Abstract
Domestication of animals imposes strong targeted selection for desired traits but can also result in unintended selection due to new domestic environments. Atlantic salmon (Salmo salmar) was domesticated in the 1970s and has subsequently been selected for faster growth in systematic breeding programmes. More recently, salmon aquaculture has replaced fish oils (FOs) with vegetable oils (VOs) in feed, radically changing the levels of essential long-chain polyunsaturated fatty acids (LC-PUFAs). Our aim here was to study the impact of domestication on metabolism and explore the hypothesis that the shift to VO diets has unintentionally selected for a domestication-specific lipid metabolism. We conducted a 96-day feeding trial of domesticated and wild salmon fed diets based on FOs, VOs or phospholipids, and compared transcriptomes and fatty acids in tissues involved in lipid absorption (pyloric caeca) and lipid turnover and synthesis (liver). Domesticated salmon had faster growth and higher gene expression in glucose and lipid metabolism compared to wild fish, possibly linked to differences in regulation of circadian rhythm pathways. Only the domesticated salmon increased expression of LC-PUFA synthesis genes when given VOs. This transcriptome response difference was mirrored at the physiological level, with domesticated salmon having higher LC-PUFA levels but lower 18:3n-3 and 18:2n-6 levels. In line with this, the VO diet decreased growth rate in wild but not domesticated salmon. Our study revealed a clear impact of domestication on transcriptomic regulation linked to metabolism and suggests that unintentional selection in the domestic environment has resulted in evolution of stronger compensatory mechanisms to a diet low in LC-PUFAs.
Highlights
The genetics and physiology of domesticated animals are heavily influenced by the initial domestication process, the captive environment, followed by persistent targeted selection for desirable animal production traits such as faster growth and delayed sexual maturation (Mueller & Diamond, 2001; Zeder, 2015)
We hypothesized that the shift to vegetable oils (VOs) diets has selected for a domestication-specific lipid metabolism phenotype to compensate for dietary shortage of LC-PUFAa. We approach this question by feeding domesticated and wild salmon contrasting diets either rich in fish oils (FOs), VOs or phospholipid oil (PL), and perform comparative analyses of transcriptomes and fatty acids in tissues involved in lipid uptake and endogenous synthesis
Fish for gene expression and fatty acid measurements were sampled at 94 dpf, when domesticated fish reached an average weight of 4.5 g and wild salmon 2.6 g
Summary
The genetics and physiology of domesticated animals are heavily influenced by the initial domestication process, the captive environment, followed by persistent targeted selection for desirable animal production traits such as faster growth and delayed sexual maturation (Mueller & Diamond, 2001; Zeder, 2015). The LC-PUFAs are important for fish because they are key components of cell membranes, they regulate cell membrane fluidity, function as precursors for eicosanoid production and are important components of neural tissues (Sargent, Tocher, & Bell, 2002; Tocher & Glencross, 2015) This is reflected in the ability of domesticated salmon to increase endogenous synthesis of LC-PUFAs when given VO-rich diets (Datsomor et al, 2019; Stubhaug, Tocher, Bell, Dick, & Torstensen, 2005; Zheng, Tocher, Dickson, Bell, & Teale, 2004). We approach this question by feeding domesticated and wild salmon contrasting diets either rich in FOs, VOs or PLs, and perform comparative analyses of transcriptomes and fatty acids in tissues involved in lipid uptake (pyloric caeca) and endogenous synthesis (liver) This experiment allows us to identify metabolic pathways that respond differently in domesticated compared to wild salmon and reveal novel lipid metabolism features in domesticated salmon putatively linked to unintentional selection and adaptation to a typical domestic VO diet with low LC-PUFA levels
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