Successful production of functional Y eggs derived from spermatogonia transplanted into female recipients and subsequent production of YY supermales in rainbow trout, Oncorhynchus mykiss

Abstract

Abstract Mono-sex culture provides economic advantages in aquaculture. In particular, YY supermales, which produce all-male progeny, are desirable in many fish species whose males have more economically desirable characteristics than females, such as faster growth. The production of YY supermales has been achieved by mating XY males with XY sex-reversed females in many fish species. However, the production of sex-reversed XY females requires long-term estrogen administration, which requires considerable time and labor. As an alternative technique, we attempted a spermatogonia transplantation technique to obtain Y eggs in the present study using rainbow trout, Oncorhynchus mykiss. Spermatogonia are the testicular male germ cells that are known to be able to be involved in oogenesis and subsequently differentiate into functional eggs when transplanted into female recipients (Okutsu et al., 2006a). However, whether Y eggs can be derived from transplanted spermatogonia remains unclear. First, we produced F1 progeny by insemination of donor spermatogonia-derived eggs and wild-type milt and then determined their sex. Out of 16 donor-derived fish examined, 3 and 13 were females and males, respectively (1.0:4.3 female:male ratio). Second, we used the milt from the sex-reversed males, which possessed XX sex chromosome sets, for artificial insemination with the donor spermatogonia-derived eggs produced by the female recipients. In the progeny, 8 out of 21 donor-derived fish examined were males, although no males were observed in the control group produced by sex-reversed XX males and intact XX females. Finally, we produced F2 progeny by insemination of the milt from F1 males, which were generated from spermatogonia-derived eggs and wild-type sperm, and the eggs from wild-type females. As a result of a progeny test, 3 out of 10 F1 males (30.0%) produced all-male progeny in the F2 generation. These findings clearly demonstrate that we successfully achieved the production of Y eggs and subsequent YY supermales via spermatogonia transplantation. The present study offers a unique system that enables us to produce YY supermales without administering exogenous sex steroids. This system can be applied to many valuable fish species targeted for aquaculture. Statement of relevance In this manuscript, we show that a successful production of YY supermales in rainbow trout using spermatogonia transplantation system (for a spermatogonia transplantation system, detailed in Okutsu et al., 2006, PNAS, 103, 2725–2729). The present study offers a promising alternative method to produce YY supermales, which can be applied to a wide range of fish species. This technique is expected to contribute to the development of mono-sex cultures in important aquaculture species.