et al., 2018). It is worth mentioning that the preponderance of scientific literature focuses on vitellogenesis and oogenesis, i.e., egg formation, while comparatively less attention has been directed towards the processes of ovulation or oviposition, i.e., egg laying. Insights into the neural and endocrine regulation of egg movements through the reproductive system have been studied in-depth in only a few insects (for a comprehensive review, see Lange, 2009; Lange et al., 2022; White, 2021).

The rapid development of technologies, mainly those that have led to the concept of “omics”, gene knockdown mediated by RNA interference (RNAi), and genome editing approaches, such as the CRISPR/Cas9 system, form the basis for accelerating the dissemination of original papers on insect reproduction control in recent years. This review focuses on recent contributions describing the mode of action of endocrine factors that control vitellogenesis and oogenesis, emphasizing insights gained from non-social insect species serving as models. The particular interest in this field is not only to deepen our knowledge about reproduction across insect species, but to respond to the need to manipulate it, both to conserve beneficial organisms (e.g., pollinators) and to combat pests that impact agriculture and public health.

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