Dissecting transcriptome intraspecific variation and sex-biased expression in Anopheles arabiensis

Malaria transmission in the anophelines is intertwined with adaptation to a changing environment. This adaptation can occur via modification of expression levels. Nevertheless, the magnitude and functional patterns of intraspecific transcriptional variation in the anophelines, including that of sex-biased genes, which crucially underlie sex-specific traits related to malaria transmission, remain understudied. We sequenced the female, male, and larval transcriptomes of three populations of Anopheles arabiensis from Burkina Faso. One-third of the genes were differentially expressed in at least one sample type in at least one population, with females showing the largest differentiation. A sizable fraction of polymorphic genes were related to insecticide resistance in a sample type-specific manner. Chromosomes harboring polymorphic inversions were not found enriched for variable genes, and regardless the sample type, the X chromosome was depleted of them compared to the autosomes. Further, variation in sex-bias across populations did not substantially differ between male- and female-biased genes, except for male-limited expressed genes, which were more variable than their female counterparts. In fact, both among males and among females of different populations, female-biased genes were more variable than male-biased genes. Our findings suggest a larger effect of the X chromosome on the evolution of gene expression in An. arabiensis than the autosomes, and a differentiation of the anopheline transcriptome less markedly driven by female adaptive evolution than previously proposed. The uncovered adaptive potential of transcriptional variation in An. arabiensis indicates that efforts to mitigate malaria transmission through insecticide-based interventions in this species might severely hindered.