A Transient Hermaphroditic Stage in Early Male Gonadal Development in Little Yellow Croaker, Larimichthys polyactis

Abstract

Animal taxa show remarkable variability in sexual reproduction, where separate sexes, or gonochorism, is thought to have evolved from hermaphroditism for most cases. Hermaphroditism accounts for 5% in animals, and sequential hermaphroditism has been found in teleost. In this study, we characterized a novel form of the transient hermaphroditic stage in little yellow croaker (Larimichthys polyactis) during early gonadal development. The ovary and testis were indistinguishable from 7 to 40 days post-hatching (dph). Morphological and histological examinations revealed an intersex stage of male gonads between 43 and 80 dph, which consist of germ cells, somatic cells, efferent duct, and early primary oocytes (EPOs). These EPOs in testis degenerate completely by 90 dph through apoptosis yet can be rescued by exogenous 17-β-estradiol. Male germ cells enter the mitotic flourishing stage before meiosis is initiated at 180 dph, and they undergo normal spermatogenesis to produce functional sperms. This transient hermaphroditic stage is male-specific, and the ovary development appears to be normal in females. This developmental pattern is not found in the sister species Larimichthys crocea or any other closely related species. Further examinations of serum hormone levels indicate that the absence of 11-ketotestosterone and elevated levels of 17-β-estradiol delineate the male intersex gonad stage, providing mechanistic insights on this unique phenomenon. Our research is the first report on male-specific transient hermaphroditism and will advance the current understanding of fish reproductive biology. This unique gonadal development pattern can serve as a useful model for studying the evolutionary relationship between hermaphroditism and gonochorism, as well as teleost sex determination and differentiation strategies.

Whole-genome assembly and annotation of little yellow croaker (Larimichthys polyactis) provide insights into the evolution of hermaphroditism and gonochorism

“…Finding a transitional species in the evolution of hermaphroditism and gonochorism in Perciformes is very important for the study of the evolution of the fish reproductive spectrum. Our previous study demonstrated that L. polyactis ' unique pattern of testis differentiation is neither typical hermaphroditism nor gonochorism (Xie et al, 2021). We speculate that this gonadal differentiation pattern inL.…”

“…Little yellow croaker (L . polyactis ) was found to be a good model for investigating the direction of evolution of hermaphroditism and gonochorism due to its special sexual reproduction process, in which males undergo a male-specific transient hermaphroditic stage (Xie et al, 2021). Briefly, L .…”

“…In 2015, an artificial breeding programme was successfully established by artificial spawning of wildL. polyactis and larval culture (Chen et al 2016;Liu et al, 2019;Xie et al, 2021). A previous report of a genetic linkage map and karyotype analysis revealed that L .…”

Evaluation of Spawning- and Natal-Site Fidelity of Larimichthys polyactis in the Southern Yellow Sea Using Otolith Microchemistry

“…Larimichthys polyactis can reach sexual maturity after 1 year (Lim et al, 2010;Xie et al, 2021), and fish of the S1 and S2 groups were believed to be in the spawning period. Therefore, the otoliths of the S1 group were analysed for the chemical composition of the core and the first annual ring (Y1) reflecting the local environment of the natal site and the first spawning site, respectively, and those of the S2 and O2 groups were in addition analysed for the composition of the second annual ring (Y2).…”

“…Small yellow croaker (Larimichthys polyactis) is an important commercial fish species endemic to the Northwest Pacific, particularly coastal waters of the East China, Yellow, and Bohai Sea between China and the Korean Peninsula (Lin, 1987). L. polyactis is an iteroparous species, which starts spawning at the age of 1 year, as evidenced by histological analyses of female individuals (Xie et al, 2021). For decades, L. polyactis has been an important source of seafood for local markets in China, Japan, and South Korea (Ma et al, 2020;Szuwalski et al, 2020); however, environmental deterioration and overfishing have led to a major decline in its population since the 1970s (Li et al, 2011).…”