Characterization of factors influencing swarm dynamics and mating efficiency in Anopheles coluzzii

Malaria vectors reproduce through in-flight copulation within swarms, which remains poorly understood. Gaining insights into swarming and mating behavior is essential for optimizing novel vector control strategies including sterile insect technique, genetically modified mosquitoes, and behavior based intervention. This study investigates the factors influencing swarm dynamics and mating efficiency in Anopheles coluzzii.

We surveyed swarms across 40 residential compounds in Burkina Faso, georeferencing swarming sites and recording swarming times and height. In a subset of three compounds selected for detailed characterization, we also measured inter-swarm distances, counted swarm size from photography, and mating pairs through direct observation during swarming. Furthermore, we collected 30% of male mosquitoes from swarms to measure wing length and perform PCR analyses. We monitored environmental variables including temperature, humidity, wind speed, and luminosity. Finally, we performed spatial and statistical analysis using ArcGIS and R to determine how swarm and mating dynamics are correlated and how they depend on biological and environmental conditions.

We identified 169 Anopheles coluzzii swarms and found strong evidence of spatial clustering (General G: P < 0.001; Moran's I = 0.2, P < 0.001), with localized hotspots. Swarming occurred between 18:05 h and 18:45 h, extending into darkness at ~19:15 h. Swarms had an average height of 2.87 m (range: 1.0-3.2 m) and consisted of 83-2783 mosquitoes. Swarm size strongly predicted pairing success in Anopheles coluzzii (t = 9.16, P < 0.001) with larger swarms producing more pairs. However, individual pairing efficiency decreased with swarm size (t = -3.515, P < 0.001). Male size positively influenced individual pairing efficiency (t = 3.25, P = 0.002) but did not affect swarm size or total pairing frequency. Inter-swarm distances varied nonrandomly, suggesting interactions between neighboring and/or swarm markers.

This study shows that An. coluzzii swarming is shaped by both biological and environmental factors. While larger males achieved higher individual mating efficiency, swarm size was the strongest predictor of mating success. Larger swarms yielded more mating pairs overall, although efficiency declined with increasing density. In addition, swarms formed in clustered nonrandom patterns within compounds. These results highlight the interplay between male traits and environment in shaping swarming dynamics.