Domestication‐induced reduction in eye size revealed in multiple common garden experiments: The case of Atlantic salmon (Salmo salar L.)

Abstract

Domestication leads to changes in traits that are under directional selection in breeding programmes, though unintentional changes in nonproduction traits can also arise. In offspring of escaping fish and any hybrid progeny, such unintentionally altered traits may reduce fitness in the wild. Atlantic salmon breeding programmes were established in the early 1970s, resulting in genetic changes in multiple traits. However, the impact of domestication on eye size has not been studied. We measured body size corrected eye size in 4000 salmon from six common garden experiments conducted under artificial and natural conditions, in freshwater and saltwater environments, in two countries. Within these common gardens, offspring of domesticated and wild parents were crossed to produce 11 strains, with varying genetic backgrounds (wild, domesticated, F1 hybrids, F2 hybrids and backcrosses). Size‐adjusted eye size was influenced by both genetic and environmental factors. Domesticated fish reared under artificial conditions had smaller adjusted eye size when compared to wild fish reared under identical conditions, in both the freshwater and marine environments, and in both Irish and Norwegian experiments. However, in parr that had been introduced into a river environment shortly after hatching and sampled at the end of their first summer, differences in adjusted eye size observed among genetic groups were of a reduced magnitude and were nonsignificant in 2‐year‐old sea migrating smolts sampled in the river immediately prior to sea entry. Collectively, our findings could suggest that where natural selection is present, individuals with reduced eye size are maladapted and consequently have reduced fitness, building on our understanding of the mechanisms that underlie a well‐documented reduction in the fitness of the progeny of domesticated salmon, including hybrid progeny, in the wild.

Red and melanized focal changes in white skeletal muscle in Atlantic salmon (Salmo salar): Comparative analysis of farmed, wild and hybrid fish reared under identical conditions

“…In contrast, our study revealed significant differences in growth parameters between farmed and wild salmon, with the hybrids displaying intermediate characteristics. These results align with previous reports investigating wild, hybrid and farmed fish kept in common conditions (Glover et al, 2009; Perry et al, 2021; Thodesen et al, 1999). Specific growth rate (SGR) and body condition (κ factor) are commonly used metrics in salmonid aquaculture to assess growth and quality, respectively.…”

Investigating the role of genetic variation in vgll3 and six6 in the domestication of gilthead seabream (Sparus aurata Linnaeus) and European seabass (Dicentrarchus labrax Linnaeus)

“…Another gene found in this region is rpgr , which has been linked to the vision ability in domesticated chickens (Wang, Zhang, et al., 2016). Vision appears to be a feature affected by domestication in fishes, as evidenced by the smaller eye size observed in domesticated Atlantic salmon (Perry et al., 2021). Additionally, the six6 gene involved in eye development in vertebrates (Pritchard et al., 2018) is also relevant in this context.…”

Consequences of domestication in eastern oyster: Insights from whole genomic analyses

“…Adaptation to captivity is well documented in salmon, where a relatively homogeneous captive environment can increase the efficacy of selection pressures resulting from high population density, release from predation, and abundant nutritious food (Fleming & Einum, 1997 ; Wessel et al., 2006 ; Zhang et al., 2016 ). Salmon traits hypothesized to evolve in response to culture conditions include fast growth (Fleming et al., 2002 ), a reduced antipredator behavior (Jackson & Brown, 2011 ), and reduction in eye size (Perry et al., 2021 ). These domestication traits could be maladaptive under natural conditions (e.g., reduced eye size in the captive condition is a maladaptive trait selected against in the wild) (Perry et al., 2021 ).…”

“…Salmon traits hypothesized to evolve in response to culture conditions include fast growth (Fleming et al., 2002 ), a reduced antipredator behavior (Jackson & Brown, 2011 ), and reduction in eye size (Perry et al., 2021 ). These domestication traits could be maladaptive under natural conditions (e.g., reduced eye size in the captive condition is a maladaptive trait selected against in the wild) (Perry et al., 2021 ).…”