Molecular and cellular components of the mating machinery in Anopheles gambiae females

Abstract

Anopheles gambiae mosquitoes are the principal vectors of malaria. A major determinant of the capacity of these mosquitoes as disease vectors is their high reproductive rate. Reproduction depends on a single insemination, which profoundly changes the behavior and physiology of females. To identify factors and mechanisms relevant to the fertility of A. gambiae, we performed a comprehensive analysis of the molecular and cellular machinery associated with copulation in females. Initial whole-body microarray experiments comparing virgins with females at 2 h, 6 h, and 24 h after mating detected large transcriptional changes. Analysis of tissue localization identified a subset of genes whose expression was strikingly regulated by mating in the lower reproductive tract and, surprisingly, the gut. In the atrium of virgin females, where the male seminal fluid is received, our studies revealed a ''mating machinery'' consisting of molecular and structural components that are turned off or collapse after copulation, suggesting that this tissue loses its competence for further insemination. In the sperm storage organ, we detected a number of mating-responsive genes likely to have a role in the maintenance and function of stored sperm. These results identify genes and mechanisms regulating the reproductive biology of A. gambiae females, highlighting considerable differences with Drosophila melanogaster. Our data inform vector control strategies and reveal promising targets for the manipulation of fertility in field populations of these important disease vectors.mosquito ͉ post-mating response ͉ reproduction ͉ microarray ͉ reproductive tract

Sexual transfer of the steroid hormone 20E induces the postmating switch in Anopheles gambiae

“…The discovery that male-transferred 20E is a key regulator of female reproductive biology in An. gambiae adds to the myriad of effects that this hormone exerts on insect adult physiology (2,3,(17)(18)(19)(20)(21)(22)(23). Interestingly, the steady decline of 20E levels in the atrium during the first day after copulation (17) is reminiscent of the process of mating plug digestion, which is completed in a similar time frame (5)(6)(7)16).…”

“…To gain better insight into the molecular link between the postmating transcriptional and morphological changes and the behavioral and physiological shift induced by copulation (3,17,25), we initially performed an indepth transcriptional analysis of the female lower reproductive tract (LRT), comprising the atrium and the spermatheca. To identify the molecular pathways specifically regulated in these female reproductive tissues, we analyzed three time points (3,12, and 24 h post mating; hpm) that would capture transcriptional changes occurring within a broad time window after copulation.…”

“…To gain better insight into the molecular link between the postmating transcriptional and morphological changes and the behavioral and physiological shift induced by copulation (3,17,25), we initially performed an indepth transcriptional analysis of the female lower reproductive tract (LRT), comprising the atrium and the spermatheca. To identify the molecular pathways specifically regulated in these female reproductive tissues, we analyzed three time points (3,12, and 24 h post mating; hpm) that would capture transcriptional changes occurring within a broad time window after copulation. These analyses identified 708 genes induced and 412 genes repressed by mating across the different time points [P < 0.05; false-discovery rate (FDR) corrected] (Dataset S1), unveiling a greater induction of transcription than of repression and a much larger transcriptional response than previously observed in the whole-female analysis, in which only 141 mating-regulated genes were identified (3).…”

“…Sex also increases the number of eggs developed after a blood meal and induces laying of mature eggs (2). Parallel to these modifications in postcopulatory behavior, the female reproductive tract undergoes significant morphological changes, possibly reflecting a switch from an insemination to an egg-laying requirement in these tissues (3). The evolutionary forces behind monandry in An.…”

Morphological and morphometrical assessment of spermathecae of Aedes aegypti females

“…In spite of such high output, Ae. aegypti females are restricted to a single mating event, sufficient to acquire enough sperm to fertilize a lifetime supply of eggs (Rogers et al 2008). How mosquito females are capable of maintaining live gametes for several days or weeks remains unknown.…”