High individual variation in pheromone production by tree-killing bark beetles (Coleoptera: Curculionidae: Scolytinae)

Abstract

Aggregation via pheromone signalling 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 paradoxical. One explanation is that the technique of measuring static pheromone pools overestimates true variation among individuals. An alternative hypothesis is that aggregation behaviour 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.

Semiochemicals in the Natural History of Southern Pine Beetle Dendroctonus frontalis Zimmermann and Their Role in Pest Management

“…It is present in newly emerged, host-arriving, and gallery-establishing females Pureswaran et al, 2007;Renwick and Vit e, 1968;Sullivan et al, 2007bSullivan et al, , 2012 and generally is undetectable in males (although see Grosman, 1996;Grosman et al, 1997;Pureswaran et al, 2006;. Evidence of its uniqueness to females is consistent with the observation that logs infested with solitary D. frontalis females are attractive whereas those with forced male attacks are not .…”

“…Forcing a solitary male to chew into the bark by confinement appears to cause a similar drop in presence of verbenone as does pairing with a female, suggesting the reduction is due to defecation of the hindgut-stored quantities of the compound and not mating (Sullivan et al, 2007b). Nonetheless, despite this apparent depletion of verbenone amounts in the gut and reduction of amounts in headspace aerations of isolated male beetles before vs after feeding (Pureswaran et al, 2007), aerations of trees undergoing mass attack indicated that entrances of beetle pairs released about twice as much verbenone as entrances of solitary females (Pureswaran and Sullivan, 2012).…”

“…Furthermore, pine posts infested with virgin female D. frontalis reached maximum attractiveness after 48 h (Coster and Vit e, 1972), and pine logs either artificially infested with beetles or cut from mass-attacked trees could maintain some attractiveness for multiple days Franklin, 1970). Additionally, static headspace aerations (ie, involving beetles confined in still air with chemical adsorbent) indicated that emergent females released frontalin at a lower rate than females that were excised from logs after feeding for $1 d (Sullivan et al, 2007b;Pureswaran et al, 2008b). The opposite was observed for transverbenol, which is by far the dominant volatile compound present in the hindguts of emergent females.…”

“…It apparently is released quickly upon landing or gallery initiation since feeding females-both solitary and paired with males inside galleries-contain and release much smaller amounts, even within a few hours after entering a host (Coster and Vit e, 1972;Hughes, 1973;Pureswaran et al, 2006Pureswaran et al, , 2008bSullivan et al, 2012). Its presence is strongly sexually dimorphic in newly emerged beetles (Renwick, 1967) with females containing 10 to >1000 times more than emerged males (Grosman et al, 1997;Pureswaran et al, 2008a;Sullivan et al, 2012).…”

“…Likewise these droplets disappear and the quantities measured in hindgut extracts decline rapidly following the male's entry into the bark Pureswaran et al, 2007;Vit e and Crozier, 1968). Forcing a solitary male to chew into the bark by confinement appears to cause a similar drop in presence of verbenone as does pairing with a female, suggesting the reduction is due to defecation of the hindgut-stored quantities of the compound and not mating (Sullivan et al, 2007b).…”