High individual variation in pheromone production by tree-killing bark beetles (Coleoptera: Curculionidae: Scolytinae)
Aggregation via pheromone signaling is essential for tree-killing bark beetles to overcome tree defenses and reproduce within hosts. Pheromone production is a trait that is linked to fitness, so high individual variation is paradoxica1. One explanation is that the technique of measuring static pheromone pools overestimates true variation among individuals. An alternative hypothesis is that aggregation behavior dilutes the contribution of individuals to the trait under selection and reduces the efficacy of natural selection on pheromone production by individuals. We compared pheromone measurements from traditional hindgut extractions of female southern pine beetles with those obtained by aerating individuals till they died. Aerations showed greater total pheromone production than hindgut extractions, but coefficients of variation (CV) remained high (60- 182%) regardless of collection technique. This leaves the puzzle of high variation unresolved. A novel but simple explanation emerges from considering bark beetle aggregation behaviour. The phenotype visible to natural selection is the collective pheromone plume from hundreds of colonisers. The influence of a single beetle on this plume is enhanced by high variation among individuals but constrained by large group sizes. We estimated the average contribution of an individual to the pheromone plume across a range of aggregation sizes and showed that large aggregation sizes typical in mass attacks limit the potential of natural selection because each individual has so little effect on the overall plume. Genetic variation in pheromone production could accumulate via mutation and recombination, despite strong effects of the pheromone plume on the fitness of individuals within the aggregation. Thus, aggregation behaviour, by limiting the efficacy of natural selection. can allow the persistence of extreme phenotypes in nature.
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