X-chromosome driven speciation through testes-expressed genes: comparative population genomics meets scRNA analysis in primates

ongoing

Primate X chromosomes evolve extraordinary fast and are also tightly associated with the establishment of reproductive barriers between emerging species. The hypothesis of this proposal is that genetic conflicts between the X chromosome and the rest of the genome during spermatogenesis cause rapid X chromosome evolution and build reproductive barriers. Genetic conflicts for transmission to haploid gametes, called meiotic drive, will cause non-adaptive evolution, which is expected to be countered by other genomic elements that will then be under selection. Such an arms race is expected to lead to a very rapid evolution of the X chromosome and a fast accumulation of incompatibilities between isolated populations, leading to speciation. The goal of the project is to identify the underlying mechanisms and the genes responsible for meiotic drive using primates as the study system. A priori candidate processes include X-linked genes under repeated fast evolution with a focus on genes targeted by pachytene piRNAs and on ampliconic genes. Population genomics analysis will generate specific hypotheses that will then be tested by following expression of candidate genes during spermatogenesis through scRNAseq, and validate findings by ultrasensitive, in situ, staining of single transcripts and immunohistochemistry. Finally, the behaviour of key genes and processes will then be investigated in incipient speciation events. Specifically, 850 individuals of 250 species of primates with full genome data will be analysed for candidate genes on the X chromosome. These genes will be investigated in large scale comparative scRNA sequencing analyses of >10,000 individual testicular cells from 14 primate species, including all great ape species, thus allowing expression trajectories through spermatogenesis to be inferred and followed up in functional experiments. The success criterion is to report on primate speciation genes together with their biological mode of action.