Experimental evidence of masculinization by continuous illumination in a temperature sex determination teleost (Atherinopsidae) model: is oxidative stress involved?

Abstract

The present study evaluates the influence of continuous light on phenotypic sex ratios in Chirostoma estor, a temperature sex determination animal model. Relative gene expression levels of 5 day old larvae were performed on two early gonad differentiation genes (sox9 and foxl2), two stress axis activation genes (gcr1 and crf) and four reactive oxygen species (ROS) antagonist effector genes (sod2, ucp2, gsr and cat). Two light treatments were applied from fertilization; control (12L:12D) simulated natural photoperiod and a continuous illumination photoperiod. By the end of the trial (12 weeks after hatching), differentiated and normal gonads were clearly identifiable in both treatments by histological observations. Regarding sex ratio, 73% of phenotypic males were found in continuous illumination compared with 40% in controls. Consistently, the sox9 gene (involved in early testis differentiation) showed an over expression in 64% of the individual larvae analysed compared with foxl2 (ovarian differentiation) suggesting a masculinization tendency in continuous illumination. On the other hand, only 36% of individuals showed the same tendency in the control treatment consistent with phenotypic sex ratios found under normal culture conditions. Relative gene expression results did not show significant difference in sod2, ucp2 and gcr1 levels, but cat, gsr and crf showed significantly higher expression levels in the continuous illumination treatment suggesting that both, the stress axis and ROS response mechanisms were activated at this time. This study suggests, a link between continuous light, oxidative stress and environmental sex determination in vertebrates. However, further research is necessary to describe this possible upstream mechanism that may drive some aspects of sexual plasticity in vertebrates.

Phenotypic/genotypic sex mismatches and temperature‐dependent sex determination in a wild population of an Old World atherinid, the cobaltcap silverside Hypoatherina tsurugae

“…Interestingly, this study also uncovered compelling evidence of the influence of daylength during early development on sex determination in cobaltcap silverside, with short and long daylengths inducing masculinization and feminization, respectively (Figure ). This places this species together with the grunion (Brown et al., 2014) and the pike silverside (Corona‐Herrera et al., 2018), other atheriniforms in which sex determination is affected by photoperiod. Although this finding still needs to be scrutinized in carefully conducted laboratory experiments, including the evaluation of synergistic and antagonistic effects with temperature, in hindsight, it may help explain the seemingly paradoxical formation of sex‐reversed males at the relatively low temperatures early and late in the breeding season, the inconsistency between results for wild and reared XY models, as well as the occurrence of some sex‐reversed females at high temperatures in the laboratory experiments (which used a long 14 hr photoperiod).…”

“…and the pike silverside(Corona-Herrera et al, 2018), other atheriniforms in which sex determination is affected by photoperiod. Although this finding still needs to be scrutinized in carefully conducted laboratory experiments, including the evaluation of synergistic and antagonistic effects with temperature, in hindsight, it may help explain the seemingly paradoxical formation of sex-reversed males at the relatively low temperatures early and late in the breeding season, the inconsistency between results for wild and reared XY models, as well as the occurrence of some sex-reversed females at high temperatures in the laboratory experiments (which used a long 14 hr photoperiod).…”

Two transcriptionally distinct pathways drive female development in a reptile with both genetic and temperature dependent sex determination

“…One of these genes, UCP2 , was upregulated at high male producing temperatures in A. mississippiensis (82). UCP2, and others genes involved in oxidative stress responses, were also implicated in UV induced masculinisation in larvae of a thermosensitive fish species ( Chirostoma estor ) (118). Notably, we found that UCP2 was upregulated between stages 6 to 12 in ZZf P. vitticeps embryos, suggesting a sustained response to thermal stress in the mitochondria (Additional file S3).…”

Cellular calcium and redox regulation: the mediator of vertebrate environmental sex determination?

“…Here, we propose a general model in which sex determination is mediated by cellular calcium (Ca 2+ ) and redox (reactive oxygen species; ROS) status, which are subject to environmental influence. Elements of this hypothesis have been discussed in six recent papers that explicitly posited the involvement of either ROS production or Ca 2+ flux in directing the outcomes of ESD (Yatsu et al ., , ; Czerwinski et al ., ; Corona‐Herrera et al ., ; Lin et al ., ; Hayasaka et al ., ). We suggest that these two interrelated signalling systems (Richter & Kass, ) work together to initiate sex determination.…”