Heritability of biting time behaviours in the major African malaria vector Anopheles arabiensis

The use of insecticide-treated nets for malaria control has been associated with shifts in mosquito vector feeding behaviour including earlier and outdoor biting on humans. The relative contribution of phenotypic plasticity and heritability to these behavioural shifts is unknown. Elucidation of the mechanisms behind these shifts is crucial for anticipating impacts on vector control.

A novel portable semi-field system (PSFS) was used to experimentally measure heritability of biting time in the malaria vector Anopheles arabiensis in Tanzania. Wild An. arabiensis from hourly collections using the human landing catch (HLC) method were grouped into one of 3 categories based on their time of capture: early (18:00-21:00), mid (22:00-04:00), and late (05:00-07:00) biting, and placed in separate holding cages. Mosquitoes were then provided with a blood meal for egg production and formation of first filial generation (F1). The F1 generation of each biting time phenotype category was reared separately, and blood fed at the same time as their mothers were captured host-seeking. The resultant eggs were used to generate the F2 generation for use in heritability assays. Heritability was assessed by releasing F2 An. arabiensis into the PSFS, recording their biting time during a human landing catch and comparing it to that of their F0 grandmothers.

In PSFS assays, the biting time of F2 offspring (early: 18:00-21:00, mid: 22:00-04:00 or late: 05:00-07:00) was significantly positively associated with that of their wild-caught F0 grandmothers, corresponding to an estimated heritability of 0.110 (95% CI 0.003, 0.208). F2 from early-biting F0 were more likely to bite early than F2 from mid or late-biting F0. Similarly, the probability of biting late was higher in F2 derived from mid and late-biting F0 than from early-biting F0.

Despite modest heritability, our results suggest that some of the variation in biting time is attributable to additive genetic variation. Selection can, therefore, act efficiently on mosquito biting times, highlighting the need for control methods that target early and outdoor biting mosquitoes.