Divergence in threat sensitivity among aquatic larvae of cryptic mosquito species

Abstract

Predation is a major evolutionary force driving speciation. The threat-sensitive response hypothesis predicts that prey adjust and balance the time spent on a costly antipredator response with other activities that enhance their fitness. Thus, prey able to develop an antipredator response proportional to risk intensity should have a selective advantage. Knowledge on how evolution has shaped threat sensitivity among closely related species exposed to different predation pressures is scarce, prompting investigations to better predict and explain its effect on communities. We explored and compared the antipredator response of aquatic mosquito larvae in three sibling species of the Anopheles gambiae complex, with contrasting larval biologies in Burkina Faso. Anopheles arabiensis and An. gambiae sensu stricto breed in temporary water collections where predator densities are low, whereas Anopheles coluzzii is able to thrive in permanent pools where the predation pressure is much higher. We hypothesized that the increase and decline of behavioural antipredator responses might differ between the three species over time. To test this hypothesis, progenies of field-collected mosquitoes were experimentally exposed to a range of soluble predation cues and their response was monitored for up to 48 h. The three species were all threat sensitive but their reaction norms differed. For the range of concentrations tested, An. coluzzii larvae gradually increased in antipredator response, whereas An. gambiae larvae readily displayed antipredator behaviour at low concentrations leading to a saturation of the response for high cue concentrations. An. arabiensis displayed a narrower reaction norm with low response intensity. Larval instars did not differ in their threat sensitivity. The antipredator behaviour of the three species waned after about 1 h of exposure. Early instars tended to express antipredation behaviour for longer than did older instars. This study provides information on how aquatic prey species with an aerial adult stage manage larval predation risk over time according to cue concentrations and suggests that different predation pressures might play a role as a disruptive selective force fostering habitat segregation and speciation within the An. gambiae complex. The evolution of phenotypic plasticity is further discussed in the light of divergent predation pressures.