Apoptosis in gonadal somatic cells of scleractinian corals: implications of structural adjustments for gamete production and release

Abstract

Apoptosis is an evolutionarily conserved process of programmed cell death. Here, we show structural changes in the gonads caused by apoptosis during gametogenesis in the scleractinian coral, Euphyllia ancora . Anatomical and histological analyses revealed that from the non-spawning to the spawning season, testes and ovaries increased in size due to active proliferation, differentiation and development of germ cells. Additionally, the thickness and cell density of the gonadal somatic layer decreased significantly as the spawning season approached. Further analyses demonstrated that the changes in the gonadal somatic layer were caused by apoptosis in a subpopulation of gonadal somatic cells. The occurrence of apoptosis in the gonadal somatic layer was also confirmed in other scleractinian corals. Our findings suggest that decreases in thickness and cell density of the gonadal somatic layer are structural adjustments facilitating oocyte and spermary (male germ cell cluster) enlargement and subsequent gamete release from the gonads. In animal reproduction, apoptosis in germ cells is an important process that controls the number and quality of gametes. However, apoptosis in gonadal somatic cells has rarely been reported among metazoans. Thus, our data provide evidence for a unique use of apoptosis in animal reproduction.

Development of an in vitro tissue culture system for hammer coral (Fimbriaphyllia ancora) ovaries

“…In a previous study, we reported a massive apoptotic phenomenon in gonadal somatic cells of F. ancora 8 . We found that while germ cells developed during gametogenesis, many gonadal somatic cells died by apoptosis, resulting in a significant decrease in the thickness and density of the gonadal somatic cell layer 8 . In the present study, ovaries were prepared a month or two before spawning.…”

“…These regions are usually small swellings, conventionally called gonads. Coral gonads are composed of several cell types, including germ cells, gonadal somatic cells, and neurons 7 , 8 .…”

Microbiome heterogeneity in tissues of the coral, Fimbriaphyllia (Euphyllia) ancora

“…Its relatively large polyp size (3–5 cm diameter) allows the microscopic isolation of specific tissues for histological and molecular studies (Chiu et al, 2019 ; Shikina et al, 2013 , 2016 ; Shikina, Chiu, et al, 2015 ). In the past two decades, the reproductive biology of F. ancora has been intensively studied in Taiwan, from the possible role of sex steroids in coral spawning (Twan et al, 2003 , 2006 ) to gametogenesis (Chiu et al, 2020 ; Shikina et al, 2012 , 2020 ; Shikina, Chung, et al, 2015 ). In the present study, we employed F. ancora for a survey of bacterial communities in different coral tissues.…”