National Academies Press: OpenBook

Atlantic Salmon in Maine (2004)

Chapter: Appendix D: Supportive Breeding and Risks to Genetic Quality

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Suggested Citation:"Appendix D: Supportive Breeding and Risks to Genetic Quality." National Research Council. 2004. Atlantic Salmon in Maine. Washington, DC: The National Academies Press. doi: 10.17226/10892.
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Appendix D
Supportive Breeding and Risks to Genetic Quality

There are many genetic risks associated with the production of salmon through supportive breeding programs. One genetic risk of artificial propagation that has attracted widespread attention is the loss of genetic diversity (Hedrick 2001). Ryman and Laikre (1991), and the discussion above, show how supportive breeding may reduce effective population size (Ne < N) and therefore accelerate the loss of genetic diversity within wild populations. This loss may reduce the viability of individuals, for example through reduced heterozygosity, and it may also impact the potential evolution of new adaptations by populations over the long term. Concern over the short- and long-term impacts has led managers of supportive breeding programs to develop breeding protocols that retain maximum genetic diversity. Artificial pairing may include genotyping and calculation of “mean kinship” to determine breeding value (Ballou and Foose 1996). Or individuals are randomly bred, and emphasis is placed on equal contribution from each individual by equalization of family size (e.g., Rodriguez-Clark 1999, Wiese and Willis 1999). Although these protocols may achieve the objective of maintaining genetic diversity, they are not based on natural breeding systems.

The emphasis in current supportive breeding programs is the artificial pairing of genetically unrelated individuals. In nature, however, breeding is usually not random with respect to genetics (Andersson 1994). Supportive breeding, as currently practiced, limits or even works against both sexual selection and life history decisions that are necessary for the maintenance of genetic quality within populations (e.g., Fleming and

Suggested Citation:"Appendix D: Supportive Breeding and Risks to Genetic Quality." National Research Council. 2004. Atlantic Salmon in Maine. Washington, DC: The National Academies Press. doi: 10.17226/10892.
×

Gross 1993, Grahn et al 1998, Wedekind 2002). Sexual selection in natural breeding systems is known to expose heritable genetic quality, through male competition and condition-dependent characters, that is targeted by female choice and increases offspring viability (Møller and Alatalo 1999). Life history decisions that are made by certain individuals, such as precocious maturity by higher quality males, will also expose heritable genetic quality that is not captured in supportive breeding programs (Gross 1996). If potential mates differ in heritable genetic quality, maximizing genetic diversity through preventing reproductive skew is unlikely to be the best conservation strategy (Wedekind 2002).

In natural breeding systems, “genetic quality” may have three components that are targets of female mate choice: good genes, compatible genes, and diverse genes. Good genes refer to the superior fitness provided to a bearer by some genes relative to others in a population. These genes may be those most appropriate for particular pathogens or parasites (e.g., Hamilton and Zuk 1982) or for producing the enzymes that best process local prey items. Female mate choice for good genes is made possible by condition-dependent traits in males, such as body size or ornamentation that is preferred by females. For example, Reynolds and Gross (1992) showed that progeny fathered by preferred males had faster growth rates and earlier age of maturity in guppies. Moller and Alatalo (1999) reviewed a wide variety of organisms and found that males with larger condition dependent characters, favored by females, increased off-spring viability by 1.5% (even at early offspring stages in relatively benign laboratory environments). Wedekind et al. (2001) showed that female mate choice reduced pathogen-related egg mortality in whitefish, increasing egg survival by 12% relative to random mating.

Compatible genes refer to superior fitness provided to a bearer by the complementation of genes at individual loci as well as across loci. For instance, the deterioration in viability from inbreeding is often due to the expression of two deleterious alleles; compatible alleles at a locus would therefore include at least one nondeleterious allele. Female avoidance of matched deleterious alleles, through the avoidance of breeding with kin, is well known (Pusey and Wolf 1996). Female mate choice for compatible genes at the MHC locus (major histocompatibility complex) is also well known (Penn and Potts 1999). Females target opposite MHC carriers, and their heterozygote progeny have superior fitness due to disease and pathogen resistance (Carrington et al 1999). Finally, coadapted gene complexes, such as coordination of diverse body parts, is compatibility across loci and may underlie the avoidance of outbreeding in females of some species (Andersson 1994).

Wedekind (2002) discusses some advantages of incorporating mate preference into conservation breeding programs with whitefish. Since in-

Suggested Citation:"Appendix D: Supportive Breeding and Risks to Genetic Quality." National Research Council. 2004. Atlantic Salmon in Maine. Washington, DC: The National Academies Press. doi: 10.17226/10892.
×

dividuals differ in their heritable viability, minimizing reproductive skew and thereby maximizing Ne might not be the best conservation strategy, since it disrupts the correlation between viability traits and reproductive success. Resistance to a virulent egg parasite is influence by both maternal and paternal effects. Random breeding and equalization would reduce reproductive skew, increasing genetic variation in freshly fertilized eggs, but both this genetic variation and egg number may later be reduced by directed selection from the egg pathogens. Alternatively, allowing preferential breeding by preferred males would decrease genetic variation in freshly fertilized eggs but increase mean survival of offspring. In some cases, preferential breeding would sufficiently reduce the effects of selection by pathogens and result in higher overall Ne. Random breeding and equalization could even increase the size of the pathogen population, further threatening population viability. This suggests that the supportive breeding program needs to find a breeding protocol that incorporates the heritable fitness benefits that come with natural mate choice.

Another example of the importance of incorporating natural breeding systems is seen in the life history decisions of precocious maturity in male salmon (Gross 1985). There is good theoretical reason to believe that precocious males (“jacks” or “precociously mature parr”) are those that have the best quality genes in the population and thus derive the highest fitness (Gross and Repka 1998a,b). This increased fitness results in the spread and maintenance of the high quality genes in the population. In current conservation genetics breeding protocols, these males would receive no more breeding advantage than the less fit delayed-maturity males (“hooknose” or “adult” males). This stalls the movement of high-quality genes into the population by unfairly increasing the relative fitness of poorquality genes.

In summary, supportive breeding programs that focus on maximizing genetic diversity are unlikely to maintain long-term genetic quality in wild populations. Studies of natural breeding systems reveal that genetic quality consists of good genes, compatible genes, and appropriate rather than random genetic diversity. The domestication of wildlife for agricultural consumption by human breeding protocols has only demonstrated that we can produce organisms with high fitness in artificial environments. We do not have equivalent evidence for the capacity of conservation breeding programs to produce organisms that are adapted for their natural environments. Until evolutionary and conservation genetics has matured in its understanding of genetic quality, the use of supplementation and the potential for genetic interactions between hatchery and wild fish should be viewed as further threats to population viability.

Suggested Citation:"Appendix D: Supportive Breeding and Risks to Genetic Quality." National Research Council. 2004. Atlantic Salmon in Maine. Washington, DC: The National Academies Press. doi: 10.17226/10892.
×
Page 258
Suggested Citation:"Appendix D: Supportive Breeding and Risks to Genetic Quality." National Research Council. 2004. Atlantic Salmon in Maine. Washington, DC: The National Academies Press. doi: 10.17226/10892.
×
Page 259
Suggested Citation:"Appendix D: Supportive Breeding and Risks to Genetic Quality." National Research Council. 2004. Atlantic Salmon in Maine. Washington, DC: The National Academies Press. doi: 10.17226/10892.
×
Page 260
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Because of the pervasive and substantial decline of Atlantic salmon populations in Maine over the past 150 years, and because they are close to extinction, a comprehensive statewide action should be taken now to ensure their survival. The populations of Atlantic salmon have declined drastically, from an estimated half million adult salmon returning to U.S. rivers each year in the early 1800s to perhaps as few as 1,000 in 2001. The report recommends implementing a formalized decision-making approach to establish priorities, evaluate options and coordinate plans for conserving and restoring the salmon.

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