Molecular Mechanisms and Evolutionary Processes Contributing to Accelerated Divergence of Gene Expression on theDrosophilaX Chromosome

Abstract

In species with a heterogametic sex, population genetics theory predicts that DNA sequences on the X chromosome can evolve faster than comparable sequences on autosomes. Both neutral and nonneutral evolutionary processes can generate this pattern. Complex traits like gene expression are not predicted to have accelerated evolution by these theories, yet a "faster-X" pattern of gene expression divergence has recently been reported for both Drosophila and mammals. Here, we test the hypothesis that accelerated adaptive evolution of cis-regulatory sequences on the X chromosome is responsible for this pattern by comparing the relative contributions of cis- and trans-regulatory changes to patterns of faster-X expression divergence observed between strains and species of Drosophila with a range of divergence times. We find support for this hypothesis, especially among male-biased genes, when comparing different species. However, we also find evidence that trans-regulatory differences contribute to a faster-X pattern of expression divergence both within and between species. This contribution is surprising because trans-acting regulators of X-linked genes are generally assumed to be randomly distributed throughout the genome. We found, however, that X-linked transcription factors appear to preferentially regulate expression of X-linked genes, providing a potential mechanistic explanation for this result. The contribution of trans-regulatory variation to faster-X expression divergence was larger within than between species, suggesting that it is more likely to result from neutral processes than positive selection. These data show how accelerated evolution of both coding and noncoding sequences on the X chromosome can lead to accelerated expression divergence on the X chromosome relative to autosomes.

Buffering of Genetic Regulatory Networks inDrosophila melanogaster

“…There is a strong consensus emerging from the analyses of a variety of model organisms: in yeast (Kvitek et al 2008;Artieri and Fraser 2014), fly (Wang et al 2008;Coolon et al 2014Coolon et al , 2015Graze et al 2014), and mouse (Goncalves et al 2012;Crowley et al 2015;Pinter et al 2015) that cis-and trans-effects are compensatory. In intraspecific D. melanogaster F 1 's, compensatory interactions were observed in 79% of cases, and in interspecific D. simulans/D.…”

The Y Chromosome Modulates Splicing and Sex-Biased Intron Retention Rates in Drosophila

“…These sex-specific and sex-biased phenotypes partially emerge from regulatory differences in gene expression. While sex differences in gene expression are observed in several tissues, they are especially manifested in the gonads (MEIKLEJOHN et al 2003;PARISI et al 2003;ELLEGREN AND PARSCH 2007;ZHANG et al 2007;ASSIS et al 2012;PARSCH AND ELLEGREN 2013;PERRY et al 2014) and are often traced to variation in the sex chromosomes (GIBSON et al 2002;LEMOS et al 2008;SACKTON et al 2011;COOLON et al 2015). In Drosophila, the X-chromosome is relatively large with thousands of protein-coding genes, with experimental evidence confirming population genetic predictions about the consequences of X-linked variation.…”

Gene Regulation and Speciation

“…If regulatory divergence underlies hybrid dysfunction, evolutionarily diverged regulation of sex-linked genes may be expected [67]. Several recent studies have found that expression diverges faster for some genes on the X (in XY taxa) and Z (in ZW taxa) chromosomes than on the autosomes between species [68–73]. Faster divergence of sex-linked gene expression is especially strong for genes with sex-biased effects (male-biased effects in XY taxa and female-biased effects in ZW taxa) [69,70,71,74].…”