Reproductive and programming consequences of a high carbohydrate nutrition of trout broodstock – SweetSex

The first part of the project consisted of the evaluation of dietary carbohydrate utilization by male and female broodstock throughout the reproductive cycle and its consequences on gametogenesis and reproductive performance. To do this, two-year-old female and male rainbow trout were fed either a carbohydrate-free (NC) diet or a 35% carbohydrate (HC) diet throughout the reproductive cycle. Zootechnical parameters and the activities of enzymes involved in carbohydrate metabolism were measured in the liver and gonads over the course of the year. Finally, these broodstock were reproduced to study the effects of such a diet on reproductive performance.

Regarding the results obtained, we have shown that the broodstock fed and used the HC diet throughout the year, were able to grow and did not display postprandial hyperglycaemia, contrary to what is commonly observed in juveniles. Modulation of their hepatic metabolism, with increased glycogenesis, phosphate pentose pathway and better regulation of gluconeogenesis, may be explanations for their better ability to utilize dietary carbohydrates. Finally, although the HC diet induced early maturation in both sexes, the reproductive performance of the fish was not affected, confirming that broodstock are able to reproduce when fed a 35% carbohydrate diet. This work has just been published in Frontiers in Physiology (Callet et al., 2020, In press).

A follow-up of the progeny of these broodstock is underway and some analyses have begun. Their zootechnical performance as well as their short and long term metabolism will be evaluated according to the nutrition received by their parents. Finally, depending on the results obtained and the time remaining, an evaluation of the epigenetic mechanisms potentially underlying the observed phenotypes may be envisaged.

Callet T, Hu H, Larroquet L,Surget A, Liu J, Plagnes-Juan E,Maunas P, Turonnet N,Mennigen JA, Bobe J, Burel C,Corraze G, Panserat S and Marandel L (2020) Exploring the Impact of a Low-Protein High-Carbohydrate Diet in Mature Broodstock of a Glucose-Intolerant Teleost, the Rainbow Trout. Front. Physiol. 11:303. doi: 10.3389/fphys.2020.00303
Marandel L, Callet T, Hu H, Liu J, Mennigen JA, Bobe J, Corraze G, Burel C, Panserat S. Consequences on Gametogenesis and Reproduction Performances of a High Carbohydrate Nutrition During the Whole Reproductive Cycle of Males and Females Trout. Poster presented at Experimental Biology, Orlando, USA, 2019, April 5th-9 th

In order to improve the sustainability of salmonid aquaculture, fishmeal (FM) and fish oil, the traditional ingredients of aquafeeds, must be replaced by renewable, eco-friendly and less costly alternative terrestrial plant products, and particularly digestible carbohydrates. This is particularly true for salmonid broodstock breeding as these animals consume a high quantity of expensive diet and reject important quantity of nitrogen. Indeed the main source of energy in salmon comes from proteins provided by FM. Increasing the proportion of digestible carbohydrates in aquafeed may be one solution to reduce the cost of broodstock feeding because they are easy and economical to produce. Moreover such a replacement will help to limit broodstock environmental impact by providing another energy source, saving protein for growth and thus limiting their environmental impact by decreasing nitrogen waste.
However, salmonids and more particularly rainbow trout (the main fresh water fish produce in Europe) are carnivorous species, and thus usually consider as glucose-intolerant (GI) species and poor user of dietary carbohydrates displaying a decrease in growth and a persistent postprandial hyperglycaemia when (FM) is substituted at more than 20% by digestible carbohydrates in the diet. In particular, the non-inhibition of the last step of the hepatic gluconeogenesis is suspected to be involved in this GI phenotype in trout. However, these findings were mainly deduced from experiments conducted on immature trout juvenile. Studies published in the 90’s strongly suggested that a metabolic switch between liver and gonads, more particularly related to glucose metabolism, occurred during gametogenesis in both males and females. In this regard, our first hypothesize is that trout broodstock should be able to be good users of dietary digestible carbohydrates and be able to regulate and modulate their intermediary metabolism in this purpose.
Nevertheless it is now well accepted that early environmental events, of a nutritional or non-nutritional nature, occurring during the perinatal life at critical developmental windows (including gametogenesis) may result in permanent changes in postnatal growth potential, health and metabolic status. The notion of early programming has clearly been established in fish and especially in trout. Thus our second hypothesize is that feeding broodstock with a high content of digestible carbohydrates should modify gametes and thus impact the phenotype and the intermediary metabolism of offspring in the short and long term. Such programming is also known to be triggered by epigenetics mechanisms.
In this context, SweetSex aims to evaluate 1) the use of dietary carbohydrates by broodstock (both males and females) during the whole reproductive cycle and its consequences on gametogenesis and reproduction performances, 2) the short-term effect of such a broodstock nutrition on alevins at first feeding, and 3) its long-term effect on juveniles metabolism and growth performance with a particular focus on epigenetic mechanism underlying this programming.