Prevalence and Influence of Sexual Antagonism on Genome Evolution

Project Information

SexAntag

Grant agreement ID: 715257

DOI

10.3030/715257

Project closed

EC signature date 19 October 2016

Start date 1 March 2017

End date 28 February 2022

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 1 444 394,00

EU contribution

€ 1 444 394,00

Coordinated by

INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA
Austria

Periodic Reporting for period 4 - SexAntag (Prevalence and Influence of Sexual Antagonism on Genome Evolution)

Reporting period: 2021-09-01 to 2022-02-28

Summary of the context and overall objectives of the project

Males and females display profound differences in phenotype, physiology and behaviour, and understanding the evolutionary forces driving this diversity is a long-standing goal in evolutionary biology. Sexually antagonistic conflict, resulting from traits and/or mutations that are beneficial to one sex but harmful to the other, can in theory lead to strong dimorphism, and has been invoked to explain many evolutionary features, including the large number of genes that acquire sex-biased expression. Quantifying it, however, has proved difficult. A key goal of the project is to characterize the prevalence and role in genome evolution of sexual conflict and sex-specific selection.
Species groups with both sexual and asexual populations offer a promising approach to understand sex-specific selective pressures, as they allow for a direct comparison of gene expression when selection occurs 1⁄2 of the time in females and 1⁄2 of the time in males (in sexual species), versus a female-only selective regime (asexual species). We tested the hypothesis that release from sexual conflict should shape the expression of ancestrally sex-biased genes, especially on sex chromosomes, in newly asexual populations of the brine shrimp Artemia. Our results show that while sex-biased genes do have unusually high rates of divergence, this pattern is not specific to asexual lineages, likely reflecting the young origin of asexuality in this group. We further looked at the role of sex-specific expression in shaping gene evolution after whole genome duplications in carps and mercuries plants. We found that many duplicated genes have had each copy co-opted for one sex, in agreement with predictions made under sexually antagonistic models. These results emphasize the unique evolutionary patterns of genes with sex-specific functions in a variety of contexts, consistent with them being under an unusual selective regime.
While we are addressing fundamental questions, the idea that each sex cannot reach their own optimum due to selection in the opposite sex has important implications. For instance, genetic variants that cause disease in one sex could be maintained in the population, as long as they benefit the other sex. Understanding the prevalence of sex-specific selective pressures will be essential for estimating this so called "gender load".

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

Comparative transcriptomics of sexual and asexual species (AIM 1): We sequenced RNA from various tissues of sexual and asexual populations. RNA-seq reads of each species were pooled and assembled into high quality transcriptomes,. We detected sex-biased genes (genes expressed primarily in either females or males) in each of the sexual species. We then compared sexual and asexual lineages to understand how asexuality affects gene expression (Huylmans et al., Proc. B, 2021).

Genome assembly of A. sinica and identification of the Z-chromosome (AIM 2): We chose the sexual A. sinica for deep genome sequencing with Illumina, PacBio long and HiC reads. Our current assembly has an N50 of 67Mb and a BUSCO score of 92%, with 86% of the assembly falling into the largest 21 scaffolds (which correspond to the 21 chromosomes). We showed detected a small region that is fully differentiated between the Z and W in all sexual and asexual Artemia lineages. We also estimated genetic differentiation across the genome between males and females of A. Sinica (AIM III), and found a large young "stratum" on the pair of sex chromosomes.

Dosage compensation of the Z-chromosome (AIM 2): We investigated the expression of Z-specific genes in the American species A. franciscana and in A. sinica. We used male and female RNA-seq to infer sex-specific patterns of expression on the Z and the autosomes. Z-linked genes were expressed at very similar levels in the two sexes (they were "dosage compensated"; Huylmans, Toups, et al., 2019).

Characterization of rare males and their progeny (AIM 2): We obtained rare males from A. partenogenetica Aibi Lake, as well as 25 males and 23 asexual females resulting from a cross between one of them and an A. kazakhstan female. The F1 males were backcrossed to A. Kazakhstan females, yielding an F2 progeny that consisted of males, asexual females, and putative sexual females, of which sexual and asexual females were DNA-sequenced (as was the original rare male).

Population genomics (AIM 3): We used the extensive RNA-seq data obtained for AIM 1 to estimate Fst between males and females, in order to search for putative loci under sexual antagonism. While many loci with elevated Fst were found, they were mostly located on the sex-chromosomes, and corresponded to non-recombining but undifferentiated parts of the sex-determining region.

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)

* Sex chromosome evolution: We showed that the ZW pair of sex chromosomes is ancestral to the Artemia genus (Elkrewi et al., under review), but that parts of it lost recombination independently in the American and Eurasian lineages, making this system a perfect model for investigating young and older sex-linked regions.

* Dosage compensation on the Z-chromosome: We found that Z-specific genes are expressed at similar levels in males and females, supporting the presence of global dosage compensation (Huylmans et al., GBE, 2019; Elkrewi et al., under review), an uncommon occurrence in ZW systems.

* Evolution of asexuality: Only a small set of genes shows convergent shifts in expression in asexuals, suggesting that the switch to asexuality may involve few molecular changes to the meiotic program. Asexual females have neither a feminized nor masculinized transcriptome, contrary to theoretical expectations (Huylmans et al. 2021).

* A role for the Z chromosome in the transmission of asexuality: We use backcrossing experiments between a rare male (derived from an asexual lineage) and sexual females to obtain evidence for the presence of a locus controlling asexuality on the Z-chromosome (Elkrewi et al., under review), highlighting the interplay between sex determination and asexual reproduction.

* A role for sex-specific selective pressures in shaping polyploid genomes: We showed that after a whole genome duplication, duplicated genes often become “sexually subfunctionalized”, i.e. each copy is coopted by one sex, in agreement with predictions made for the resolution of sexual conflict (but previously only described in the context of individual gene duplications; Toups et al., under revision; Gammerdinger et al., under revision) .

* Evolution of the t-haplotype: We characterized this mouse selfish genetic element at the genomic level and transcriptomic level (Kelemen & Vicoso, 2018, Kelemen et al., Proc. B, 2022), and inferred highly dynamic patterns of evolution, with both loss and gain of expression as well as recruitment of gene duplicates from other chromosomes.

shared ZW pair of Artemia-characterized: sex-specific patterns of genomic coverage, genetic variatio