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Evolution of dosage compensation on recently evolved sex chromosomes

Reference	BB/P009808/1
Principal Investigator / Supervisor	Professor Dmitry Filatov
Co-Investigators / Co-Supervisors
Institution	University of Oxford
Department	Plant Sciences
Funding type	Research
Value (£)	363,625
Status	Completed
Type	Research Grant
Start date	01/07/2017
End date	28/02/2021
Duration	44 months

Abstract

This project aims to shed light on the very early stages in evolution of dosage compensation. It will take advantage of the recent origin of heteromorphic sex chromosomes in plant Silene latifolia, and the presence of nascent dosage compensation at a fraction of the X-linked genes in this species, to unravel the evolutionary forces and processes driving evolution of dosage compensation in this species. The particular strength of this system is the availability of congeneric non-dioecious species representing the ancestral state without sex chromosomes, as well as closely related dioecious species with the sex chromosomes. This makes it possible to compare expression of sex-linked genes in different dioecious and non-dioecious species to analyse the change in gene expression over time once genes become X- and Y-linked. We will use this powerful system to address the following questions central to our understanding of evolution of dosage compensation: q1) How long does it take dosage compensation to evolve at the particular X-linked genes once their Y-linked gametologs become non-functional? q2) Does up-regulation of X-linked genes occur specifically in males or in both sexes, resulting in sexual conflict for gene expression? q2a) If there is such sexual conflict for gene expression, how long does it take to settle by secondary modifications? q3) Do dosage compensated genes cluster in the older part ('stratum') of S. latifolia X-chromosome, or they are distributed randomly across the chromosome? q3a) Are there any local effects - i.e. do genes adjacent to a dosage compensated gene on the genomic scaffold also tend to be dosage compensated? q4) Were recent shifts in gene expression of X-linked genes driven by positive selection at cis-regulatory regions? q5) Is there a pre-existing dosage compensation system in Silene, such as transcriptional buffering? q5a) If there is indeed a pre-existing system, can it fully account for the patterns of dosage compensation?

Summary

In most species, the development of an individual as a male or a female depends on the presence of sex chromosomes; for example, in humans, XY-individuals become males and XX-individuals develop as females. Similar situation exists in many other organisms where sex chromosomes evolved independently. Despite multiple independent origins, the properties of sex chromosomes are rather similar in different organisms, indicating the generality of evolutionary forces shaping sex chromosomes. In particular, Y-chromosome tends to lose functional genes and become genetically degenerate, while genes on the X-chromosome remain functional. For example, human Y-chromosome contains only a few dozen functional genes, which contrasts with about a thousand genes on the X-chromosome. The challenge is to understand the evolutionary forces shaping sex chromosomes and currently this is a very hot topic of on-going research. The loss of genes from Y-chromosome leaves only one functional copy of a sex-linked gene in males, while two copies of the gene are present in females (because they have two X-chromosomes). This creates disbalance between sexes and is likely to be detrimental in males, where not enough product is produced from sex-linked genes. To resolve this problem, fruit fly (Drosophila melanogaster) males increase yield from X-linked genes to compensate for lack of second copy of X-linked genes in males. Such 'dosage compensation' has also been discovered in other organisms, but the way they achieve the balance between sexes varies. For example, mammals increase expression of X-linked genes in both males and females and then switch off one of the X-chromosomes in females. How such dosage compensation systems evolve remains poorly understood, and 'old' sex chromosomes, such as those in mammals and Drosophila melanogaster, are hardly suitable to study evolution of dosage compensation. This project will take advantage of the recent evolution of sex chromosomes in plant Silene latifolia to study the early steps in evolution of dosage compensation system. Most species in genus Silene are hermaphroditic, while a few species, including Silene latifolia, evolved separate sexes relatively recently, allowing us to compare closely related species with different mating systems. Importantly, sex in S. latifolia is determined by sex chromosomes that evolved from scratch within only few million years. It has been demonstrated that Y-chromosome in this species has begun degenerating and nascent dosage compensations is present on the X-chromosome. The recent origin of S. latifolia sex chromosomes and the presence of congeneric species, representing the ancestral state without sex chromosomes, provide a unique opportunity to unravel the evolutionary forces and processes shaping the sex chromosomes at the early stages of their evolution.

Impact Summary

The primary impact of this research will be enhanced knowledge and understanding of a fundamental evolutionary process, namely the evolution of sex chromosomes. More specifically, it will significantly improve our understanding of the processes leading to evolution of dosage compensation. Understanding the forces driving genome evolution is the prime goal in evolutionary genetics field and sex chromosome evolution is one of the hottest topics in evolutionary biology. Thus, our results are likely to have fairly wide-reaching implications and its impact will be ensured by publication of the results in the top scientific journals and magazines. Beyond biology, this project will also help to attract more attention to science and promote popularisation of biology. All sorts of questions related to sexual reproduction prove particularly attractive for the general public and they often enjoy extensive media coverage. It will be relatively easy to explain the essence and interest of our work to the public in an accessible form as the question of why males and females are so different from each other is intuitively appealing and is of intrinsic interest to a non-specialist. We will take benefit of this with our outreach activities. The knowledge gained in this project will be communicated to the general public in a number of ways; for example in seminars at the University of Oxford Botanic Garden and through interactive displays at the University of Oxford Museum of Natural History. Advances in understanding will also be disseminated at secondary education level. These knowledge exchange activities will enrich societal understanding of the scientific method in general and of research in evolutionary biology in particular.

Committee	Research Committee C (Genes, development and STEM approaches to biology)
Research Topics	X – not assigned to a current Research Topic
Research Priority	X – Research Priority information not available
Research Initiative	X - not in an Initiative
Funding Scheme	X – not Funded via a specific Funding Scheme

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