Contrasting Oviposition Preference Despite Limited Chemosensory Receptor Gene Differentiation in Two Cryptic Anopheles Species

Abstract

Adaptation to novel environments is often associated with behavioural changes, but how decision-making processes and their genetic underpinnings evolve during ecological divergence remains poorly understood. Human-modified environments provide an ideal context in which to investigate how species adjust their behaviours in response to altered ecological conditions. We used oviposition site selection in two incipient mosquito species segregating along gradients of anthropogenic disturbance to investigate how differences in sensory perception modulate behavioural shifts accompanying ecological divergence. Using two-choice assays, we tested oviposition preferences in 1046 gravid female mosquitoes from field and laboratory populations by offering a choice between water collected from natal and foreign natural breeding sites. We found that females of Anopheles gambiae, a species adapted to rural environments, preferentially oviposited in natal water and deposited 89% of their eggs in a single breeding site. In contrast, females of its sibling species, Anopheles coluzzii, which is adapted to urban environments, exhibited weaker natal-water preference and frequently distributed their egg clutches between multiple breeding sites. To assess the extent of chemosensory divergence between these cryptic species, we analyzed amino acid substitutions within odorant, ionotropic and gustatory receptor gene families using whole-genome sequencing data. Despite limited differentiation across the gene families overall, several loci implicated in the detection of carboxylic acids, amines and volatile compounds exhibited elevated genetic divergence between species. Our work suggests that shifts in decision making associated with ecological divergence between emerging species can arise prior to substantial differentiation throughout the genome or across chemosensory receptor gene families.