Precocious maturation in male tiger pufferfish Takifugu rubripes: genetics and endocrinology

Abstract

Testes of the tiger pufferfish Takifugu rubripes are a delicacy in Japan, and selective breeding for a male precocious phenotype, i.e., with early initiation of testes development, is desirable. However, it is unknown if precocious gonad development in this species is under genetic control. Here, we investigated genetic involvement in precociousness by using progeny tests with sires from two cultured populations, including a family line anecdotally known for its precociousness, and a wild population. Progeny derived from the “precocious” line consistently had greater testes weight than that from the other lines, even after accounting for effects of body weight, which indicates that precociousness is truly heritable. We also compared chronological changes in plasma steroid hormones between progenies sired by males from the precocious line and a wild population, and found that the precocious family line had higher levels of plasma estradiol-17β (E2) prior to the initiation of testicular development. Our findings suggest that selective breeding for testes precociousness in the tiger pufferfish is feasible, and that plasma E2 may be an indicator of this phenotype, which would allow for phenotype evaluation without the need to sacrifice specimens.

Genetic Dissection of a Precocious Phenotype in Male Tiger Pufferfish (Takifugu rubripes) using Genotyping by Random Amplicon Sequencing, Direct (GRAS-Di)

“…We produced four full-sib families that were descendants of a grandfather (GF) and a grandmother (GM). The GF individual was derived from one of the major domesticated family lines in Japan and identified as genetically precocious by progeny tests (Yoshikawa et al 2020 ), while GM belonged to another major line not characterized as precocious. These grandparents were crossed in March 2012 at private hatchery in Nagasaki Prefecture, Japan, to obtain the first generation ( F 1 ) (Table 1 ).…”

“…All test families were obtained by in vitro fertilization and reared following the recommendations of Yoshikawa et al ( 2020 ). Each full-sib family of the F 2 generation was cultured separately until the mean standard length (SL) reached approximately 160 mm and mixed in a communal tank in September 2015.…”

“…Testes size is a valuable economic trait, since mature testes, known as “shirako”, are regarded as a delicacy in Japan (Hamasaki et al 2013 ). Recently, a family line which is genetically precocious, i.e., early onset of testicular development about 2 months prior to the other lines, was identified (Yoshikawa et al 2020 ). However, the genetic architecture of the precocious phenotype has not yet been studied.…”

Genomic selection for heterobothriosis resistance concurrent with body size in the tiger pufferfish, Takifugu rubripes

“…The tiger pufferfish Takifugu rubripes is a delicacy in Japan and is one of the most valuable marine fish species in Japanese aquaculture, ranking fourth in production value among cultured finfish 10 . To fulfill the growing demand for this species, selective breeding will be a practical approach to boost farming efficiency; however, tiger pufferfish aquaculture has not yet fully applied this technology 11,12 . Apart from growth-related traits, disease resistance should be highly valued in the breeding program, as disease outbreaks easily hamper the aquaculture industry.…”

“…For example, the breeding program which improves the resistance to sea lice possibly diminishes growth-related traits in farmed Atlantic salmon 27 . Likewise, improving resistance to H. okamotoi may negatively affect growth-related traits in the tiger pufferfish 11 . Thus, simultaneous genetic improvement of resistance to heterobothriosis and body size is most desirable for aquaculture of the tiger pufferfish, although complicated by traits with antagonistic genetic correlations.…”