Origin and evolution of the sexes and reproductive systems: novel insights from a distant eukaryotic lineage

Project Information

SEXSEA

Grant agreement ID: 638240

DOI

10.3030/638240

Project closed

EC signature date 20 May 2015

Start date 1 June 2015

End date 31 May 2020

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 1 498 694,89

EU contribution

€ 1 498 694,89

Coordinated by

CENTRE NATIONAL DE LA RECHERCHE SCIENTIFIQUE CNRS
France

Periodic Reporting for period 4 - SEXSEA (Origin and evolution of the sexes and reproductive systems: novel insights from a distant eukaryotic lineage)

Reporting period: 2019-12-01 to 2020-05-31

Summary of the context and overall objectives of the project

Sexual reproduction is an extraordinarily widespread phenomenon that assures the production of new genetic combinations in nearly all eukaryotic lineages. Although the core mechanisms of sexual reproduction (meiosis and syngamy) are highly conserved, the control mechanisms that determine whether an individual is male or female are remarkably labile across eukaryotes. In genetically controlled sexual systems, gender is determined by sex chromosomes, which have emerged independently and repeatedly during evolution. Sex chromosomes have been studied in only a handful of classical model organism, and empirical knowledge on the origin and evolution of the sexes is still surprisingly incomplete. The goal of our project is to exploit the remarkable richness of sexual characteristics of the brown algae to gain novel insights into the functional and evolutionary interactions between the sex chromosomes and key eukaryotic reproductive and life cycle features.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

Using resources generated by our group as part of the Ectocarpus genome project (Cock et al., 2010 Nature), we identified, mapped and characterized the male and female sex chromosomes. The sex-determining regions of these UV chromosomes share features those of XY and ZW systems but also exhibit specific evolutionary characteristics (Ahmed et al., 2014 Current Biology). In addition, analysis of the pseudo-autosomal (PAR) region of the sex chromosomes identified several unique structural and evolutionary features, including clusters of recently evolved, sporophyte-
expressed genes (Luthringer et al., 2015 Molecular Biology and Evolution). Our results indicated that the evolution of the PAR in haploid systems is influenced by differential selection pressures in males and females acting on alleles that are advantageous during the sporophyte generation of the life cycle. A large RNA-seq dataset was generated to analyse the transcriptional network involved in sex determination and differentiation and we showed that both female- and male-biased genes are evolving rapidly, at least partly as a result of adaptive evolution, and that rates were similar for the two sexes. This contrasts with XY (or ZW) systems, where male (or female)-biased genes evolve more rapidly. The patterns of sex-biased gene expression in Ectocarpus are consistent both with predicted characteristics of UV (haploid) sexual systems and with the distinctive aspects of this organism’s reproductive biology, that involves separate sexes at the haploid stage of the life cycle and low levels of sexual dimorphism. More recently, these analyses have been extended to additional brown algal species to understand sex chromosome evolution and sex differentiation across this group. This work has provided the first analysis of gene traffic in a haploid UV system and has identified several features of general relevance to the evolution of sex chromosomes (Lipinska et al., 2017 Genome Biology). Sex-markers for kelps are being used as valuable tools for algal cultivation practices and algal breeding programs.
Our further analysis using more brown algal sex chromosomes will not only reveal the fundamental forces that shape sex chromosome evolution in the scope of the tree of life, but will also uncover the mechanisms underlying important evolutionary transitions between major reproductive and life cycle modes and shed new light on the origin and evolution of the sexes.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

- Full characterisation of the sex chromosomes of a model organism from an important multicellular eukaryotic lineage
- Identification of a candidate master sex determination gene
- Identification of the evolutionary forces affecting the evolution of haploid sex chromosomes
- Validation and substantial expansion of existing models for the evolution of the sexes
- Identification of sex-markers for algae with important economic interest (kelps), which will not only facilitate seaweed breeding programs but also represent useful tools for population and demography studies
- identifications of the first macroalgal developmental regulators using forward genetics
- identification of major life cycle regulators of ancient origin

Release of haploid spores in the brown alga Ectocarpus sporophyte.