Pervasive and Largely Lineage-Specific Adaptive Protein Evolution in the Dosage Compensation Complex of Drosophila melanogaster

Abstract

Dosage compensation refers to the equalization of X-linked gene transcription among heterogametic and homogametic sexes. In Drosophila, the dosage compensation complex (DCC) mediates the twofold hypertranscription of the single male X chromosome. Loss-of-function mutations at any DCC protein-coding gene are male lethal. Here we report a population genetic analysis suggesting that four of the five core DCC proteins-MSL1, MSL2, MSL3, and MOF-are evolving under positive selection in D. melanogaster. Within these four proteins, several domains that range in function from X chromosome localization to proteinprotein interactions have elevated, D. melanogaster-specific, amino acid divergence.

Loss of reproductive parasitism following transfer of male-killing Wolbachia to Drosophila melanogaster and Drosophila simulans

“…Thus, interfering with the dosage compensation complex (DDC), which is responsible for such X chromosome upregulation in males, could bring about embryonic male killing. It is therefore notable that most or all of the genes encoding the proteins of the DDC have undergone rapid, positive selection in the melanogaster group (Levine et al, 2007;Rodriguez et al, 2007). Therefore, if wInn targets a certain component of the DDC of D. innubila, it is possible that this component is sufficiently different in D. melanogaster and D. simulans to be unrecognizable.…”

Positive Selection at the Binding Sites of the Male-Specific Lethal Complex Involved in Dosage Compensation in Drosophila

“…Two recent studies have shown that the proteins involved in dosage compensation have undergone adaptive protein evolution in D. melanogaster, but not in its close relatives (Levine et al 2007;Rodriguez et al 2007). In particular, the protein domains of MSL1 and MSL2 that are responsible for their specific targeting to the X chromosome harbor strong signatures of positive selection (Levine et al 2007;Rodriguez et al 2007).…”

“…Interestingly, two recent studies found evidence for adaptive evolution in all five (or four of five) proteincoding genes of the MSL complex in D. melanogaster (Levine et al 2007;Rodriguez et al 2007). In particular, dramatic positive selection was detected in MSL1 and MSL2 protein domains shown to be responsible for their specific targeting to the X chromosome (Levine et al 2007;Rodriguez et al 2007).…”

“…In particular, dramatic positive selection was detected in MSL1 and MSL2 protein domains shown to be responsible for their specific targeting to the X chromosome (Levine et al 2007;Rodriguez et al 2007). This signature of positive selection at an essential protein-DNA interface of the complex was surprising and may suggest that X chromosomal MSL-binding DNA segments themselves are changing rapidly.…”

“…Here, I study patterns of molecular evolution and population variation of the roX genes and the putative binding site 18D10 in D. melanogaster populations to test whether the MSL-binding sites are indeed under positive selection in the D. melanogaster lineage. For comparisons, the same regions were sequenced in D. simulans, where no evidence of adaptive protein evolution was detected (Levine et al 2007;Rodriguez et al 2007), and D. yakuba populations, a species where we have no a priori expectation of positive selection operating on the MSL-binding sites. Indeed, I find various signatures of positive selection acting on the MSL-binding sites in D. melanogaster, but little evidence for adaptive evolution in D. simulans or D. yakuba.…”