Abstract
Anopheles gambiae and An. coluzzii, the two most important malaria vectors in sub-Saharan Africa, are recently radiated sibling species that are reproductively isolated even in areas of sympatry. In females from these species, sexual transfer of male accessory gland products, including the steroid hormone 20-hydroxyecdysone (20E), induces vast behavioral, physiological, and transcriptional changes that profoundly shape their post-mating ecology, and that may have contributed to the insurgence of post-mating, prezygotic reproductive barriers. As these barriers can be detected by studying transcriptional changes induced by mating, we set out to analyze the post-mating response of An. gambiae and An. coluzzii females captured in natural mating swarms in Burkina Faso. While the molecular pathways shaping short- and long-term mating-induced changes are largely conserved in females from the two species, we unravel significant inter-specific differences that suggest divergent regulation of key reproductive processes such as egg development, processing of seminal secretion, and mating behavior, that may have played a role in reproductive isolation. Interestingly, a number of these changes occur in genes previously shown to be regulated by the sexual transfer of 20E and may be due to divergent utilization of this steroid hormone in the two species.
Highlights
Overall malaria mortality rates have significantly declined since 2010 due to increased prevention and control measures, Sub-Saharan Africa continues to carry a disproportionately high share of the global malaria burden, bearing more than 90% of the 212 million cases and of the estimated 429,000 deaths caused by Plasmodium parasites[1]
This hormone is a potent regulator of gene transcription during both juvenile development and oogenesis in adults[13,14], and in some anopheline species is synthetized in the male accessory glands (MAGs) and transferred during mating to the female atrium together with other seminal secretions embedded in a gelatinous structure named the mating plug[15,16,17,18,19,20]
We report the first data on the transcriptional changes induced by mating in An. gambiae and An. coluzzii females captured in natural mating swarms from Burkina Faso
Summary
Overall malaria mortality rates have significantly declined since 2010 due to increased prevention and control measures, Sub-Saharan Africa continues to carry a disproportionately high share of the global malaria burden, bearing more than 90% of the 212 million cases and of the estimated 429,000 deaths caused by Plasmodium parasites[1]. These species are sympatric in West and Central Africa[4,5], but differ in their larval ecology, with An. gambiae being more adapted to temporary rain-dependent and An. coluzzii to permanent anthropogenic breeding sites[6,7,8,9] Due to their major role as malaria vectors, the two species are the target of several studies aimed at developing novel approaches for the control of disease transmission in sub-Saharan Africa, with the view to complement or strengthen current insecticide-based control methods[10,11,12]. Our results corroborate previous data obtained under laboratory conditions[18,22], allow the identification of factors potentially important for mating, fertility and reproductive success in each species, and provide novel insights on inter-specific differences that shape their reproductive ecology and may help unravel the mechanisms of their reproductive isolation
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