Mats Grahn

Good genes, oxidative stress and condition-dependent sexual signals

The immune and the detoxication systems of animals are characterized by allelic polymorphisms, which underlie individual differences in ability to combat assaults from pathogens and toxic compounds. Previous studies have shown that females may improve offspring survival by selecting mates on the basis of sexual ornaments and signals that honestly reveal health. In many cases the expression of these ornaments appears to be particularly sensitive to oxidative stress. Activated immune and detoxication systems often generate oxidative stress by an extensive production of reactive metabolites and free radicals. Given that tolerance or resistance to toxic compounds and pathogens can be inherited, female choice should promote the evolution of male ornaments that reliably reveal the status of the bearers level of oxidative stress. Hence, oxidative stress may be one important agent linking the expression of sexual ornaments to genetic variation in fitness–related traits, thus promoting the evolution of female mate choice and male sexual ornamentation, a controversial issue in evolutionary biology ever since Darwin.

On the adaptive significance of stress-induced immunosuppression

We approach the field of stress immunology from an ecological point of view and ask: why should a heavy physical workload, for example as a result of a high reproductive effort, compromise immune function? We argue that immunosuppression by neuroendocrine mechanisms, such as stress hormones, during heavy physical workload is adaptive, and consider two different ultimate explanations of such immunosuppression. First, several authors have suggested that the immune system is suppressed to reallocate resources to other metabolic demands. In our view, this hypothesis assumes that considerable amounts of energy or nutrients can be saved by suppressing the immune system; however, this assumption requires further investigation. Second, we suggest an alternative explanation based on the idea that the immune system is tightly regulated by neuroendocrine mechanisms to avoid hyperactivation and ensuing autoimmune responses. We hypothesize that the risk of autoimmune responses increases during heavy physical workload and that the immune system is suppressed to counteract this.

Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon

We have tested the importance of genetic variation in the major histocompatibility complex (MHC) class IIB in Atlantic salmon (Salmo salar) for survival after challenge with a highly virulent bacterial pathogen. Forty juvenile full siblings from each of 120 families were infected with the bacterium Aeromonas salmonicida, which causes high mortality in salmon due to furunculosis. Fishes from high–resistance (HR, < 35% mortality) and low–resistance (LR, > 80% mortality) families were screened for their MHC class IIB genotypes using the denaturing gradient gel electrophoresis (DGGE) technique. The exon 2 sequences, encoding the major part of the peptide–binding region, were established for each DGGE fragment. One allele, e, containing a missense single base substitution was significantly more prevalent in HR families than in LR families. An odds–ratio test showed that broods carrying this allele had a 12–fold higher chance of being HR than broods without the e allele. A second allele, i, showed significantly higher frequencies in uninfected and surviving individuals than in infected dead individuals. A third allele, j, tended to be more prevalent both in LR families and in individuals that had died of the infection. There was no correlation between MHC heterozygosity and resistance to A. salmonicida. Our results support the hypothesis that MHC polymorphism is maintained through pathogen–driven selection acting by means of frequency–dependent selection rather than heterozygous advantage.

MHC and kin discrimination in juvenile Arctic charr, Salvelinus alpinus (L.)

Kin recognition and discrimination are thought to occur in several species of various taxonomic groups. In salmonid fish, juveniles can discriminate between odours of siblings and nonsiblings from the same population even if the odour donors and the test fish have been reared separately since fertilization. This indicates that some genetic factor is important in the recognition process. The mechanisms behind kin recognition and discrimination have not yet been described. In the present study, we performed fluviarium tests to examine whether kin recognition and discrimination in juvenile Arctic charr are influenced by the major histocompatibility complex (MHC). Prior to the fluviarium tests, exon 2 of an MHC class II B gene in charr was analysed with denaturing gradient gel electrophoresis (DGGE) and individual genotypes were determined. In the fluviarium, when fish had the choice between water scented by an MHC identical sibling and a sibling with a different MHC genotype they preferred water from identical siblings. Moreover, water scented by an MHC different sibling was preferred to water from an MHC different nonsibling. However, we observed no discrimination when the test fish shared one allele with the nonsibling donor but no alleles with the sibling donor. Our results indicate that the MHC has a significant influence on the odours used for kin recognition and discrimination in juvenile Arctic charr.Copyright 1998 The Association for the Study of Animal Behaviour

MHC genotype and male ornamentation: Genetic evidence for the Hamilton-Zuk model

The major histocompatibility complex (MHC) is an immunologically important cluster of highly variable genes that is known to affect fitness in domesticated mammals and birds. Spur length of male pheasants in southern Sweden correlates with male viability, female mate choice, and offspring survival rate. Here we show by genetic analyses that the MHC genotype is associated with variation in both male spur length and male viability. These are the first data that directly support a ‘good genes’ hypothesis by Hamilton and Zuk predicting that females discriminate among males on the basis of secondary sexual characters in order to pass on genes for disease resistance that improve fitness in their offspring.

Spatial pattern of MHC class II variation in the great snipe (Gallinago media)

The genes of the major histocompatibility complex (MHC) code for proteins involved in antigen recognition and triggering of the adaptive immune response, and are therefore likely to be under selection from parasites. These selection regimes may vary in space and time. Here we report a strong geographical structure in MHC class II B genes of a migrating bird, the great snipe (Gallinago media). Genetic differentiation in the MHC between two ecologically distinct distributional regions (Scandinavian mountain populations vs. East European lowland populations) was still present after statistically controlling for the effect of selectively neutral variation (microsatellites) using partial Mantel tests. This suggests a role for selection in generating this spatial structure and that it represents local adaptation to different environments. Differentiation between populations within the two regions was negligible. Overall, we found a high number of MHC alleles (50, from 175 individuals). This, together with a tendency for a higher rate of nonsynonymous than synonymous substitutions in the peptide binding sites, and high Tajimas D in certain regions of the gene, suggests a history of balancing selection. MHC variation is often thought to be maintained by some form of balancing selection, but the nature of this selection remains unclear. Our results support the hypothesis that spatial variation in selection regimes contributes to the high polymorphism.

Experimental evidence for major histocompatibility complex-allele-specific resistance to a bacterial infection

The extreme polymorphism found at some major histocompatibility complex (MHC) loci is believed to be maintained by balancing selection caused by infectious pathogens. Experimental support for this is inconclusive. We have studied the interaction between certain MHC alleles and the bacterium Aeromonas salmonicida, which causes the severe disease furunculosis, in Atlantic salmon (Salmo salar L.). We designed full–sibling broods consisting of combinations of homozygote and heterozygote genotypes with respect to resistance or susceptibility alleles. The juveniles were experimentally infected with A. salmonicida and their individual survival was monitored. By comparing full siblings carrying different MHC genotypes the effects on survival due to other segregating genes were minimized. We show that a pathogen has the potential to cause very intense selection pressure on particular MHC alleles; the relative fitness difference between individuals carrying different MHC alleles was as high as 0.5. A co–dominant pattern of disease resistance/susceptibility was found, indicative of qualitative difference in the immune response between individuals carrying the high– and low–resistance alleles. Rather unexpectedly, survival was not higher among heterozygous individuals as compared with homozygous ones.

Influence of genetic dissimilarity in the reproductive success and mate choice of brown trout – females fishing for optimal MHC dissimilarity

We examined the reproductive success of 48 adult brown trout (Salmo trutta L.) which were allowed to reproduce in a stream that was controlled for the absence of other trout. Parentage analyses based on 11 microsatellites permitted us to infer reproductive success and mate choice preferences in situ. We found that pairs with intermediate major histocompatibility complex (MHC) dissimilarity mated more often than expected by chance. It appears that female choice was the driving force behind this observation because, compared with other individuals, males with intermediate MHC dissimilarity produced a larger proportion of offspring, whereas female reproductive output did not show this pattern. Hence, rather than seeking mates with maximal MHC dissimilarity, as found in several species, brown trout seemed to prefer mates of intermediate MHC difference, thus supporting an optimality‐based model for MHC‐dependent mate choice.

Major histocompatibility complex variation and mate choice in a lekking bird, the great snipe (Gallinago media)

Genes of the major histocompatibility complex (MHC) play a major part in the activation of the vertebrate immune system. In addition, they also appear to function as cues for mate choice. In mammals especially, several kinds of MHC‐dependent mate choice have been hypothesized and observed. These include choice of mates that share no or few alleles with the choosing individual, choice of mates with alleles that differ as much as possible from the choosing individual, choice of heterozygous mates, choice of certain genotypes and choice of rare alleles. We investigated these different aspects of mate choice in relation to MHC in a lekking bird species, the great snipe (Gallinago media). We found no evidence for MHC disassortative mating, no preference for males with many MHC alleles and no preference for rare alleles. However, we did find that some allelic lineages were more often found in males with mating success than in males without mating success. Females do not seem to use themselves as references for the MHC‐dependent mate choice, rather they seem to prefer males with certain allele types. We speculate that these alleles may be linked to resistance to common parasites.

Genetic, morphological, and feather isotope variation of migratory willow warblers show gradual divergence in a ring

The circular distribution of the willow warbler Phylloscopus trochilus around the Baltic Sea shares many features with the classic examples of ring species; however, the system is much younger. It has previously been shown that a secondary contact zone is located in central Scandinavia, where there are narrow clines for several morphological traits coincident with a migratory divide. Here we analyse multiple traits and genes from > 1700 males captured on breeding territories at 77 sites spread around the Baltic Sea to test the following hypothesis. If the secondary contact zone in Scandinavia is a result of divergence in two allopatric refuge populations during the last glaciation, we expect to find a similar secondary contact zone somewhere else around the circular distribution. Our results show that the trait clines were wider and displaced from each other along the eastern side of the Baltic Sea. Analyses of 12 microsatellite loci confirmed that the genome is very similar between the terminal forms (FST = 0). Two AFLP‐derived markers filtered out from a genomic scan instead appear to be maintained by selection. These markers exhibited steep clines at the secondary contact zone in Scandinavia, but as for the phenotypic traits, had vastly different cline centres east of the Baltic Sea. The trait clines along the ring distribution outside the Scandinavian secondary contact zone thus seem to have been shaped by independent action of selection or drift during the process of postglacial colonization.