Sex-specific transcriptome dynamics of <i>Anopheles gambiae</i> during embryonic development

Malaria-transmitting mosquitoes are extremely sexually dimorphic in their anatomy and behavior. Sex-specific gene expression in <i>Anopheles gambiae</i> is well studied in adult stages, but its onset during embryogenesis, apart from sex determination factors like <i>Yob</i>, remains largely unknown. Here, we report a comprehensive single-embryo transcriptome atlas of <i>A. gambiae</i> males and females to understand the earliest stages of establishing the sex-specific expression networks. Our data set reveals embryonic RNA isoform diversity, including a global shift toward distal alternative polyadenylation (APA) event sites during the maternal-to-zygotic genome transition. Sex-biased gene expression and alternative splicing are limited during embryogenesis, with most sex-specific patterns emerging postembryonically. X-chromosome dosage compensation (DC) is established shortly after zygotic genome activation, concomitant with direct binding of the master regulator protein SOA to X-linked promoters. In contrast to known DC regulators in other species, we did not find evidence for early high-affinity sites or distance-dependent patterns in <i>Anopheles</i> Instead, SOA binding and DC are dynamically specified on genes according to gene activity, where the most strongly expressed genes tend to show the strongest SOA binding. We propose that the <i>Anopheles</i> DC system represents an extreme case of a gene-by-gene regulatory mechanism that operates at the chromosome-wide level.