Evolution of sexual traits influencing vectorial capacity in anopheline mosquitoes

Abstract

The availability of genome sequences from 16 anopheline species provides unprecedented opportunities to study the evolution of reproductive traits relevant for malaria transmission. In Anopheles gambiae, a likely candidate for sexual selection is male 20-hydroxyecdysone (20E). Sexual transfer of this steroid hormone as part of a mating plug dramatically changes female physiological processes intimately tied to vectorial capacity. By combining phenotypic studies with ancestral state reconstructions and phylogenetic analyses, we show that mating plug transfer and male 20E synthesis are both derived characters that have coevolved in anophelines, driving the adaptation of a female 20E-interacting protein that promotes oogenesis via mechanisms also favoring Plasmodium survival. Our data reveal coevolutionary dynamics of reproductive traits between the sexes likely to have shaped the ability of anophelines to transmit malaria.

Evolution of sexually-transferred steroids inAnophelesmosquitoes

“…Consistent with this, while we show that male steroid production and subsequent transfer to females is likely to have evolved only once in the common ancestor of Cellia species, phylogenetic analyses on malaria mosquitoes support a convergent evolution with independent acquisitions of vectorial capacities in Anopheles mosquitoes (45)(46)(47). Also, a previous study has suggested that post-mating responses in Anopheles mosquitoes only exist in species whose males produce and transfer steroids to females shaping malaria vectorial capacities (15). Here we demonstrate that mating-induced phenotypes are variable among species and possibly even among strains or under different environmental conditions.…”

“…Cellia species such as Anopheles arabiensis and Anopheles dirus (15), strongly suggesting that transfer of steroids to females during mating is part of the "male 20E production" synapomorphy of Cellia mosquitoes.…”

“…arabiensis (Cellia, whose males produce steroids) (15) but not in An. albimanus (Nyssorhynchus, whose males do not produce steroids) (15,31), experiments presented here and repeated with three independent cohorts of mosquitoes show that there is an effect of mating on egg development in An. albimanus but not in An.…”

“…gambiae mated females (14). A report further suggested that production of steroids by male Anopheles mosquitoes, their transfer to females during mating and mating-induced phenotypes would be specific to dominant human malaria vectors, likely determining these mosquito species' ability to transmit malaria to humans (15,16). Steroids became as such a promising target to manipulate mosquito female reproduction with the aim to reduce malaria vector populations specifically.…”

Malaria genotyping for epidemiologic surveillance

“…At the same time, advances in the study of parasite genetics, especially for Plasmodium falciparum, have enabled important insights into specific questions regarding parasite biology, such as the mechanisms underlying immune evasion and the origins and evolution of drug resistance (1-3). Additional insights have come from genetic analysis of mosquito populations (4). Although genetic studies have improved our basic understanding of malaria, links between malaria genetics and transmission-and a path to generating operationally useful information-have been more elusive.…”