A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior

Abstract

The male accessory glands (MAGs) of many insect species produce and secrete a number of reproductive proteins collectively named Acps. These proteins, many of which are rapidly evolving, are essential for male fertility and represent formidable modulators of female postmating behavior. Upon copulation, the transfer of Acps has been shown in Drosophila and other insects to trigger profound physiological and behavioral changes in females, including enhanced ovulation/oviposition and reduced mating receptivity. In Anopheles gambiae mosquitoes, the principal vectors of human malaria, experimental evidence clearly demonstrates a key role of MAG products in inducing female responses. However, no Acp has been experimentally identified to date in this or in any other mosquito species. In this study we report on the identification of 46 MAG genes from An. gambiae, 25 of which are male reproductive tract-specific. This was achieved through a combination of bioinformatics searches and manual annotation confirmed by transcriptional profiling. Among these genes are the homologues of 40% of the Drosophila Acps analyzed, including Acp70A, or sex peptide, which in the fruit fly is the principal modulator of female postmating behavior. Although many Anopheles Acps belong to the same functional classes reported for Drosophila, suggesting a conserved role for these proteins in mosquitoes, some represent novel lineage-specific Acps that may have evolved to perform functions relevant to Anopheles reproductive behavior. Our findings imply that the molecular basis of Anopheles female postmating responses can now be studied, opening novel avenues for the field control of these important vectors of human disease.reproduction ͉ malaria ͉ mating ͉ Acp ͉ seminal fluid

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

“…A gene encoding a putative andropin-like AMP (AGAP009429, also found in the A. gambiae male accessory glands; see ref. 13) was ''switched on'' at this early time point, and remained highly expressed at 6 h (Table S1).…”

Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: Potential tools for control of female feeding and reproduction

“…Further investigation of mosquito mRGPs identified in this study, and in a recent study of An. gambiae (Dottorini et al, 2007), may provide targets for controlling the reproductive output of these important disease vectors. Furthermore, promoters of genes expressed exclusively in the male reproductive accessory glands can be used to drive expression of a number of useful constructs.…”

“…aegypti mRGPs 3.5.A Ae. aegypti mRGP protein classes-One striking feature of male mRGPs is the conservation of protein classes across a wide range of organisms (Mueller et al, 2004;Clark and Swanson, 2005;Braswell et al, 2006;Collins et al, 2006;Davies and Chapman, 2006;Poiani, 2006;Dottorini et al, 2007). The 63 putative Ae.…”

Anopheles gambiaemales produce and transfer the vitellogenic steroid hormone 20-hydroxyecdysone to females during mating

“…In Anopheles, mating-induced changes in female mediated by MAG secretions have also been demonstrated (45,46), but the mediators remained uncharacterized. A recent genome-wide blast analysis has identified Anopheles Acps specifically expressed in MAGs and possibly involved in the modulation of post-mating effects in Anopheles females (47). Thus, in association with Acps, the steroid hormone 20E offered by the male may play a crucial role in eliciting post-mating physiological changes in A. gambiae females.…”