Sex chromosome evolution under male- and female-heterogamety

In humans, a pair of sex chromosomes, the X and the Y, is responsible for generating males (which carry one X and one Y) and females (which carry two X-chromosomes). Understanding where these sex-chromosomes came from, and how they became so specialized, has been the topic of extensive research, from which two main results have emerged: 1. The Y is a degenerated version of the X, and has lost most of its gene content. 2. Genes on the X have modified patterns of expression, to compensate for the missing genes on the Y (missing a copy of many genes would otherwise be damaging to males). This process is called dosage compensation, and has been found in several species with degenerated Y- chromosomes. While many animals have X and Y-chromosomes, other sex chromosomes exist: in birds, for instance, females carry the sex-specific chromosome (in this case it is called a W rather than a Y). In such female-heterogametic species, females are ZW, and males ZZ. Since theories of XY evolution should also apply to ZW systems, we expect W- chromosomes to be degenerated, and Z-chromosomes to be compensated. To some extent this is true, and the W of birds resembles the mammalian Y. However, both W-degeneration and Z-compensation are often strongly reduced (or absent) in ZW species, and the reason for such a drastic difference is unknown. Several theories have been put forward, many of them focusing on the direct consequences of female- versus male-heterogamety. For instance, females could be sturdier and not require dosage compensation of the Z. However, a minority of ZW species is in fact compensated, and some XY species are not, suggesting a more complicated scenario. Here, we will test the hypothesis that evolutionary forces that act differently on the two sexes, rather than direct differences between males and females, lead to different dynamics of evolution for XY and ZW chromosomes. In particular, both mutation and sexual selection, two crucial parameters, can be more frequent in males. This can lead to different expectations for the degeneration of the female-specific W and the male-specific Y, and the consequent compensation of the X- and Z-chromosomes. We will use theory, experiments and data analysis to investigate this issue. We will generate new RNA-seq datasets to obtain gene expression profiles for males and females of XY and ZW species, and combine them with published DNA and RNA data, to systematically quantify how fast sex chromosomes evolve, and to which extent they have acquired dosage compensation. Obtaining a fuller picture of the variation within and between these male- and female-heterogametic species will allow us to test the different theories that could account for the differences between them. This will not only shed light on why the evolution of XY and ZW systems follows different paths, but also provide new insights into the processes driving genome evolution.

In species that have separate sexes, sex-determination can be environmental, or genetic. In the case of genetic sex-determination, a pair of sex chromosomes, such as the human X- and Ychromosomes, is responsible for the generation of males (which carry one X and one Y) and females (which carry two X-chromosomes). The origin and evolution of sex chromosomes have been the topic of extensive research. Most of this has focused on the XY systems of the most commonly used model animals: mammals, fruit flies, and nematode worms. Two main themes have emerged from this research: 1. The Y chromosome is a degenerated version of the X, and has lost most of its gene content. 2. The X chromosome adjusts to the loss of gene content of the Y by acquiring mechanisms of dosage compensation that adjust the gene expression levels of X-linked genes that no longer exist on the Y. Another type of sex chromosomes exists: in birds, for instance, females carry the sex- specific chromosome (in this case it is called a W-chromosome rather than a Y). In such female-heterogametic species, females are therefore ZW, and males ZZ. Since the theories used to explain XY evolution should also apply to ZW systems, we expect W-chromosomes to be degenerated, and Z-chromosomes to be compensated. To some extent this is true, and the W-chromosome of birds resembles the mammalian Y-chromosome. However, both W- degeneration and Z-compensation are often strongly reduced (or even absent) in ZW species, and the reason for this difference is unknown. In this project, we combined genome sequencing and gene expression analyses to investigate the evolution of ZW chromosomes. We did this in two very different groups: moths (insects) and schistosome parasites (trematode worms that cause snail fever in humans). We first focused on the history of their sex chromosomes, by comparing them to those of other related species. We showed that the Z-chromosome of moths has likely been around for over 200MY, making it one of the most ancient Z-chromosomes ever described. On the contrary, the ZW pair of schistosome parasites is still fairly young. We then looked at how genes on these Z-chromosomes are expressed, to see if they are balanced between males and females or not. Contrary to what had been previously described, we found that, in both cases, some compensation was occurring. These results increased our understanding of the evolution of ZW systems, but also raise many new questions about what drives some organisms to have complicated mechanisms of dosage compensation while others do not.