Resistance to three pathogens in the endangered winter-run chinook salmon (Oncorhynchus tshawytscha): effects of inbreeding and major histocompatibility complex genotypes

Abstract

We have carried out the first major infectivity trial to examine differential genetic resistance in fish for pathogens. We used captive-bred, endangered winter-run chinook salmon (Oncorhynchus tshawytscha) to determine resistance to three pathogens: the bacterium, Listonella (Vibrio) anguillarum, infectious hematopoietic necrosis virus (IHNV), and Myxobolus cerebralis, the parasite that causes whirling disease. We compared resistance to these three pathogens between inbred and outbred salmon and between siblings that were heterozygous or homozygous for a class II gene in the major histocompatibility complex (MHC). In two of five different comparisons, we found significant genetic effects on disease resistance. First, MHC heterozygotes had a higher survival than MHC homozygotes when exposed to IHNV and the selection disadvantage of homozygotes was estimated to be 8.5%. Second, outbred fish had a higher resistance (or lower infection severity) than inbred fish when exposed to M. cerebralis. Using a quantitative genetics approach, it appears that there are slightly more than three gene equivalents segregating that would result in no resistance to M. cerebralis when homozygous. Overall, our investigation suggests that pathogen susceptibility in the winter-run chinook salmon will increase if further genetic variation is lost in this endangered species.

Terminal Investment Induced by Immune Challenge and Fitness Traits Associated With Major Histocompatibility Complex in the House Sparrow

“…In theory, the optimal number of Mhc alleles is predicted to be determined by the trade-off between two opposing selective forces. The first maximizes the number of alleles to permit the recognition of the largest antigenic peptide repertoire (Arkush et al 2002;Penn et al 2002;). In contrast, the number of alleles is limited to minimize the loss of T-cell clones due to selftolerance induction (thymic negative selection, Nowak et al 1992).…”

“…In contrast, the number of alleles is limited to minimize the loss of T-cell clones due to selftolerance induction (thymic negative selection, Nowak et al 1992). Heterozygocity has been found to be advantageous in multiple-strain infections (Arkush et al 2002;Penn et al 2002) and associated with higher fitness (Sauermann et al 2001). Recent experimental studies have also provided evidence of an advantage associated to the existence of an optimal, rather than a maximal, number of Mhc alleles (Wegner et al 2003;Kurtz et al 2004).…”

The evolutionary ecology of the major histocompatibility complex

“…MHC heterozygosity (Arkush et al, 2002) and specific MHC alleles (Miller et al, 2004) have also been associated with resistance to infectious hematopoietic necrosis virus (IHNV) in Chinook salmon (Oncorhynchus tshawytscha) and Atlantic salmon (S. salar), respectively.…”

“…Indeed, levels of MHC diversity in populations are increasingly being used in a conservation context to identify those populations that are relatively depaurperate in diversity. MHC variation is viewed as being a better marker for conservation not because it is a better proxy than any neutral marker for determining genome wide diversity, but because it is intimately associated with factors likely to impinge on individual fitness, population viability and evolutionary potential in a changing environment (Edwards and Potts, 1996;Hedrick, 1999;Arkush et al, 2002;Aguilar et al, 2004;Hedrick, 2004b;Seddon and Ellegren, 2004).…”

Sexual selection for genetic compatibility: the role of the major histocompatibility complex on cryptic female choice in Chinook salmon (Oncorhynchus tshawytscha)

“…This hypothesis was inferred from observations in mice (McClelland et al, 2003;Froeschke and Sommer, 2005) and fish Arkush et al, 2002;Kekäläinen et al, 2009), in which individuals heterozygous at the MHC had higher survival rates and lower parasite loads than homozygotes. It is thought that the different MHC alleles in heterozygous individuals likely enable immunity against a wider range of pathogens (Agbali et al, 2010).…”