Environmental effects on sex determination and fertility of fish, with special reference to temperature and atheriniforms

CARLOS A. STRÜSSMANN; GUSTAVO M. SOMOZA; LEANDRO A. MIRANDA; RICARDO S. HATTORI; YOJI YAMAMOTO

Kona

Congreso; 7th International Symposium on Vertebrate Sex Determination; 2015

Fishes worldwide are under a growing threat from environmental problems such as habitat degradation, eutrophication, acidification, climate change, pollutants and endocrine disruptors, among others. The ongoing trend of global warming and associated asymmetric thermal fluctuations will likely impact developmental and physiological processes in fish that include sex determination, gonadogenesis, and reproductive function. Here we present a review of the current knowledge on the effects of temperature on fish gonadal sex differentiation and fertility, with special reference to Atheriniform fishes.Atheriniforms, often called ?silversides?, are found in marine, estuarine, and inland waters around the globe, where they are ecologically and socioeconomically important. Several Atheriniforms are known to have temperature-dependent sex determination (TSD). In the genera Menidia and Odontesthes, the two most studied groups, low and warm temperatures favor the formation of females and males, respectively. In O. bonariensis, all-female and all-male populations are formed when larvae are exposed to environmentally relevant temperatures of 17 and 29ºC, respectively, between 1 and 5 weeks after hatching, a sensitiveness that is unparalleled so far in other fish species. The sex ratios of young-of-the-year O. bonariensis in a natural population monitored for 10 years were highly skewed (10-80% females) and variable from year to year, and this variation was experimentally linked to TSD. We also demonstrated for the first time the occurrence of heat-induced germ cell degeneration in fish, a phenomenon previously known only in males of scrotal mammals (e.g. cryptorchidism). Interestingly, fish females are also susceptible to heat-induced germ cell degeneration. Partial or total loss of fertility in both sexes, tentatively associated with past and prolonged exposure to heat, has been also observed in a natural population.Functional studies have shown that TSD in our fish models involves temperature-induced changes in gene expression, stress (cortisol) response, steroidogenesis, gonadal apoptosis, and likely also brain and pituitary factors. We showed also that histological gonadal sex differentiation in O. bonariensis follows a peculiar chephalocaudal, left-to-right gradient through the bilobed gonadal primordium, which is possibly related to TSD. In contrast to O. bonariensis, sex ratios in the congeneric O. hatcheri remain relatively stable at 1:1 over a range of intermediate temperatures, suggesting a relatively strong genetic component of sex determination. A major sex determinant, amhy (Y-linked anti-Müllerian hormone), has been described from this species. This was the first report of a non-transcription factor, actually a hormone, being implicated as the major sex determinant in vertebrates. This gene was recently found and shown to be functional at intermediate temperatures in the TSD species O. bonariensis. These findings hint at the coexistence of TSD and genotypic sex-determination (GSD) in fish. Apoptosis has been implicated in germ cell degeneration and disappearance from gonads of fish exposed to high temperatures.Skewed sex ratios, sex-reversals, and super-males (YY males) caused by temperature effects on sex determination and partial to total loss of fecundity due to heat-induced germ cell degeneration may become recurrent with further global warming and climate change and cause demographic unbalances and even localized extirpations in this group of fishes.