Effects of Rearing Environment and Strain Combination on Heterosis in Brook Trout

Three strains of brook trout Salvelinus fontinalis (domestic [D], Laval [L], and Rupert [R]) and their reciprocal hybrids were reared from 7 to 21 months of age in three different environments (indoor, constant temperature conditions; indoor, seasonal temperature variations; and outdoor, seasonal temperature variations) to test for the occurrence of heterosis in important life history traits of interest for production (body mass, length, condition factor, the absence of early sexual maturation, and survival). For each cross, body mass, length, and mortality were measured at regular intervals and sexual maturity was assessed in age-1+ fish (21 months of age). We found evidence for heterosis in mass and length that varied according to strain, cross direction in reciprocal hybrids, developmental stage, or environment; no significant outbreeding depression was detected for these traits. Heterosis expression for weight varied from 4.9% to 23.8% depending on the hybrids and environments. We found that one out of five reciprocal hybrids tested (L[female]R[male]) expressed heterosis at each age stage throughout the experiment in the three environments while the other four had mixed results. No evidence for heterosis was observed for sexual maturity and survival. These results not only provide one of the first clear pieces of evidence for the occurrence of heterosis in salmonids but also illustrate the complex nature and the unpredictability of this phenomenon. Heterosis, or hybrid vigor, refers to the increased performance and fitness of first generation progeny when compared with parental lines (Falconer and Mackay 1996; Birchler et al. 2003). The main explanation supporting the occurrence of heterosis is based on nonadditive genetic components: the dominance effect seen in hybrids, which is based on the replacement or complementation of deleterious alleles accumulated in one parental line by superior alleles from the other parent; overdominance, which suggests that heterozygotes perform better than homozygotes; and epistasis, which refers to allelic position and *Corresponding author: celine [email protected] Received October 22, 2010; accepted July 31, 2011 interactions in the hybrid (Birchler et al. 2003; Hochholdinger and Hoecker 2007; Lippman and Zamir 2007). The relative contribution of each of these processes in the expression of heterosis is still a matter of debate (Lippman and Zamir 2007). The intensity of heterosis is usually higher when parental lines are highly inbred or genetically distant from each other (Shikano et al. 2000; Wang and Xia 2002; Hochholdinger and Hoecker 2007). However, the opposite phenomenon that results from genome admixture—outbreeding depression—could also affect crosses involving genetically distant strains. 188 D ow nl oa de d by [ U ni ve rs ite L av al ] at 1 2: 34 0 6 A pr il 20 12 HETEROSIS IN BROOK TROUT 189 Outbreeding depression may arise from a disruption of the linkage arrangement of co-adapted gene complexes in the presence of a divergence in the genetic architecture of populations (based on epistasis components and referred to as intrinsic outbreeding depression) or from a loss of favorable allelic interactions (based on additive and dominance components and referred to as extrinsic outbreeding depression) (Edmands 2007; McClelland and Naish 2007; Tymchuk et al. 2007; Wang et al. 2007). When a cross is made, it is difficult to predict which phenomenon might appear since both heterosis and outbreeding depression result from outbreeding crosses between distant parental lines and are controlled, at least in part, by similar nonadditive effects. Breeding programs in plants and animals commonly use heterosis to improve traits of interest for production as an alternative to the use of additive genetic components (Falconer and Mackay 1996; Comings and MacMurray 2000; Hochholdinger and Hoecker 2007). While such practice has been more limited in fish production, it has been used to improve aquaculture in common carp Cyprinus carpio (Wohlfarth 1993; Hulata 1995; Nielsen et al. 2010) and Nile tilapia Oreochromis niloticus (Marengoni et al. 1998), and has also been experimentally explored in guppy Poecilia reticulata (Shikano and Taniguchi 2002a). Previous studies have also investigated heterosis for various traits, including growth, survival, salinity, and temperature tolerance (Moav and Wohlfarth 1976; Bentsen et al. 1998; Nakadate et al. 2003), and more recently for patterns of gene expression (Bougas et al. 2010). In salmonids, it is still unclear whether heterosis occurs. Heterosis for growth and survival in intraspecific hybrid crosses have been reported (Ayles and Baker 1983; Gjerde and Refstie 1984; Bryden et al. 2004) while other investigators only observed additive interactions for these same traits (Cheng et al. 1987; Einum and Fleming 1997; Glover et al. 2006) and even outbreeding depression (Gharrett et al. 1999). From these studies, it has been hypothesized that heterosis may be generally rare in salmonids (Gjerde and Refstie 1984; Gharrett et al. 1999; Bryden et al. 2004). More specifically, Tymchuk et al. (2007) suggested that salmonid populations may be too genetically distant and locally adapted to produce heterosis. However, in brook trout Salvelinus fontinalis in particular, previous studies on hybrid crosses between wild and domestic populations have suggested a potential for heterosis expression for growth and survival (Fraser 1981; Webster and Flick 1981) although it has not been investigated in detail. The choice of the strain used as dam or sire in the cross may also be determinant on heterosis expression (Bentsen et al. 1998). A strain can perform better when used as dam or sire, improving specific capacities in hybrids (Bentsen et al. 1998; Perry et al. 2004; X. X. Wang et al. 2006). The environment may also modify genetic expression and influence the additive and nonadditive genetic components. A decrease in the additive variance and an increase in the epistasis variance are usually expected under unfavorable environmental conditions (Wohlfarth 1993; Hoffmann and Merilä 1999). In addition, heterosis seems to be more sensitive to environmental variations than to additive components (Bentsen et al. 1998). Different strains could also express different sensitivities to environmental variations involving possible genotype–environment interactions relative to heterosis expression (Falconer and Mackay 1996; Bentsen et al. 1998). In this context, the aim of this study was to investigate the effects of rearing environment and strain combination on the occurrence of heterosis for growth in the brook trout. In teleost fishes, body mass and size at the juvenile stage can be considered as fitness-related traits since they are correlated with different components of fitness such as survival, life history tactic, or reproductive success (Sogard 1997; Wilson et al. 2003; Garcia de Leaniz et al. 2007; Thériault et al. 2007). Our specific objectives were therefore to evaluate (1) the occurrence of intraspecific heterosis on important life history traits that are also of interest for production (body mass, length, condition factor, absence of early sexual maturation, survival), (2) the presence of dam or sire effects on the hybrid performance and heterosis for the traits considered, and (3) the effects of environment on heterosis expression.