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Sniffing Around for Mr. Right

What turns women on: good genes or complementary genes?

One of the great remaining mysteries of human reproduction is whether some biological basis exists for choosing a mating partner. Is it possible that the profound emotional power of romantic love is linked to underlying processes that conform to some genetic agenda? Or is love a completely open system without any deep biological significance? Evidence regarding a genetic basis for mate choice in other organisms has interesting implications for human biology when considered from a female perspective.

Seeking good genes?

It seems intuitively obvious that it is advantageous for a female to seek a mate who has successfully competed with other males. If a male’s social status reflects his genetic make-up, it logically follows that females could benefit from having sons who, in turn, should be similarly successful in competing with other males for mating access. This “good genes” hypothesis, which predicts that the choosing sex should mate with individuals with features indicating overall genetic quality, has been widely accepted. Consider, for instance, a troop of plains baboons in which several adult males compete with one another to establish rank in a dominance hierarchy. Numerous observations of social groups of baboons have revealed that the highest-ranking “alpha” male typically achieves the greatest mating success with resident females. As a rule, he also has preferential access to food resources. In short, bullying despots who kick sand in the eyes of other males would seem to be prized mates. Such observations easily lead to the assumption that mate choice in women follows the same principle and that they are generally attracted to men who have attained high socioeconomic status.

The “good genes” hypothesis, taken at face value, seemingly makes very good sense, but closer examination reveals problems. In the first place, it stems from an inherent tendency to see females as passive responders during mate selection: It is a male prerogative to establish a hierarchy, and females simply accept high-ranking males as the best sires of their offspring. But it is vital to consider alternatives. A substantial literature on cryptic female choice in animals reveals that various mechanisms permit selection of paternity both before and after mating.

It is also important to remember that social rank commonly changes dynamically over a male’s lifetime. After attaining sexual maturity, a male must engage in contests with other males to establish his social rank, usually after migrating to a different troop in plains baboons. Once a male’s rank is determined, it is generally fairly stable, but changes can occur in various ways and at various times. Eventually, as a male ages, his rank usually declines in the face of increasing challenges from younger males. So a male’s relative value in social competition will be reflected mainly by how long he keeps his highest rank. In baboons, for instance, a particularly successful male may occupy the alpha position for several years. But this is where a largely unrecognized problem arises. A male who holds on to the alpha position for some time has the same genes both when he is a young challenger and when he loses that status in old age. So if females really do benefit from seeking “good genes”, it would be advantageous to mate with very promising but not yet successful young males and with old but once successful males in their twilight years.

Vive la difference

In fact, there is an intriguing alternative to the good genes hypothesis, which is that a female seeks a male whose genes optimally match her own. If a potential mate’s genes are too similar, the offspring may lack sufficient genetic variability, and this could trigger Inbreeding avoidance. At the other extreme, if the mate’s genes are too different, the offspring may suffer disruptive effects of mismatched genes. So a female may benefit by mating with a male possessing complementary genes, enabling her to produce offspring that have appropriate genetic variability (heterozygosity). With so-called good genes, all females benefit similarly from choosing specific males who have proven successful in social competition. But with complementary genes mate choice may differ markedly between females depending on individual-specific matching of genes.

Natural selection directly depends on genetic variation, so it may be that a particular level of heterozygosity across the genome is in itself advantageous. But it is also possible that optimized variability in specific classes of genes may be particularly advantageous. A prime candidate is the Major Histocompatibiilty Complex (MHC), which plays a key part in acquired immunity and hence resistance to infections. The MHC  —  present in all vertebrates from fish to humans  —  consists of  molecules presented on the cell surface that interact with antigens (foreign proteins). Those molecules are produced by a strikingly large family of genes (140 in humans), each of which shows great variability. Crudely stated, it seems that the availability of many different MHC molecules increases the probability that one or more will cross-react with any given foreign protein and activate an immune response. So a female can increase offspring survival by choosing a mate whose MHC optimally complements her own.

Numerous studies of mice have indicated that mate choice is, indeed, connected with variation in the MHC, signalled by differences in individual odour. British biologist Jo Setchell and colleagues investigated reproduction in a semi-free-ranging population of mandrills in relation to MHC type, testing paternity with microsatellites. The probability of a given male siring an offspring increased along with MHC dissimilarity from the mother. Reproductive success also increased as males showed greater heterozygosity in microsatellites and MHC diversity. Moving on to humans, biologist Claus Wedekind and colleagues conducted intriguing experiments in Switzerland in which students rated the odours of T-shirts previously worn for two nights by individual members of the opposite sex. Students scored body odours as more pleasant when the MHC of an opposite-sexed individual differed from theirs than when it was more similar. These results suggest that the MHC, or genes linked to it, influence mate choice not only in other mammals but also in humans.

Overall, it seems likely that both good genes and compatible genes play a significant part in mate choice. Considerable evidence from paternity tests shows that dominance rank is correlated with male reproductive success. On the other hand, there is convincing evidence that MHC-associated mate choice also occurs. As usual in biology, the conclusion is some sort of compromise solution. Females may be impressed by sand-kicking alpha males, but they may also pay attention to their body odour.

References

Brown, J.L. (1997) A theory of mate choice based on heterozygosity. Behav. Ecol. 8:60-65.

Grob, B., Knapp, L.A., Martin, R.D. & Anzenberger, G. (1998) The major histocompatibility complex and mate choice: Inbreeding avoidance and selection of good genes. Exp. Clin. Immunogenet. 15:119-129.

Knapp, L.A., Ha, J.C. & Sackett, G.P. (1996) Parental MHC antigen sharing and pregnancy wastage in captive pigtailed macaques. J. Reprod. Immunol. 32:73-78.

Milinski, M. & Wedekind, C. (2001) Evidence for MHC-correlated perfume preferences in humans. Behav. Ecol. 12:140-149.

Ober, C., Weitkamp, L.R., Cox. N., Dytch, H., Kostyu, D. & Elias, S. (1997) HLA and mate choice in humans. Am. J. Hum. Genet. 61:497-504.

Roberts, S.C. & Little, A.C. (2008) Good genes, complementary genes and human mate choice. Genetica 132:309-321.

Setchell, J.M., Charpentier, M.J.E., Abbott, K.M., Wickings, E.J. & Knapp, L.A. (2010) Opposites attract: MHC-associated mate choice in a polygynous primate. J. Evol. Biol. 23:136-148.

Wedekind, C. & Füri, S. (1997) Body odour preferences in men and women: Do they aim for specific MHC-combinations or simply heterozygosity? Proc. Roy. Soc. Lond. B 264:1471-1479.

Wedekind, C., Seebeck, T., Bettens, F. & Paepke, A.J. (1995) MHC-dependent mate preferences in humans. Proc. Roy. Soc. Lond. B 260:245-249.

Wedekind, C., Seebeck, T., Bettens, F. & Paepke, A.J. (2006) The intensity of human body odors and the MHC: Should we expect a link? Evol. Psychol. 4:85-94.

Yamazaki, K. & Beauchamp, G.K. (2007) Genetic basis for MHC-dependent mate choice. Genet. Sex. Diff. Sexual. Dimorph. Behav., 59:129-145.

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