Abstract
The X chromosome is present as a single copy in the heterogametic sex, and this hemizygosity is expected to drive unusual patterns of evolution on the X relative to the autosomes. For example, the hemizgosity of the X may lead to a lower chromosomal effective population size compared to the autosomes, suggesting that the X might be more strongly affected by genetic drift. However, the X may also experience stronger positive selection than the autosomes, because recessive beneficial mutations will be more visible to selection on the X where they will spend less time being masked by the dominant, less beneficial allele—a proposal known as the faster-X hypothesis. Thus, empirical studies demonstrating increased genetic divergence on the X chromosome could be indicative of either adaptive or non-adaptive evolution. We measured gene expression in Drosophila species and in D. melanogaster inbred strains for both embryos and adults. In the embryos we found that expression divergence is on average more than 20% higher for genes on the X chromosome relative to the autosomes; but in contrast, in the inbred strains, gene expression variation is significantly lower on the X chromosome. Furthermore, expression divergence of genes on Muller's D element is significantly greater along the branch leading to the obscura sub-group, in which this element segregates as a neo-X chromosome. In the adults, divergence is greatest on the X chromosome for males, but not for females, yet in both sexes inbred strains harbour the lowest level of gene expression variation on the X chromosome. We consider different explanations for our results and conclude that they are most consistent within the framework of the faster-X hypothesis.
Highlights
It has long been suspected that the distinct properties of the X chromosome might in turn produce distinct patterns of evolution on the X relative to the autosomes [1,2]
There is a single copy of the X chromosome in males, yet two copies in females
Our results show that mean gene expression divergence is higher for the X chromosome relative to autosomes and, more surprisingly, this effect is much stronger in the Drosophila embryos relative to the adults
Summary
It has long been suspected that the distinct properties of the X chromosome might in turn produce distinct patterns of evolution on the X relative to the autosomes [1,2]. We consider adaptive evolution, the hemizygosity of the X is expected to facilitate the spread of recessive beneficial mutations, the selective benefit of which would otherwise be masked when in a heterozygous state on the autosomes [1,3,4,5]. A faster X may be expected if mutations have sexually antagonistic effects, in which the sign of the selection coefficient is opposite in males and females [6]. In both adaptive and non-adaptive scenarios, it is the hemizygous context of the X chromosome in the heterogametic sex that is expected to drive more rapid evolution relative to the autosomes [7]
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