Most organisms are infected by a multitude of parasites species [1
]. The associated fitness costs for hosts are often profound [2
], rendering the host-parasite relationship as one of the most intense ecological interactions. The selection pressure on the host to overcome infection might result in an evolutionary arms race between parasite and host. One consequence of such host-parasite co-evolution is the maintenance of genetic diversity in defense genes resulting in marked fitness differences among host genotypes [3
]. The identification of variable genetic loci that determine specific resistance and thereby enhance host fitness is of prime importance in ecological and evolutionary research [5
]. The most striking example of genetic polymorphism that is maintained by parasites is the vertebrate major histocompatibility complex (MHC). MHC molecules activate T-cells by presenting parasite-derived peptides, if the host's individual collection of MHC molecules includes those that can bind to a peptide of the actual infectious agent. Otherwise the infection escapes a T cell response. This suggests that pathogens are the ultimate cause driving MHC diversification [6
] and several studies found associations between resistance and presence of single MHC alleles or MHC haplotypes (reviewed in [7
This applies to three-spined sticklebacks Gasterosteus aculeatus
L. MHC class II loci that were shown to influence parasite load [12
] and female mate choice [15
]. Interestingly, these studies, along with findings from sparrows [17
], turkeys [18
] and pythons [19
] demonstrate that an intermediate number of MHC sequence variants may be favored by selection, as has been predicted by an optimality model [20
]. The crucial evidence that is missing thus far is the link between an intermediate number of MHC alleles and maximal Darwinian fitness, under natural, yet still controlled settings. Hence, we wanted to combine advantages of a field study with the knowledge from earlier experimental studies [13
] by using enclosures in the field. Enclosures were stocked with 14 lab reared, parasite free fish families.
Based on previous laboratory studies [13
], we predicted that genotypes with an intermediate number of MHC class IIB sequence variants are least infected under more natural field conditions and thus may have higher survival rates. Such a result would reveal the still missing direct link between the number of MHC sequence variants and fitness under almost natural conditions.
Recent studies suggested that a habitat specific MHC genotype cannot fully account for local adaptation to the sympatrically prevalent parasite fauna. The family specific genetic background still explained a large proportion of parasite load [21
]. Since parasite load is dependent on individual MHC diversity in sticklebacks [13
] a true genetic family background effect can best be assessed in families that lack variation in individual MHC diversity. Therefore, we wanted to test the relative importance of MHC genotypes compared to other genetic components by using two kinds of families: one group of families with variable MHC genotypes of the same kind used in previous studies (i.e. segregating families [22
] and one where families only showed a single MHC genotype (non-segregating families). The latter kind results from a cross of parents, which are homozygous at their MHC loci, while segregation of MHC genotypes results from at least some loci being heterozygous. A comparison of both types of families can separate effects attributable to variation in individual MHC diversity in segregating families from effects only dependent on the family genetic background in non-segregating families. If individual MHC diversity is responsible for determining parasite load within-family variation as well as among family variation should be larger for segregating families.
It has been shown recently that the expression of virulence in coupled genetic interactions between hosts and parasites depend on abiotic factors like temperature [24
]. The strength of selection on MHC diversification might be amplified by additional environmental stress [28
]. In which direction expression of virulence is modified is however hard to predict [26
]. Hence, phenomena associated with global climate change such as heat waves or precipitation extremes will alter the impact of parasitism, ultimately selecting for increased genetic variability at immune defense loci such as the MHC. On a larger geographic scale MHC diversity was already shown to covary with temperature and bacterial diversity in the water body among Canadian populations of salmon [29
]. Our study conducted in 2003 coincided with a period of exceptionally high temperature in central and northern Europe that may be viewed as precursor of future climate extremes [30
]. High water temperatures led to substantial mortality in our experimental population. We explore here whether parasitism was a likely cause of mortality selection, and whether this is linked to MHC diversity on a local scale as well.