Alarm pheromone habituation in Myzus persicae has fitness consequences and causes extensive gene expression changes

Abstract

In most aphid species, facultative parthenogenetic reproduction allows rapid growth and formation of large single-genotype colonies. Upon predator attack, individual aphids emit an alarm pheromone to warn the colony of this danger. (E)-beta-farnesene (EBF) is the predominant constituent of the alarm pheromone in Myzus persicae (green peach aphid) and many other aphid species. Continuous exposure to alarm pheromone in aphid colonies raised on transgenic Arabidopsis thaliana plants that produce EBF leads to habituation within three generations. Whereas naive aphids are repelled by EBF, habituated aphids show no avoidance response. Similarly, individual aphids from the habituated colony can revert back to being EBF-sensitive in three generations, indicating that this behavioral change is not caused by a genetic mutation. Instead, DNA microarray experiments comparing gene expression in naive and habituated aphids treated with EBF demonstrate an almost complete desensitization in the transcriptional response to EBF. Furthermore, EBF-habituated aphids show increased progeny production relative to EBF-responsive aphids, with or without EBF treatment. Although both naive and habituated aphids emit EBF upon damage, EBF-responsive aphids have a higher survival rate in the presence of a coccinellid predator (Hippodamia convergens), and thus outperform habituated aphids that do not show an avoidance response. These results provide evidence that aphid perception of conspecific alarm pheromone aids in predator avoidance and thereby bestows fitness benefits in survivorship and fecundity. Therefore, although habituated M. persicae produce more progeny, EBF-emitting transgenic plants may have practical applications in agriculture as a result of increased predation of habituated aphids.