Salinity and photoperiod modulate pubertal development in Atlantic salmon (Salmo salar)

Abstract

The Atlantic salmon shows substantial life cycle plasticity, which also applies to the timing of puberty. While it is characterized by the activation of the brain-pituitary-gonad axis, many morphophysiological aspects of puberty and the influence of environmental conditions, such as water salinity, are not well understood in fish. Here, 12-month-old Atlantic salmon coming from an out-of-season smoltification regime in December were exposed to freshwater (FW) or seawater (SW) at 16 8C to stimulate puberty under a 24-h constant light (LL) or 12 h light:12 h darkness (LD) photoperiod. These four treatment groups (FWLL, SWLL, FWLD, and SWLD) were studied from January to March. Next to 11-ketotestosterone (11-KT) plasma levels, the expression of pituitary genes (gnrhr4, fshb, and lhb) and spermatogenesis was quantified. When spermatogonial proliferation started, fshb mRNA levels increased steeply and began to decrease when spermatogonial mitosis approached completion and most germ cells had reached meiotic or post-meiotic stages. Conversely, lhb mRNA levels increased progressively during spermatogenesis. Most males in all treatment groups matured, but exposure to SW resulted in the strongest stimulation of the onset of spermatogenesis and elevation of pituitary gnrhr4 and fshb mRNA levels. Later on, the LD photoperiod accelerated, irrespective of the salinity, the completion of spermatogenesis, associated with higher lhb mRNA and 11-KT plasma levels than in the LL groups. We find that both salinity and photoperiod modulated different aspects of spermatogenesis, and resulted in a differential activation of pituitary and testis functions; SW stimulating the onset and the shorter photoperiod the completion of spermatogenesis.

Developmental exposure to progestins causes male bias and precocious puberty in zebrafish (Danio rerio)

“…As in all vertebrates, puberty in fish is governed by the hypothalamus-pituitary-gonad (HPG) axis and is marked by an increased production of gonadotropins (follicle stimulating hormone, FSH; luteinizing hormone, LH) in the pituitary (Chen and Ge, 2012). The timing of puberty is different for different fish species and is influenced by age, size and environmental cues Ge, 2012, 2013;Melo et al, 2014). However, it has been shown that treatment with androgenic steroids can advance the timing of puberty, both with regard to gonadotropin production and gonad maturation (Antonopoulou et al, 1995;Antonopoulou et al, 1999;Melo et al, 2014).…”

“…The timing of puberty is different for different fish species and is influenced by age, size and environmental cues Ge, 2012, 2013;Melo et al, 2014). However, it has been shown that treatment with androgenic steroids can advance the timing of puberty, both with regard to gonadotropin production and gonad maturation (Antonopoulou et al, 1995;Antonopoulou et al, 1999;Melo et al, 2014). There are also several pieces of evidence suggesting that EDCs could be involved in the decreased age of pubertal onset observed in humans over the last decades (Parent et al, 2015).…”

Approaches for delaying sexual maturation in salmon and their possible ecological and ethical implications

“…The timing of maturation events in Atlantic salmon has been linked to physical condition and could possibly be connected to certain set-points or ratios of lipid and protein mass (Thorpe et al, 1990, Thorpe et al, 1998 interacting with external cues, and in particular photoperiod, for initiation of sexual maturation (Melo et al, 2014, Andersson et al, 2013, Benedet et al, 2010, Vikingstad et al, 2008. The high plasticity of salmon seems to allow for specific time windows (signaled through photoperiod) during which the salmon can initiate the sexual maturation process or wait depending on body condition and ambient circumstances (Thorpe et al, 1990, Thorpe et al, 1998.…”

“…Many studies have shown the effect of exposure to artificial light/dark cycles on the onset of maturation; hereby opening an opportunity to postpone maturation by keeping the fish under a light regime not providing photoperiodic cues that could induce maturation (Adams and Thorpe, 1989, Taranger et al, 1998, Porter et al, 1999, Melo et al, 2014. In a study by Porter et al (1999) only 6.1% matured under an artificial light regime (exposed to additional light during night) compared to 61.5% maturing in the control group exposed to the natural light regime.…”

“…activation of the brain-pituitary-gonad axis, activation of steroidogenesis in gonads, and effects of growth and adiposity factors) can be used to develop ways to control the maturation process in such a way that fish health and quality is not deteriorated (Andersson et al, 2013, Benedet et al, 2010, Melo et al, 2014.…”