A Scientific Review of the Potential Environmental Effects of Aquaculture in Aquatic Ecosystems - Volume 4

The Role of Genotype and Environment in Phenotypic Differentiation among Wild and Cultured Salmonids

Wendy E. Tymchuk
Centre for Aquaculture and Environmental Research, Fisheries & Oceans Canada, 4160 Marine Drive, West Vancouver, BC, Canada V7V 1N6

Robert H. Devlin
Department of Zoology University of British Columbia, Vancouver, BC, Canada V6T 1Z4

Ruth E. Withler
Fisheries & Oceans Canada, 4160 Hammond Bay Road, Nanaimo, BC, Canada V9T 6N7

Executive Summary

This paper reviews the existing literature examining genetic influences on and consequences of the interaction between cultured and wild salmonids. The paper identifies major phenotypic changes that have occurred in domestic strains (e.g. morphology, physiology, and behavior), and examines whether these changes have effects on fitness in laboratory and natural environments. Long-term effects of interactions between domestic and wild strains will primarily arise from genetic effects, but the phenotype of domestic strains relative to wild strains arises from both genetic and environmental forces. Separating these causal components of phenotype is required to understand the potential effects of introgression events, yet achieving this goal remains a difficult task. Studies in the wild are required to fully determine the fitness of domestic and wild strains and thus examine potential long-term consequences arising from their interaction.

Genotype, in addition to environment, determines the adaptive phenotypic characteristics (i.e. reproductive capabilities and ongoing survival) of salmonids, and, as such, it is likely that disruption of this genetic structure may have short-term and long-term effects on individual fitness as well as the future resilience of populations to natural and anthropogenic pressures. Domestication has been noted to have a significant effect on life history traits in salmonids (Thorpe 2004). Domestication may select for many different traits, including improved growth rates, earlier age at maturity and spawning, greater survival, increased tolerance to high temperature and resistance to disease (Hynes et al. 1981). Differences between wild and cultured fish represent a phenotypic continuum, ranging from differences among natural strains, to differences between wild and sea-ranched fish, to differences between wild and highly selected domestic cultured fish (Figure 1). Alterations in fitness-related traits in hatchery fish should be typical of differences expected in aquacultured salmon, although the latter may show a greater magnitude of change due to an increased length of time under intentional and indirect selection, which is usually conducted in isolation from wild genetic pools. Accumulated evidence now indicates that some fitness-related traits affected by domestication, such as growth, competitive ability, and anti-predator behavior, are in part genetically controlled. Transgenic fish, which can be viewed as an extreme form of domestication, are not considered in the present discussion except when examined as a model system for assessment of genotype/phenotype relationships (Devlin et al. 2001).

Figure 1. Representation of the relationships among phenotypic states for one hypothetical set of wild, hatchery, domestic, and transgenic strains. The ranges of phenotype observed among different wild populations are anticipated to overlap considerably with each other and with hatchery strains derived from them. Domestic strains that have undergone directed and unintentional selection are expected to possess phenotypes different from wild and hatchery populations, often in a common direction away from the wild phenotype, and in some cases to an extent seen for transgenic strains. Transgenic strains can possess a wide range of phenotypic transformations for novel traits, and for existing traits previously possessed by the host strain, or may have no change in phenotype from the host strain.

Phenotypic differences between cultured and wild fish

Rearing fish in a culture environment can lead to environmentally determined differences in morphology relative to those reared in the wild. The extent of these differences depends on the type and the length of time spent within the artificial environment, and the intensity of the culture conditions such as crowding, food supply, etc. Multiple generations of strains kept within the culture environment may lead to genetically based morphological differences arising from selection for traits affording fitness benefits in culture.

Domestication has also been shown to alter the physiology of fish. Environmental factors such as availability of food resources and temperature will of course have an effect on growth of fish. However, there can also be large differences in growth between cultured and wild strains as a result of genetic differences between the strains. The magnitude of the growth differences caused by genotype will be dependent on the purpose and history of the cultured strain. Aquacultured strains that have been intensely selected for enhanced growth show a larger shift in growth phenotype from the founding line compared with those strains that have not experienced directed selection. It is important to note that it is often not clear whether physiological differences are a cause or consequence of other phenotypic differences between the strains (such as growth or behavior differences). It is therefore difficult to clarify whether physiological differences have a genetic basis per se, or if they are a product of the environment.

Behavioral differences commonly arise during domestication. Cultured and wild fish do show differences in the level of aggression displayed towards conspecifics, although there has not been a consistent trend as to whether aggression increases or decreases under culture. A common assertion is that aggression will decrease under culture when fish are reared in crowded conditions and do not have to fight for limited food resources. A genetically determined reduced response to predators seems to be a consistent trend in domestic strains across several species. In contrast, little research has been conducted to reveal genetic control of foraging strategy, habitat selection, and dispersal. A genetic basis for altered foraging strategy could arise from phenotypic expression of other genetically influenced traits such as growth or morphology, which would drive foraging behavior characteristics.

Expression of physiological and behavioral phenotypes will ultimately determine survival. Survival is influenced by most other phenotypic traits, and the environment in which they are expressed. Cultured fish, either through a plastic response to their environment or through an adaptive response to altered selection pressures, tend to express phenotypic characteristics best suited for the culture environment. Consequently, they tend to have a lower survival than wild fish in a natural environment. However, few studies have examined whether cultured fish that experience a natural environment throughout their life history will still show decreased survival relative to the wild fish. Furthermore, the strength of the genetic basis of survival is not known, nor is it clear whether cultured fish still have the ability to show a phenotypically plastic response to the environment that will maximize their ability to survive.

Reproductive capabilities of domesticated fish are often affected. The literature consistently observes that cultured fish often have the physiological ability to spawn, but that altered spawning behavior limits their success. While the reproductive success of farmed fish may be low, the potential for significant gene flow still exists because the population of farmed fish often outnumbers the population of resident wild fish (at least in the case for Atlantic salmon), at times by as much as 3:1 (Lund et al. 1994; Lura and Økland 1994). There are no data comparing the ability of farmed and wild Pacific salmon to spawn in nature, but comparisons between hatchery and wild coho salmon, and studies examining cultured wild strains indicate that trends observed for Atlantic salmon may be typical of the phenotypic changes expected during domestication.

Genetic effects of farmed fish on wild populations would depend in part on the reproductive behavior of farmed fish in the wild. Evidence suggests that farmed fish have the ability to breed successfully in the wild, although contradicting results exist. There are generally significant differences in breeding potential between cultured and wild fish (Fleming and Gross 1992, 1993; Fleming et al. 1996; Berejikian et al. 1997; Bessey et al. 2004), although other studies have found similar reproductive success for hatchery and native fish in the wild (Dannewitz et al. 2004; Palm et al. 2003). Morphology and life history traits related to reproductive behavior respond evolutionarily to altered selection regime in the hatchery environment (Fleming 1994; Fleming and Gross 1989). The genetic effect of aquacultured salmon on wild populations will depend not only on the size of the wild population, but also on variation in breeding success (Fleming and Petersson 2001).

Cause of phenotypic differentiation between cultured and wild strains

Phenotypic differences between farmed and wild salmonids may arise from a combination of genetic and environmental effects, but in most cases, the origin of the difference is not well defined. Environmentally based phenotypic differences would not be passed to offspring as they do not have a genetic basis, and are thus anticipated to have single generation effects arising directly from escaped fish. In contrast, genetic differences have the potential to affect the wild populations of a species over a longer time frame. Thus, it is therefore critical to separate the influence of genotype and environment.

To assess genetic effects, experiments must be performed by rearing fish of different origins in a common environment (i.e. common-garden experiments.). Such experiments can help determine whether cultured fish have an altered genotype that has arisen in response to selection pressures from an artificial environment. Environmental effects (i.e. phenotypic plasticity) can be tested by rearing fish of a common genetic background in different environments, revealing whether phenotypic plasticity (Hutchings 2004) may have altered phenotype in response to the environmental conditions.

Currently, there is still limited knowledge on how the environment will act on inherent genetic differences among strains (i.e. will environmental conditions affect different genotypes in distinct ways through genotype x environment interactions). For example, fast-growing domestic fish may have a greater growth advantage relative to wild fish under culture conditions than they do in nature. An understanding of genotype by environment interactions remains one of the most critical components influencing phenotype and fitness. Research in this area is required to improve prediction of genetic effects arising from interaction between wild and cultured fish.

Mechanism of genetic interaction

Genetic effects of domestic fish may be direct or indirect. Direct genetic effects include the alteration of the wild genome (introgression) as a result of interbreeding between wild and domesticated fish, or the production of sterile hybrids. Indirect effects include the effect of reduced effective population size or altered selection pressure arising from competition or the introduction of pathogens (Krueger and May 1991; Skaala et al. 1990; Waples 1991). Genetic effects of hybridization between farmed and wild salmon are somewhat unpredictable and may differ between populations, but most interactions have been generally found to be disadvantageous when the genetic effects alter fitness-related traits (Hindar et al. 1991). Most studies have focused on the fitness of the F1 generation when exploring the effects of interbreeding between domestic and wild strains. While such hybrids may have enhanced fitness due to hybrid vigor, the negative effects of outbreeding depression are not manifested until F2 and later generations, and thus simple first-generation hybrid studies have limited predictive value.

The genetic effect of escaped cultured fish on wild populations will also depend on the demographic of the wild population, the magnitude and frequency of the escape, and the extent of introgression of aquacultured genotypes into the wild population (Hutchings 1991). The phenotype of wild and farmed hybrids may vary depending on the source and genetic structure of the wild population (e.g., see Einum and Fleming 1997). Anadromous populations of salmonids may be somewhat resistant to introgression due to aspects of their complex life histories such as overlapping maturation age classes and straying among distinct populations (Utter and Epifanio 2002). Furthermore, genetic distance between the two populations does not seem to be a reliable indicator of the potential effects of introgression (Utter and Epifanio 2002).

Knowledge Gaps and Recommendations

More fully define the genetic basis of domestic traits and the mechanisms by which they alter phenotype.

It is clear that phenotypic differences (particularly growth) between cultured and wild fish are due in part to altered genotype. However, the specific genetic changes that have occurred to cause these phenotypic differences are not yet understood. For example, traits that are controlled by many alleles of small effect will present different risks to wild populations and will require different management strategies relative to traits that are caused by a small number of alleles of large effect. A better understanding of the genetic changes underlying desired traits will also aid in the development of custom aquaculture strains through the use of marker-assisted selection. Such genetic information may be obtained from:

1. additional breeding studies (e.g. assessing heteritabilities for critical traits in wild and cultured populations under culture and natural conditions, and the scale to which outbreeding depression and/or heterosis are at play among populations);
2. experiments mapping and identifying genes and alleles responsible for specific phenotypes;
3. and, gene expression studies identifying candidate genes involved in fitness-related processes.

Determine whether conserved genetic and physiological pathways are employed among domestic strains to achieve alteration of specific trait.

Further to the above, it will be crucial to assess whether genetic changes arising through the process of domestication are a conservative process. There has been little comparison among strains and species of cultured fish to determine if the genetic alterations leading to phenotypic differences occur in predictable patterns, or if each strain is developed through a unique set of alleles. This information will determine whether a general risk management strategy could be generalized, or if plans must be developed on a case-by-case basis.

Extensive research is required to determine which environmental variables play controlling roles in influencing the magnitudes of phenotypic differences among wild and between wild and domestic strains (i.e. improve our knowledge of phenotypic plasticity and genotype x environment interactions).

Because of the difficulty of making observations in natural environments, there are few studies that test whether differences among strains observed in an artificial environment are an accurate predictor of the characteristics that will be displayed in the natural environment. Thus, there is a need for more rigorous assessments of the plasticity of cultured and wild strains to assess whether domestic genotypes have response to environmental conditions which differ from wild type in non-parallel ways (i.e. genotype x environment interactions). This area of research is critical.

Undertake experiments to evaluate the contribution of phenotypic differences between domestic and wild strains to survival and reproductive fitness.

Altering the expression of a phenotypic trait can alter overall fitness. Different phenotypic traits will interact in a complex manner to determine the fitness of an individual. While there is much literature on discrete phenotypic differences among cultured and wild strains, there is a need for more complex analyses of how these differences interact during the life history of the fish and consequently influence their ability to survive and reproduce.

Fitness evaluations must be undertaken in nature to provide information to reliably predict net fitness and consequences of domestic genotypes introgressed into wild populations. Without data from nature, laboratory experiments may reveal forces causing phenotypic and fitness differences, but their true magnitudes cannot be known with certainty.

It is critical to extend laboratory studies and assess identified genetic differences such that true determinations of their influence on fitness in nature can be determined. It will also be important to examine the ability and the rate that populations may be able to revert to naturally selected genotypes and phenotypes following introgression events.

Given current uncertainty in our ability to a priori predict consequences of introgression, research directed to monitoring and minimizing interactions should be supported.

The outcome of genetic interaction between farmed and wild populations is difficult to predict as our understanding of genetic dynamics is poorly developed for age-structured populations with overlapping generations such as those shown by salmonid populations. Consequently, conservative approaches have been recommended when assessing genetic effect risks (Ryman 1997; Waples 1991). Clearly, an important first step is to minimize escape of cultured fish into the wild (Altukhov and Salmenkhova 1990; Krueger and May 1991). Effort should also be directed at developing molecular techniques to better identify and monitor introgression of cultured strains into wild populations, particularly for reproductively mature stages and consequent early stages of their progeny. The use of triploid fish or other containment techniques in aquaculture may eliminate genetic effects, and reduce the ecological consequences of escaped farmed fish on wild stocks (Cotter et al. 2000; Devlin and Donaldson 1992).

Develop models that make use of the emerging understanding of the relationship between genotype, phenotype and fitness to allow prediction of the consequences of introgression of domestic and wild strain.

Recent research has revealed that many phenotypic traits that differ between wild and domestic strains are controlled by additive genetic variation (Tymchuk et al. 2006, McGinnity et al. 1997, 2003, Fleming et al. 2000). These observations could now allow estimation of the effects of introgression on the genotype of wild populations, assuming neutral fitness. Further, modeling exercises can allow sensitivity analysis to estimate risk arising from different genotypes under various introgression scenarios, and, coupled with studies of natural fitness among genotypes, may be used in the future to predict consequences in the wild.

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