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Report

Teaser, summary, work performed and final results

Periodic Reporting for period 1 - SexDiff (Sex differences in expression in the shared genome)

Teaser

Summary

SEX DIFFERENCES IN EXPRESSION IN THE SHARED GENOME
Males and females in many animals are strikingly different in behaviour, physiology, shape and form. In humans, rates of ageing and disease incidence vary markedly between the sexes. Moreover, sex differences in response to medical therapies and treatments have recently become an area of major biomedical concern. Because there are very few genes that are expressed in just one sex, sex differences are largely a product of contrasting patterns of gene expression between males and females. Despite their ubiquity and clear biomedical importance, the evolutionary causes of sex differences in gene expression remain essentially unknown and pose a fundamental problem for biologists: How do sex differences evolve given that the sexes largely share the same genome?

My research addresses this fundamental question using three approaches: (1) a data-driven large-scale phylogenetic approach (2) capitalizing upon natural variation in male reproductive behavior in species with and without distinct male morphs and (3) genetic manipulation of chromosomes in Drosophila melanogaster.

The results from this project will create comprehensive understanding of whether males and females differ in how gene expression is regulated and evolves. This broad research addresses the genomic basis of sex differences and has important implications for medical, developmental and evolutionary studies.

Work performed

To understand how sex differences evolve, my project analysed a number of complementary gene expression datasets. These datasets were chosen to encompass different aspects of my overarching aim to understand how sex differences evolve from a shared genome. Datasets included (i) six different bird species that varied in their mating system, (ii) a species of fish where males come in three forms which have different mating tactics, and finally two different fruit fly datasets, (iii) one involving inbred lines and (iv) the other involving chromosome substitutions and genetic crosses. I performed a range of analyses and measured how genetically correlated males and females are in the expression of different types of genes, expression levels of different types of genes, rates of evolution in gene expression and the relationship between gene expression and male behaviour.

Overall, I found that males and females regulate gene expression differently and this largely overcomes the constraint imposed by sharing the same genome. Furthermore, sex chromosomes accentuate sex differences by controlling expression of genes across the whole genome. I also found that high quality in males was controlled by the expression of many genes with small effect, rather than a few key genes with large effect. Together, this research helps to explain how profound differences between males and females can evolve and further adds to our understanding of how males and females can achieve different evolutionary optima.

The datasets produced during this fellowship are publicly available, providing exploitation by future researchers. They include (i) and RNA-seq dataset of ocellated wrasse gonadal gene expression (www.ncbi.nlm.nih.gov/sra) BioProject ID PRJNA344726 (ii) male reproductive phenotypes of a selection of lines from the Drosophila Genetic Reference Panel (https://doi.org/10.5061/dryad.s3mr73b) and (iii) the code for transcriptome assembly and data visualisation are available on github (https://github.com/beckydean).

This project has resulted in publications in Nature Communications, Molecular Ecology, American Naturalist and Evolution, which have been well cited to date with >100 citations. I have presented at international conferences, including being an invited speaker at a specialist conference organised by the Centre for Ecology and Evolution in London called â€œWar and Peace - the dynamics of evolutionary conflictâ€. My research has been more widely disseminated through an exhibition at the Grant Museum in London called â€œNatural Creativity: Sex and Trickeryâ€ which I co-organised along with the artist, Clara Lacy. This exhibition highlighted examples of reproductive tactics and deceit in the natural world. The Grant Museum receives over 4000 visitors per month and by showcasing my research on the ocellated wrasse through art, we potentially reached around 8000 members of the public with this outreach activity.

Final results

The main aim of this project was to explore how sex differences evolve from a shared genome. Sitting at the interface of phylo-genomics, experimental genetic manipulations and behavioural ecology, my project was uniquely placed to achieve this aim in a novel way, providing progress beyond the state of the art.

The novelty lies both in the conceptual advances and combination of comparative and experimental approaches. For example by developing a new statistical approach to measure gene expression correlation between the sexes, we synthesize this quantitative genetics approach with studies of gene expression. Likewise, combining behavioural ecology with genomics enabled us to understand how different forms of sexual selection shape the male and female genome.

The primary value of the results generated during this fellowship lies within the scientific community, with particular relevance for medical research, sexual selection theory and understanding phenotypic evolution. Understanding sex differences have been identified as a key aim for Horizon 2020 and as such will impact upon European society. The need for sex to be taken into account in clinical medical research has become a topic of recent concern, both within Europe and worldwide.