Effects of steroid treatment on growth, nutrient partitioning, and expression of genes related to growth and nutrient metabolism in adult triploid rainbow trout (Oncorhynchus mykiss)

Authors: Cleveland, Beth; Weber, Gregory - Greg

Submitted to: Domestic Animal Endocrinology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/17/2016
Publication Date: 7/1/2016
Publication URL: http://handle.nal.usda.gov/10113/62905
Citation: Cleveland, B.M., Weber, G.M. 2016. Effects of steroid treatment on growth, nutrient partitioning, and expression of genes related to growth and nutrient metabolism in adult triploid rainbow trout (Oncorhynchus mykiss). Domestic Animal Endocrinology. 56:1-12.

Interpretive Summary: Growth performance in the diploid (2N, two sets of chromosomes) sexually maturing female rainbow trout is compromised in favor of putting energy into gonad development. For this reason, triploid (3N, three sets of chromosomes) rainbow trout are often raised due to their sterility and subsequent ability to produce a larger fillet without interruptions in growth that is attributed to puberty. It is unknown whether the redirection of nutrients away from muscle growth and viscera fat during sexual maturation is mediated by increased sex steroid signaling or by the high energy demand associated with gonad growth. Triploids fed an estrogen or androgen-containing diet were analyzed against sexually maturing diploids to determine how steroids affect growth, nutrient partitioning, and expression of genes involved in growth and nutrient metabolism. Results indicate that estrogen played a significant role in liver to regulate physiological pathways affecting growth and lipid metabolism, which led to reductions in fish growth and fillet yield. However, steroids did not affect the accumulation of viscera fat in triploids. This study indicates that while estrogen is a maturation-related signal important for directing nutrients away from muscle growth, mobilization of viscera fat is driven primarily by the energy demands of gonad growth. These findings improve our understanding of the interaction between sex steroids and the growth-axis in fish and is knowledge, central for continued improvement of growth performance without negative impacts on reproductive capacity.

Technical Abstract: In rainbow trout sexual maturation occurs parallel with declines in growth performance and fillet quality. For this reason sterile triploids (3N) are often reared for their ability to produce larger fillets and avoid the negative effects of sexual maturation. It is unknown to what extent increases in sex steroid signaling versus a negative energy balance orchestrates the movement of nutrients from growth toward gonad development. In the current study nineteen-month old triploid female rainbow trout were fed an E2-, T-, or DHT- supplemented diet (30 mg/kg diet) for one month. Growth performance, nutrient partitioning, and expression of genes central to growth and nutrient metabolism were compared to triploids and age-matched diploids (2N) consuming a control feed. Only diploid fish exhibited active gonad development, with gonad weights (GSI) increasing from 3.7% to 5.5% of body weight throughout the study while GSI in 3N fish remained at 0.03%. Triploid fish consuming DHT exhibited faster specific growth rates than 3N-Controls. Consumption of E2 in 3N fish reduced fillet growth and caused lower fillet yield compared to all other treatment groups. In contrast, viscera fat gain was not affected by steroid consumption. Gene expression data identified physiological pathways that responded similarly in maturing 2N and E2-treated 3N. In liver these mechanisms included the growth hormone/insulin-like growth factor (IGF) axis (igf1, igf2), IGF binding proteins (igfbp1b1, igfbp2b1, igfbp5b1, igfbp6b1), and genes associated with lipid binding and transport (fabp3, fabp4, lpl, cd36), fatty acid oxidation (cpt1a), and the pparg transcription factor. In muscle these mechanisms included reductions in myogenic gene expression (fst, myog) and the proteolysis-related gene, ctsl, suggesting an E2-induced reduction in the capacity for muscle growth. These findings suggest that elevated E2 signaling during sexual maturation regulates physiological pathways in liver, particularly those related to IGF signaling and lipid metabolism, to partition nutrients away from muscle growth towards support of maturation-related processes. In contrast, the mobilization of viscera lipid stores appear to be mediated less by E2 and more by energy demands associated with gonad development. These findings improve understanding of how steroids regulate nutrient metabolism to meet the high energy demands associated with gonad development during sexual maturation.