Of Geese and Ganders

Brian at Laelaps has written a post entitled “What’s good for the gander isn’t always good for the goose“, in which he describes some examples of sexual dimorphism in charismatic vertebrates. Studying the phenotypes of these traits is interesting, but what’s happening on the genomic level? That is, how do differences between males and females affect the distribution of genes on chromosomes?

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Many of the traits that are beneficial for males are deleterious in females (and vice versa). For example, male sheep with big horns will mate more and leave more offspring, but females with big horns will waste their energy on those horns rather than producing babies (feminism has yet to catch on amongst bighorn sheep). If a single gene controls this trait, there will be antagonism between males and females for which variants are most fit. This sexual antagonism was modeled in an elegant way by William Rice. Rice developed a model that integrated sexual antagonism with sex chromosomes, and showed that, depending on a couple parameters, you could predict whether sexually antagonistic genes will be located on X chromosomes or autosomes.

Here are Rice’s results in a nutshell. For these examples, we’re assuming males are the heterogametic sex (XY), and females are homogametic (XX). If beneficial mutations are recessive, you would expect male-biased genes to accumulate on the X chromosome. That’s because those beneficial mutations will manifest themselves immediately in males (they aren’t masked by a dominant allele), while they will be essentially neutral in females (she will still have a copy of the dominant allele). This will lead to more fixations of male-biased mutations on the X chromosome than on the autosomes (where beneficial mutations will be masked in both males and females).

Alternatively, if beneficial mutations are dominant, they will be under selection regardless if they are on the X chromosome or an autosome. But the X chromosome spends 2/3 of it it’s evolutionary history in females, but only 1/3 in males (assuming equal numbers of breeding males and females). Therefore, selection for male-biased genes will be stronger on the autosomes than on the X chromosome, while selection for female-biased genes will be stronger on the X chromosome. And we will expect male-based genes to accumulate on the autosomes, while female-biased genes will accumulate on the X chromosome.

That’s the gist of the model. If we know the dominance of new beneficial sex-biased alleles and the sex ratio of breeding individuals, we can predict the genomic distribution of male- and female-biased genes. The problem is, it’s damn near impossible to know the values of those parameters, so the theory won’t get us much further. That said, it’s an important first step in figuring out the distribution of sex-biased genes.

Next time, we’ll take a look at what the data show regarding the distribution of these sexually antagonistic genes.

Rice WR. 1984. Sex Chromosomes and the Evolution of Sexual Dimorphism. Evolution 38: 735-742 URL


  1. #1 Graham
    November 23, 2007

    nice description. Though if the trait has strong deleterious effects in females, the fact that it is recessive does not ensure that it will become fixed in the population. An important (though slightly more complicated) point (discussed by Rice) is that fixation of new male biased recessive traits on the X is aided by modifier mutations that subsequently arise. A mutation whose effect is to modify the new trait to only be expressed in males, will aid the spread of the new trait through the population as it helps avoid the deleterious effects in females. The initial absence of the trait in females increases the persistence time of the new trait and so the time available for the such modifiers to arise.

  2. #2 Jim Thomerson
    November 25, 2007

    For species which do not have sex chromosomes; am I correct in thinking this argument does not apply? Ii think of sex chromosomes as chromosomes which appear different in a prepared karyotype. I am probably 10 years behind the curve on this.

    The two species currently placed in the Rivulid killifish genus Gnatholebias are (so says DNA) sister species. G. hoignei has XY sex chromosomes, and G. zonatus does not. This latter statement based on our published karyotypes.

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