A new paper in tomorrow’s issue of Nature finds a surprisingly simple explanation for the variation in horn size among Soay sheep on an uninhabited Scottish isle. Because males with the biggest horns tend to win more battles, get access to more females, and therefore have higher reproductive success, we would expect that given such strong directional sexual selection there would be little variation left in terms of horn size. Instead, horn size varies from really big to downright petite (scurred, see photo above). So how is this variation maintained in light of strong directional selection for large horns? A few hypotheses have been forwarded, but some of the most favored include good genes and genetic trade-offs. In the good genes hypothesis, many genes determine condition in males, and those in the best condition have the most sexually desirable trait. Because so many genes are involved there is great potential for mutation thus, variation is maintained. In the genetic trade-off hypothesis there is a trade-off between natural and sexual selection (imagine if your horns got too long you wouldn’t be able to lift your head).
Johnson et al. offer a 3rd hypothesis, although it is connected to the genetic trade-off hypothesis: heterozygote advantage. Heterozygote advantage is a case in which heterozygous individuals that possess two different alleles (version of a gene) have greater fitness (survivorship and reproduction) than individuals that have two of the same alleles (homozygotes). Probably the most famous example of heterozygote advantage is the case of sickle cell anemia (but see this blog on relaxed heterozygote advantage). Two copies of a mutated allele results in sickle-cell anemia while two copies of the wild-type allele makes individuals more susceptible to malaria. One copy of each allele is ‘just right;’ those individuals have higher fitness because they are less susceptible to malaria nor do they suffer the ill effects of sickle-cell anemia. While heterozygote advantage has been shown in a few cases of natural selection, this is the first evidence I’ve seen for heterozygote advantage in sexual selection.
So why has heterozygote advantage rarely been documented (and never before in sexual selection as far as I know)? First, traits are rarely determined by a single gene. In a previous article, Johnson and colleagues found that horn size was almost completely controlled by a single gene locus and it has only two alleles. As long as an individual possesses one normal allele (Ho+), they have big horns. Possession of two mutated alleles (HoP) results in less than impressive horns (see Figure from Johnson et al. above). After genotyping and tracking the fitness of 1750 sheep, Johnson et al. found that individuals homozygous for HoP had significantly lower reproductive success than heterozygotes or those homozygous for Ho+. Homozygotes for Ho+, however, had significantly lower survivorship than the other two genotypes. Heterozygotes, then, get the mating AND survivorship advantage and thus have the highest fitness. With heterozygotes being favored, the HoP allele is maintained in the population and scurred horn males remain.
So why are two copies of the Ho+ gene detrimental to survivorship? The authors argue that with big horns males spend more time fighting and defending their females and thus spend less time on feeding and other survivorship necessities. I don’t find this argument compelling because it doesn’t explain how heterozygotes maintain high survivorship. Likely the authors will need to explore exactly how this gene affects horn growth. In mice the gene is known to play a role in both bone formation and male sexual development. I’m guessing we’ll be seeing more from this research group soon.