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Evolutionary Consequences of Arrested Genomic Conflict in Asexual Species

Periodic Reporting for period 3 - No Sex No Conflict (Evolutionary Consequences of Arrested Genomic Conflict in Asexual Species)

Reporting period: 2023-04-01 to 2024-09-30

Genomic conflicts are an important motor for evolutionary change and innovation. Genomic conflicts are also expected to be frequent sources of phenotypic maladaptation, as the optima targeted by different genetic elements differ from the values that maximize fitness of the carriers ). Finally, genetic conflicts play an increasingly recognized role in human disease with multiple pathologies believed to arise as a consequence of disturbed conflict resolution between parts of an individual’s genome. Our project leverages the fact that all forms of genetic conflict disappear in lineages that transition from sexual to asexual reproduction. Under asexuality, all genetic elements are transmitted together, meaning their evolutionary interests become aligned. Asexual species further consist solely of females, meaning that there is no more selecting acting on male phenotypes. By comparing different asexual species to their sexual relative allows us to globally assess the contribution of intra- and inter-genomic conflicts to phenotype and genome evolution in sexual species.

Our specific objectives are to study how genes featuring sex-biased expression in different tissues of sexual species shift their sex-specific expression patterns in asexual species. Of particular interest are genes on the X-chromosome, because males in sexual species have a single X while females have two, which has resulted in the establishment of dosage compensation mechanisms acting in males. Furthermore, we will study the evolution of centromeres, the regions of the chromosomes that mediate the movement of chromosomes at meiosis. Alternative centromere versions are expected to compete in outbreeding, sexual species, but such competition is expected to be rare or absent in asexual ones. Finally, we will test whether transposable elements, a type of intragenomic parasite, evolve to be more benign in the absence of conflict.
We have finished the generation of the key resources and most of the raw data needed for the planned projects. The resources include notably the annotated genome assemblies for the 10 Timema species where we have achieved chromosome-level resolution for 8 of the 10 species, with telomere-to-telomere assemblies for the majority of chromosomes in each species. We annotated approximately 30’000 genes in each species and are currently annotating tandem repeats and specific transposable element insertion sites. We have made significant progress on whole genome alignments across the 10 species and are identifying 1:1 orthologous gene sets.
We have also generated and quality checked the extensive RNAseq datasets required for WP1 and WP2 and are proceeding with the detailed data analyses for these work packages. We have tested different custom antibodies against the centromere-binding protein CenH3, and are currently waiting for the first sequencing results obtained from ChIP-seq and CUT&RUN techniques. We have also developed additional custom antibodies for proteins from the inner and outer kinetochore of stick insects which will be used to describe the meiosis phenotype in stick insects.
We have been making progress on all four planned workpackages. Regarding WP1 and WP2, we are using the generated transcriptome data in a combinatorial approach of population genetics and quantification of sex-biased gene expression in sexual and asexual species to identify genes subject to sexual antagonism. We will further investigate the extent and consistency of dosage compensation and sex-bias of X-linked genes across the ten Timema species and assess if sexual conflict influences the extent of dosage compensation and sex-biased expression.
Regarding WP3, we will use the ChIP-seq/CUT&RUN data of centromere sequences and 1:1 orthologs of centromere-binding proteins for comparisons between sexual and asexual Timema species. The finding of any consistent difference between sexual and asexual species would result in major progress for our understanding of the evolution of centromere and centromere-binding proteins.
Using the generated genome assemblies, we are identifying individual copies of different TEs in each species and map specific TE deletions and insertions onto the Timema phylogeny. This will allow us to compare the number of de novo insertions between species with different reproductive modes and infer evolutionary instances of reduced TE activity and rates of TE turnover. In combination, these data will allow us to directly identify changes in the evolutionary dynamics of TEs in asexual species where there is no conflict between TEs and their host.