Recently, the highly invasive Asian tiger mosquito, Aedes albopictus, rapidly displaced resident populations of the yellow fever mosquito, Aedes aegypti in the southeastern United States and in Bermuda. Although multiple mechanisms of competitive displacement have been hypothesized, recent evidence of cross-insemination between these species in nature and the sterilizing effects of male accessory gland products asymmetrically favoring A. albopictus in interspecific matings support a role for satyrization (a form of reproductive interference) to explain the rapid displacements. Because of the drastic reproductive loss of A. aegypti females satyrized by A. albopictus males, we predicted selection for prezygotic isolation in populations of A. aegypti sympatric with A. albopictus. Exposures in cages demonstrated that female A. aegypti from populations in Florida sympatric with A. albopictus for the past 20 y were significantly less likely than nearby allopatric populations to mate with heterospecific males. Cross-inseminations of A. albopictus females by A. aegypti males were significantly less common, supporting the one-way direction of displacements observed in nature. Our results indicate rapid sexual selection leading to reproductive character displacement and the potential for satyr-resistant A. aegypti to recover from competitive displacements. These results have implications for increased risks of dengue transmission where these vector species meet worldwide.

BackgroundMicrosporidian parasites of mosquitoes offer a possible way of controlling malaria, as they impede the development of Plasmodium parasites within the mosquito. The mechanism involved in this interference process is unknown.MethodologyWe evaluated the possibility that larval infection by a microsporidian primes the immune system of adult mosquitoes in a way that enables a more effective anti-Plasmodium response. To do so, we infected 2-day old larvae of the mosquito Anopheles gambiae with one of 4 isolates of the microsporidian Vavraia culicis and reared one group as an uninfected control. Within each treatment, we fed half the adult females on a mix of P. berghei ookinetes and blood and inoculated the other half with a negatively charged CM-25 Sephadex bead to evaluate the mosquitoes' melanisation response.ConclusionsThe microsporidian-infected mosquitoes were less likely to harbour oocysts (58.5% vs. 81.8%), harboured fewer oocysts (8.9 oocysts vs. 20.7 oocysts) if the malaria parasite did develop and melanised the Sephadex bead to a greater degree (73% vs. 35%) than the controls. While the isolates differed in the number of oocysts and in the melanisation response, the stimulation of the immune response was not correlated with either measure of malaria development. Nevertheless, the consistent difference between microsporidian-infected and –uninfected mosquitoes — more effective melanisation and less successful infection by malaria — suggests that microsporidians impede the development of malaria by priming the mosquito's immune system.

In this paper we examine the effect of reproductive interference on the dynamics of two mosquito vectors of public health concern and add to the growing literature on the strength and speed with which interspecific reproductive interference may drive evolution. Recent evidence supports a role for asymmetric reproductive interference, or satyrization, in competitive displacements of Aedes aegypti by Aedes albopictus. However, populations of A. aegypti sympatric with A. albopictus in nature evolve resistance to satyrization. Here we report that A. aegypti from Tucson, Arizona (USA), where A. albopictus are not known to occur, are satyrization-susceptible. Furthermore, in cage experiments we demonstrate rapid evolution in satyrization-susceptible lines. Exposing allopatric strains of A. aegypti to A. albopictus in cages led to significant reductions, within 1–3 generations, in the frequency of reproductive interference. We also demonstrate that satyrization-resistant A. aegypti females derived from selection experiments are significantly slower to mate with conspecific males, suggesting a cost for the evolution of satyrization-resistance. Results show how interspecific interactions between these vector species are rapidly evolving, with implications for the arboviral diseases, especially dengue and chikungunya, which they transmit.