Morphological patterns of cell death in ovarian follicles of primary and secondary growth and postovulatory follicle complex of the annual killifish Millerichthys robustus (Cyprinodontiformes: Cynolebiidae)

Abstract

The dynamics of cellular development and homeostasis of the ovary depend on the balance between proliferation and cell death throughout the reproductive cycle.Millerichthys robustus is an annual fish whose ovarian follicles develop asynchronously, allowing daily reproduction from sexual maturity until death. The objective of this research is to describe, histologically, the processes of follicular atresia and regression of postovulatory follicular complexes (POC) throughout a reproductive cycle of M. robustus. Patterns of cell death were documented by apoptosis in atretic follicles and POC, and necrosis in the POC after ovulation with an associated inflammatory response. Atretic follicles were seen from the onset of sexual maturity, duringweek three post-hatching (PH), both in primary growth (from the Cortical alveoli step, with folliculogenesis completed) and secondary growth Stages, with a higher prevalence in the latter. POCs were observed in different stages of regression from week four PH until the death of the fish. The apoptotic characteristics found were:(i) fragmentation of the nuclear membrane and zona pellucida, and liquefaction of the cortical alveoli and yolk; (ii) follicular cells becoming phagocytic, increasing their size, and migrating within the oocyte; and (iii) formation of an intrafollicular lumen, a product of phagocytosis of the oocyte constituents and dispersed pigments that remain after the digestion of yolk and cortical alveoli. The morphological changes of the follicular cells of the POC, from a squamous morphology after ovulation to columnar during its regression with PAS+ contents, was documented, suggesting a secretory activity.

Atresia of ovarian follicles in fishes, and implications and uses in aquaculture and fisheries

“…A possible explanation is that oocytes at advanced stages of primary growth that have not been recruited into vitellogenesis, once they have finalized the building of the organelle machinery and the synthesis of the membrane receptors needed for the uptake of exogenous proteins, cannot survive until the following reproductive season. In the daily spawner killifish, atresia affects both primary and secondary growth follicles from the onset of sexual maturity until fish death, supporting the hypothesis that atresia plays a role in selecting follicles able to perform vitellogenesis and subsequent stages of development (Dominguez‐Castanedo et al, 2019 ).…”

“…In late β atretic follicles, extensive apoptosis of follicular cells occurs (see below) (Morais et al., 2012 ). A large transient cavity has been sometime observed inside β atretic follicles of the killifish Millerichthys robustus (Miller & Hubbs 1974) (Dominguez‐Castanedo et al, 2019 ), which likely results from the extraction of a large lipid drop during tissue processing for histological analysis.…”

“…As described above, oocyte atresia involves the fragmentation of the oocyte envelope to allow follicular cells to enter the oocyte and act as macrophages (Corriero et al., 2004 ; Domínguez‐Castanedo et al., 2019 ; Linares‐Casenave et al., 2002 ; Passantino et al., 2020 ; Santos et al, 2008 ). The loss of integrity of the oocyte results in the spreading of its components—including lysosomal enzymes—outside the follicle and invasion of neighbouring structures (Figure 2c ), an event that can lead to degradation of neighbouring structures, including unyolked and yolked follicles.…”

An autofluorescence‐based survey of late follicular atresia in ovaries of a teleost fish (Thunnus thynnus)

“…The ovarian follicular atresia is a natural process that consists of degeneration and resorption of developing follicles. Although atresia may occur at any stage throughout the oocyte development in teleosts, atretic follicles are more prevalent during secondary growth, because vitellogenic follicles contain a greater amount of reusable energy than earlier oogenetic stages (Domínguez-Castanedo et al, 2019). Atresia is enhanced in stressful situations, such as panic (Corriero et al, 2011), starvation (Corriero et al, 2011;Hunter & Macewicz, 1985), exposure to contaminants (Johnson et al, 1999;Migliaccio et al, 2018) or captivity (Corriero et al, 2004(Corriero et al, , 2007(Corriero et al, , 2011Passantino et al, 2020).…”

“…The physiological and regulatory pathways underlying follicular atresia are complex and involve apoptosis and autophagy mechanisms (Cassel et al ., 2017; González‐Kother et al ., 2020; Krysko et al ., 2008; Morais et al ., 2012; Santos et al ., 2008; Thomé et al ., 2009). The dynamics of these processes has been described in detail in a variety of teleost species, both under light (Cassel et al ., 2017; Domínguez‐Castanedo et al ., 2019; Ferrão et al ., 2020; Grier et al ., 2017; Hunter & Macewicz, 1985; Lambert, 1970; Morais et al ., 2012; Pérez & Figueiredo, 1992; Polder, 1971) and electron microscopy (Besseau & Faliex, 1994; Miranda et al ., 1999; Moktar & Hussein, 2020; Qiang et al ., 2021; Santos et al ., 2008; Thomé et al ., 2009). Overall, the course of fish follicular atresia has been staged into four sequential phases: α, β, γ and δ (Hunter & Macewicz, 1985; Lambert, 1970).…”