Saturday, December 22, 2007

Are males just simpler?

There is an interesting article in PNAS on the differences in inheritance in males and female Drosophila by Wayne M et al.

Sexual selection is a key driving force in evolution. Sexual dimorphisms (differences between the sexes) are one of the most obvious patterns in nature, from peacocks tails to the elaborate genitalia of insects. So there is obviously a lot of interest in understanding how sexual dimorphisms arise, and a lot of evolutionary theory (see evolgen for example) devoted to understanding how they evolve. Another pattern in nature is that male traits evolve quickly (compared to female traits) between species. The authors discuss how differences in the form take by genetic variation in males and females could be a somewhat neglected component of this rapid evolution in male traits.

Before I can discuss their results we need a brief aside into additive and dominant components of genetic variance. See also gene expression for an explanation (which may well be clearer than my own).
A mutation is said to act in an additive manner if the effect of a mutation in heterozygotes is exactly intermediate between homozgyotes for the mutation. If the heterozygote phenotype is not intermediate to the homozygotes (for example it resembles one of the parents more) then the mutation shows dominance. Now often we don't know (or perhaps care about) the mutations underlying a trait, as perhaps there are many mutations controlling a trait.

Crosses of individuals can be performed to disect the genetic basis of a trait, and we can learn about the amount of variation in a trait that can explained by different kinds of 'variance' (additive or dominant, and higher epistatic terms that we shall not worry about here). Now the additive and dominant contribution to the variance are not the properties of a individual mutations, but are the properties of the (perhaps many) mutations present in the parents in a cross (which depends on the make up of the population). A trait can show purely additive variation, with the offspring of a cross always being exactly intermediate between the parents. Or the offspring can resemble one of the parents more, suggesting that the phenotype is not determined merely by the additive sum of the mutations contributed by the parents and has some dominance component. The additive component of a trait in a cross (or a population) is defined to be the amount of genetic variation in a trait, attributable to the average contribution of parent's genotype to a phenotype in the child (
i.e. what does a parent contribute to a child averaged across the possible matings). The dominance component is the remaining proportion of variation in the phenotype assignable to the specific genotype of the child (beyond the average contribution of the allele from each parent),
i.e. the particular combination of the parents of the child.

The proportion of genetic variation in a trait that is additive (the narrow sense heritability), is very important quantity as natural selection changing the mean of a trait usually only acts on the additive variation in a trait. Imagine natural selection acting to change the mean of a phenotype,
e.g. selection for longer horns. A mother with a particular genotype might do very well for herself (i.e. have many successful offspring due to her genotype giving her a phenotype of long horns), but she only passes one of her alleles to each child. The phenotype of the child is determined by the combination of the allele from the mother, and the allele from a father. Thus it is the average (across fathers) contribution of one of the mother alleles to the child which matters, for how the mean of the trait changes. (Note that this not to say that dominant mutations are not selected upon, as dominant mutations also contribute to additive variation.)

So traits that have large additive genetic components are more easily changed by selection. The authors set out to investigate the genetic basis of gene expression level in Drosophila (for many genes measured on array) and how this differs between males and females. By a series of crosses, the authors find that many more genes show additive genetic variation in their expression level in males than in females, and that a number of these genes are found on the X chromosome (as well as on the autosomes). Now the X chromosome seems to be be the key to this difference in the form of genetic variation (and the authors conduct further experiments to show this). As males have only a single X chromosome there simply is not any dominance due to genetic variation on the X chromosome (at least not simple non-epistatic dominance). The genetic variation on the X chromosome in males mainly contributes to the additive genetic component of variation (as there is no second allele to cause dominance). So genes on the X with cis acting mutations that affect gene expression will inherited in an additive manner. Also mutations on the X which affect gene expression in trans (on the autosomes), will contribute to the additive genetic component of the trait in males but can be involved in the dominance component in females. So the expression level of many genes is more additive and so more easily selected upon in males than in females, because the single copy of the X chromosome makes thing more simple in males. I particularly like this idea that trans modifers of gene expression on the X chromosome, makes gene expression simpler to select upon in males.

This paper is a nice demonstration of the power of crosses combined with gene expression traits to reveal general patterns of inheritance. These patterns are key to understanding the raw material that evolution acts upon, and such studies are vital if we to dissect the historical patterns found in genomic data.


Evil Fruit Lord said...

Of course, the peacock, which you mention as an example, uses the ZW sex determination system (like all birds), rather than the XY system, so the females ought to evolve faster, since females in that system are ZW, while males are ZZ.

I don't recall if birds' Z and W chromosomes contain vastly differing amounts of genes like the X and Y, though.

G said...

true. Perhaps using a bird example was unhelpful.