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.

按蚊属昆虫的疟疾传播与其对多变环境的适应性紧密交织，这类适应性可通过调控基因表达水平实现。然而，按蚊属昆虫的种内转录变异（intraspecific transcriptional variation）——包括作为疟疾传播相关性别特异性性状关键基础的性别偏向基因（sex-biased genes）——的幅度与功能模式，迄今仍未得到充分研究。本研究对采自布基纳法索的3个阿拉伯按蚊（Anopheles arabiensis）种群的雌性、雄性及幼虫转录组（transcriptome）进行了测序。结果显示，至少在1个种群的至少1类样本中，三分之一的基因存在差异表达，其中雌性样本的表达分化程度最为显著。相当一部分多态性基因以样本类型特异性的方式与杀虫剂抗性（insecticide resistance）相关。未发现携带多态性倒位（polymorphic inversions）的染色体存在可变基因富集现象；且无论样本类型如何，X染色体上的可变基因丰度均低于常染色体（autosomes）。此外，不同种群间的性别偏向性差异在雄性偏向基因与雌性偏向基因之间并无显著差异，但雄性限制性表达基因（male-limited expressed genes）的变异程度高于其雌性对应基因。实际上，在不同种群的雄性或雌性个体中，雌性偏向基因的变异程度均高于雄性偏向基因。本研究结果表明，X染色体对阿拉伯按蚊基因表达进化的影响大于常染色体，且按蚊转录组的分化由雌性适应性进化驱动的程度较此前提出的更低。本次研究揭示的阿拉伯按蚊转录变异的适应性潜力表明，通过基于杀虫剂的干预措施防控该物种的疟疾传播，可能会受到严重阻碍。