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Evolution of sex chromosomes and sex-biased gene expression

Sex chromosomes have evolved from non-sex-determining chromosomes (autosomes) multiple times throughout the tree of life. Ever since their discovery, the sex chromosomes have captivated researchers because of their obvious involvement in fundamental aspects of an organism’s life, such as sex determination, sexual reproduction and sexual conflicts. Despite this long-lasting fascination, the biology of sex chromosomes remains unclear in several central aspects, in particular regarding their almost ubiquitous evolution of recombination cessation and impoverished gene content, and the multifaceted consequences thereof.

Currently we lack sufficient understanding of the evolutionary dynamics of sex chromosome gene content, how and why the sexes express sex chromosome genes differently, and the interplay between sex chromosomes and sexual conflicts. This lack of detailed knowledge about sex chromosome evolution compromises our understanding of fundamental biological questions (e.g. the evolution of sexual conflicts) as well as more practical ones (e.g. about sex-linked genetic diseases).

An obvious reason for these unfortunate knowledge gaps is that many sex chromosomes, such as in mammals and most birds, are very difficult to study because they are severely degenerated and have lost the genomic material we wish to study as they formed a long time ago.

Evolution of sex chromosomes in songbirds

Our research focuses on Sylvioidea passerine birds where we have recently detected a new sex chromosome, a neo-sex chromosome, which has been formed by a fusion between an autosome and the ancestral sex chromosomes. This neo-sex chromosome is evolutionarily very interesting and promising for research: First, the female-specific neo-W chromosome is in an intermediate stage of degeneration. This is an ideal situation for research on sex chromosomes ;because the processes we wish to study have had some time to leave detectable genomic footprints, but have not yet removed the material we want to investigate. Second, the neo-sex chromosome is homologous to the sex chromosomes of mammals, which makes it possible – for the first time – to study mammalian X gene homologs in a novel, avian Z-linked environment where females are the heterogametic sex (ZW), and thus to draw direct parallels over the avian ZW–mammalian XY boundary.

We are now exploring this remarkable neo-sex chromosome system to understand the evolution of sex chromosomes in terms of recombination cessation and gene content - this includes assembling the genome of one of our main Sylvioidea study species; the great reed warbler. Next we will use RNA-seq data from males and females to evaluate the evolution of sex-biased expression and dosage compensation (the process whereby the gene expression of the heterogametic sex is compensated for the loss of one functional gene copy). This also includes understanding whether incomplete dosage compensation (of neo-sex genes) disrupts critical co-expression networks, as has been suggested but not proved.

Finally, we plan to explore our unique 30–year ecological dataset and rich collection of DNA samples of the great reed warbler to test the widely accepted but poorly supported sexual antagonism hypothesis suggesting that sexually antagonistic mutations (i.e. mutations beneficial to one sex but unfavourable to the other) accumulate on the SCs and drive their evolution. If funding allows, predictions of the sexual antagonism hypothesis will also be tested in a species rich the Sylvioidea phylogeny by using DNA-seq data from several species.

Summary of main research objectives:

  • To understand sex chromosome evolution in terms of recombination cessation, degeneration and gene content.
  • To understand the evolution of sex-biased gene expression and dosage compensation, and whether incomplete dosage compensation disrupts critical gene co-expression networks.
  • To understand the interplay between sex chromosomes and sexual conflicts by studying whether sexually antagonistic mutations accumulate on sex chromosomes, and whether sexual conflicts drive sex chromosome evolution.

Recent publications

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Great Reed Warbler
Great Reed Warbler