genes G C A T T A C G G C A T Article Insights into Avian Incomplete Dosage Compensation: Sex-Biased Gene Expression Coevolves with Sex Chromosome Degeneration in the Common Whitethroat Hanna Sigeman ID , Suvi Ponnikas, Elin Videvall, Hongkai Zhang, Pallavi Chauhan, Sara Naurin and Bengt Hansson * ID Department of Biology, Lund University, Ecology Building, 223 62 Lund, Sweden; hanna.sigeman@biol.lu.se (H.S.); suvi.ponnikas@biol.lu.se (S.P.); elin.videvall@biol.lu.se (E.V.); ho6021zh-s@student.lu.se (H.Z.); pallavi.chauhan@biol.lu.se (P.C.); sara.naurin@fs.lu.se (S.N.) * Correspondence: bengt.hansson@biol.lu.se; Tel.: +46-46-222-4996 Received: 16 April 2018; Accepted: 23 July 2018; Published: 26 July 2018   Abstract: Non-recombining sex chromosomes (Y and W) accumulate deleterious mutations and degenerate. This poses a problem for the heterogametic sex (XY males; ZW females) because a single functional gene copy often implies less gene expression and a potential imbalance of crucial expression networks. Mammals counteract this by dosage compensation, resulting in equal sex chromosome expression in males and females, whereas birds show incomplete dosage compensation with significantly lower expression in females (ZW). Here, we study the evolution of Z and W sequence divergence and sex-specific gene expression in the common whitethroat (Sylvia communis), a species within the Sylvioidea clade where a neo-sex chromosome has been formed by a fusion between an autosome and the ancestral sex chromosome. In line with data from other birds, females had lower expression than males at the majority of sex-linked genes. Results from the neo-sex chromosome region showed that W gametologs have diverged functionally to a higher extent than their Z counterparts, and that the female-to-male expression ratio correlated negatively with the degree of functional divergence of these gametologs. We find it most likely that sex-linked genes are being suppressed in females as a response to W chromosome degradation, rather than that these genes experience relaxed selection, and thus diverge more, by having low female expression. Overall, our data of this unique avian neo-sex chromosome system suggest that incomplete dosage compensation evolves, at least partly, through gradual accumulation of deleterious mutations at the W chromosome and declining female gene expression. Keywords: sex chromosomes; recombination; degeneration; gene expression; dosage compensation 1. Introduction Sex chromosomes have evolved from autosomes repeatedly in many taxa [1–4]. This chromosomal transformation is believed to start with the acquisition of a sex-determining mutation [1,5–7]. Thereafter, sex-specific mutations that are beneficial to the sex which the locus determines accumulate, leading to suppression of genetic recombination in this region of the chromosome [8–10]. Recombination suppression will prevent expression of these sex-specific alleles in the other sex and will retain linkage of these new sex-optimizing loci [5,9,11,12]. Typically, the suppression of recombination then continues to spread across the chromosome, ultimately resulting in two divergent, heteromorphic, non-recombining sex chromosomes (X-Y or Z-W), with only a small pseudoautosomal region (PAR) continuing to recombine [13,14]. The complete lack of recombination over a substantial part of one Genes 2018, 9, 373; doi:10.3390/genes9080373 www.mdpi.com/journal/genes