Dosage compensation and meiotic sex chromosome inactivation are maintained in the absence of selection

Abstract

Dosage compensation and meiotic sex chromosome inactivation (MSCI) are key mechanisms regulating gene expression from the X chromosome in male-heterogametic species. While the convergent evolution of these mechanisms is well-documented, their evolutionary fate under relaxed selection remains poorly understood. Here, we test whether dosage compensation and MSCI persist following three independent transitions to parthenogenesis in stick insects, where selection on male phenotypes is relaxed. Using rare males occasionally produced by parthenogenetic females, chromosome-level genome assemblies, RNA-seq from multiple tissues, and immunocytochemistry, we find that dosage compensation is fully conserved across all nine studied somatic tissues. This is even the case in the oldest, approximately 1.5 million years old all-female lineage, and for tissue-specific genes for which dosage variation is not expected to be very deleterious. Meiotic X inactivation in the germline is also conserved. Surprisingly however, expression data and cytological markers indicate that MSCI signatures are even stronger in parthenogenetic males, a pattern likely driven by prolonged autosomal transcription during meiosis. These results indicate that X-targeting dosage compensation and MSCI are highly stable over evolutionary time and may be maintained in all-female lineages by a combination of evolutionary constraint, pleiotropy, or very weak selection, whereas autosomal expression during meiosis shifts rapidly under relaxed selection. Significance StatementSex chromosomes are regulated by specialized mechanisms that balance gene expression between males and females in somatic tissues (dosage compensation) and silence the X chromosome during male meiosis (meiotic sex chromosome inactivation, MSCI). These processes are thought to decay when they become redundant, yet suitable systems to test this prediction are scarce. We studied rare males from parthenogenetic stick insect lineages that have been evolving without sex for up to 1.5 million years. Surprisingly, both dosage compensation and MSCI remain fully functional, despite relaxed selection. Instead, we find altered autosomal expression during meiosis. Our results reveal that sex chromosome regulation is evolutionarily stable and constrained, persisting even after the loss of its purpose.