Claus Wedekind

MHC-dependent mate preferences in humans

One substantial benefit of sexual reproduction could be that it allows animals (including humans) to react rapidly to a continuously changing environmental selection pressure such as coevolving parasites. This counteraction would be most efficient if the females were able to provide their progeny with certain allele combinations for loci which may be crucial in the parasite-host arms race, for example the MHC (major histocompatibility complex). Here we show that the MHC influences both body odours and body odour preferences in humans, and that the women’s preferences depend on their hormonal status. Female and male students were typed for their HLA-A, -B and -DR. Each male student wore a T-shirt for two consecutive nights. The next day, each female student was asked to rate the odours of six T-shirts. They scored male body odours as more pleasant when they differed from the men in their MHC than when they were more similar. This difference in odour assessment was reversed when the women rating the odours were taking oral contraceptives. Furthermore, the odours of MHC-dissimilar men remind the test women more often of their own actual or former mates than do the odours of MHC-similar men. This suggests that the MHC or linked genes influence human mate choice today.

Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity?

The major histocompatibility complex (MHC) is an immunologically important group of genes that appears to be under natural as well as sexual selection. Several hypotheses suggest that certain MHC–allele combinations (usually heterozygous ones) are superior under selective pressure by pathogens. This could influence mate choice in a way that preferences function to create MHC–heterozygous offspring, or that they function to create specific allele combinations that are beneficial under the current environmental conditions through their complementary or epistatic effects. To test these hypotheses, we asked 121 men and women to score the odours of six T–shirts, worn by two women and four men. Their scorings of pleasantness correlated negatively with the degree of MHC similarity between smeller and T–shirt–wearer in men and women not using the contraceptive pill (but not in Pill–users). Depending on the T–shirt–wearer, the amount of variance in the scorings of odour pleasantness that was explained by the degree of MHC similarity (r2) varied between nearly 0 and 23 per cent. There was no apparent effect of gender in the correlation: the highest r2 was actually reached with one of the male odours sniffed by male smellers. Men and women who were reminded of their own mate/ex–mate when sniffing a T–shirt had significantly fewer MHC–alleles in common with this T–shirt–wearer than expected by chance. This suggests that the MHC or linked genes influence human mate choice. We found no significant effect when we tested for an influence of the MHC on odour preferences after the degree of similarity between T–shirt–wearer and smeller was statistically controlled for. This suggests that in our study populations the MHC influences body odour preferences mainly, if not exclusively, by the degree of similarity or dissimilarity. The observed preferences would increase heterozygosity in the progeny. They do not seem to aim for more specific MHC combinations.

Detailed Information about Parasites Revealed by Sexual Ornamentation

One hypothesis assumes that sexual ornamentation has evolved to reveal an individual’s health and vigour. Therefore, choosy mates may use ornamentation as an indicator of the presence and effectiveness of genes for resistance against parasites (Hamilton & Zuk (Science, Wash. 218, 384(1982) ) ). However, the connection between parasites and sexual ornamentation may be more direct: the different characters of the ornamentation could reveal the contribution of each sexual hormone to the whole hormone mix that induced the ornamentation. As androgens and oestrogens are known to weaken specifically parts of the immune system (Grossmann 1985), and several parasites require a specific aspect of the immune system to be countered effectively, the hormone mix may reveal the actual use of an animal’s immune system which depends on the presence and burden of, or even susceptibility to, different parasites. Therefore detailed information about a host’s parasites could be available by studying its sexual ornamentation. Breeding tubercles, the sexual ornamentation of many fish, are induced by several androgens and at least one oestrogen (Wiley & Colette 1970). I studied four characteristics of the ornamentation of male roach (Rutilus rutilus) and found that two of them could be used to discriminate between males that are infected with either Diplozoon or nematodes, the two most severe parasites found. Furthermore, the number of parasites of each group correlates negatively with the expression of one or both of the other ornamental characters. A female roach could potentially decode a male’s ornamentation to gather a sort of clinical picture of him and use this information in her choice of mate.

Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes.

Abstract In tetrapods, the functional (classical) class I and class II B loci of the major histocompatibility complex (Mhc) are tightly linked in a single chromosomal region. In an earlier study, we demonstrated that in the zebrafish, Danio rerio, order Cypriniformes, the two classes are present on different chromosomes. Here, we show that the situation is similar in the stickleback, Gasterosteus aculeatus, order Gasterosteiformes, the common guppy, Poecilia reticulata, order Cyprinodontiformes, and the cichlid fish Oreochromis niloticus, order Perciformes. These data, together with unpublished results from other laboratories suggest that in all Euteleostei, the classical class I and class II B loci are in separate linkage groups, and that in at least some of these taxa, the class II loci are in two different groups. Since Euteleostei are at least as numerous as tetrapods, in approximately one-half of jawed vertebrates, the class I and class II regions are not linked.

Potential genetic benefits of mate selection in whitefish

To test the potential of optimal mate selection with respect to offspring viability, we crossed 10 female and 10 male whitefish in all possible combinations and reared the resulting 100 sib groups in several replicates. We recorded two types of egg mortality, one that was correlated to developmental problems, and a later one that was correlated to a bacterial infection. We found strong maternal and paternal effects in both types of mortality. Early mortality also depended on which female was mated with which male, suggesting partial incompatibilities. The later mortality, but not the former, could be predicted by male breeding ornamentation. More strongly ornamented males sired offspring that better survived the epidemic during egg development. This ‘good genes’ effect was larger than expected from theory: optimal mate selection would have improved offspring survival during the epidemic by about 12% (or reduce mortality by about 66%) as compared with random mating.

The Long-Term Benefits of Human Generosity in Indirect Reciprocity

Among the theories that have been proposed to explain the evolution of altruism are direct reciprocity and indirect reciprocity. The idea of the latter is that helping someone or refusing to do so has an impact on ones reputation within a group. This reputation is constantly assessed and reassessed by others and is taken into account by them in future social interactions. Generosity in indirect reciprocity can evolve if and only if it eventually leads to a net benefit in the long term. Here, we show that this key assumption is met. We let 114 students play for money in an indirect and a subsequent direct reciprocity game. We found that although being generous, i.e., giving something of value to others, had the obvious short-term costs, it paid in the long run because it builds up a reputation that is rewarded by third parties (who thereby themselves increase their reputation). A reputation of being generous also provided an advantage in the subsequent direct reciprocity game, probably because it builds up trust that can lead to more stable cooperation.

Non-random fertilization in mice correlates with the MHC and something else

One evolutionary explanation for the success of sexual reproduction assumes that sex is an advantage in the coevolutionary arms race between pathogens and hosts. Accordingly, an important criterion in mate choice and maternal selection thereafter could be the allelic specificity at polymorphic loci involved in parasite-host interactions, e.g. the MHC (major histocompatibility complex). The MHC has been found to influence mate choice and selective abortions in mice and humans. However, it could also influence the fertilization process itself, i.e. (i) the oocytes choice for the fertilizing sperm, and (ii) the outcome of the second meiotic division after the sperm has entered the egg. We tested both hypotheses in an in vitro fertilization experiment with two inbred mouse strains congenic for their MHC. The genotypes of the resulting blastocysts were determined by polymerase chain reaction. We found nonrandom MHC combinations in the blastocysts which may result from both possible choice mechanisms. The outcome changed significantly over time, indicating that a choice for MHC combinations during fertilization may be influenced by one or several external factors.

Male-biased susceptibility to helminth infection : an experimental test with a copepod

Recent reviews on sex biases in parasitism found that males generally suffer from a slightly higher susceptibility to helminth infection than females. Sex hormones like testosterone have been suggested as the mechanism that causes the bias in parasite susceptibility. Many of the original studies used data that stem from free-ranging host populations which were naturally infected. Since gender-related behaviours could result in differential exposure to parasites, it is necessary to experimentally disentangle differences in exposure from differences in susceptibility. We tested whether we could find a sex bias in susceptibility under experimental conditions, i.e. by controlling for gender related differences in exposure. Furthermore, we used an invertebrate host to test whether the pattern observed in many vertebrates can be extended to a host species that lacks testosterone. As models we used the cestode Schistocephalus solidus and its first intermediate host, the copepod Macrocyclops albidus. We found that male copepods were more often infected than females. Since infected males had on average also more parasite larvae than infected females, the chance of a S. solidus larvae to become established in its first intermediate host was more than twice as high in male than in female copepods. This shows that, under experimental conditions, male-biased susceptibility to helminth infection can be very strong. Moreover, the pattern seen in many vertebrates can be extended to an invertebrate host that lacks testosterone.

The infectivity, growth, and virulence of the cestode Schistocephalus solidus in its first intermediate host, the copepod Macrocyclops albidus

In an experiment to study the infectivity, growth and virulence of Schistocephalus solidus in their first intermediate host, copepods of the species Macrocyclops albidus were kept singly and exposed to up to 9 coracidia. Eleven or 14 days post-infection (p.i.) the presence and growth of the cestode larvae relative to survival, growth and reproduction of their host was determined. As expected, the probability of a copepod becoming infected increased with increasing numbers of parasites administered. However, the chances of a single coracidium establishing in a copepod also increased with increasing numbers of coracidia administered, which indicates that the parasites profit from a dilution effect of the hosts defence. Copepod size or developmental stage had no significant effect on the infection, but 14 days p.i., constraining effects of copepod size on the growth of the parasites were apparent. Moreover, procercoids in multiple infections grew smaller and developed their cercomer at a smaller size than those in single infections. No significant effect of the parasite on host mortality was found within the observation period. However, growth between the 5th copepodid stage and adult stage was negatively affected by infection. An infection with S. solidus was also strongly linked with host reproduction: infected females were more likely to bear an egg sac at the end of the experiment than non-infected ones. These egg sacs, however, contained fewer eggs.

MHC-genotype of progeny influenced by parental infection

In a previous series of in vitro fertilization experiments with mice we found non–random combination of major histocompatibility complex (MHC) haplotypes in the very early embryos. Our results suggested that two selection mechanisms were operating: (i) the eggs selected specific sperm; and (ii) the second meiotic division in the eggs was influenced by the type of sperm that entered the egg. Furthermore, the proportion of MHC–heterozygous embryos varied over time, suggesting that non–random fertilization was dependent on an external factor that changed over time. As a higher frequency of heterozygous individuals correlated with an uncontrolled epidemic by MHV (mouse hepatitis virus), we suggested that MHV–infection might have influenced the outcome of fertilization. Here, we present an experiment that tests this hypothesis. We infected randomly chosen mice with MHV and sham–infected control mice five days before pairing. We recovered the two–cell embryos from the oviduct, cultured them until the blastocyst stage, and determined the genotype of each resulting blastocyst by polymerase chain reaction. We found the pattern that we expected from our previous experiments: virus–infected mice produced more MHC–heterozygous embryos than sham–infected ones. This suggests that parents are able to promote specific combinations of MHC–haplotypes during fertilization according to the presence or absence of a viral infection.