Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 110; no. 16; pp. 6453 - 6458
• Main Authors: Vicoso, Beatriz, Kaiser, Vera B., Bachtrog, Doris
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 16.04.2013; National Acad Sciences
• Subjects: Animals; Autosomes; Biological Sciences; Birds; Chickens; Chromosomes; Computational Biology; Dromaiidae - genetics; Emus; Evolution; Evolution, Molecular; Evolutionary biology; Female; Gene expression; Gene Expression Profiling; Gene Expression Regulation - genetics; Genes; Genetic recombination; Genomics; Male; Mutation; Polymorphism, Single Nucleotide - genetics; Sex Characteristics; Sex chromosomes; Sex Chromosomes - genetics; Species Specificity; Synteny - genetics; Z chromosome
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1217027110

Sex chromosomes originate from autosomes. The accumulation of sexually antagonistic mutations on protosex chromosomes selects for a loss of recombination and sets in motion the evolutionary processes generating heteromorphic sex chromosomes. Recombination suppression and differentiation are generally viewed as the default path of sex chromosome evolution, and the occurrence of old, homomorphic sex chromosomes, such as those of ratite birds, has remained a mystery. Here, we analyze the genome and transcriptome of emu (Dromaius novaehollandiae) and confirm that most genes on the sex chromosome are shared between the Z and W. Surprisingly, however, levels of gene expression are generally sex-biased for all sex-linked genes relative to autosomes, including those in the pseudoautosomal region, and the male-bias increases after gonad formation. This expression bias suggests that the emu sex chromosomes have become masculinized, even in the absence of ZW differentiation. Thus, birds may have taken different evolutionary solutions to minimize the deleterious effects imposed by sexually antagonistic mutations: some lineages eliminate recombination along the protosex chromosomes to physically restrict sexually antagonistic alleles to one sex, whereas ratites evolved sex-biased expression to confine the product of a sexually antagonistic allele to the sex it benefits. This difference in conflict resolution may explain the preservation of recombining, homomorphic sex chromosomes in other lineages and illustrates the importance of sexually antagonistic mutations driving the evolution of sex chromosomes.