Similarly, when aphids are raised on plants genetically engineered to emit a compound that warns surrounding aphids of a predator, they become accustomed to the chemical and no longer respond to it -- even when a predator is present, according to Cornell and Boyce Thompson Institute (BTI) researchers reporting Aug. 3 in an online edition of the Proceedings of the National Academy of Sciences.

Under normal circumstances, when a ladybug captures and bites into an aphid, the victim releases an alarm pheromone called beta-farnesene, which prompts nearby aphids to walk away or drop off the plant. Researchers are interested in protecting plants from aphids through genetically engineered crops that produce beta-farnesene or through traditional breeding methods that cross crops with plants -- such as some wild and cultivated potatoes and peppermint -- that naturally produce the pheromone.

The findings have implications for controlling aphids in crops, which could be engineered to make aphids unresponsive to warnings of ladybugs and other predators, making them easy prey.

But, as this study shows, "simply engineering plants to produce beta-farnesene will not make them resistant," said Georg Jander, an associate scientist at BTI on Cornell's Ithaca campus and a senior author of the paper with Robert Raguso, a Cornell professor of neurobiology and behavior. "When we put ladybugs into the mix, the aphids that are habituated to alarm pheromone get eaten more by ladybugs," Jander added.

In the study, aphids reared continuously on genetically engineered Arabidopsis thaliana plants that produced beta-farnesene became habituated to the pheromone within three generations and no longer responded to the compound, even though they still produced it. The habituated aphids did produce more progeny, perhaps because they expended less energy on running away and could focus on feeding more when compared with normal aphids, said Jander. Still, normal aphids had a higher survival rate in the presence of predators and would likely outcompete the habituated aphids in a natural setting.

The study also revealed that 15 percent of the genes in normal aphids displayed altered gene expression within 30 minutes of exposure to beta-farnesene, but "aphids that have been growing on alarm pheromone plants don't show this altered gene expression response," said Jander.

The results reveal a systemic response to the pheromone. "Being afraid is not just about running away, it changes the physiology of the aphid," said Jander. "But these gene expression changes don't happen with the habituated aphids, so somehow the signaling pathway is altered."

Co-authors included Martin de Vos, a former BTI postdoctoral researcher; Wing Yin Cheng '10, both members of Jander's lab; and Holly Summers, a graduate student in Raguso's lab.

The study was funded by the National Science Foundation and the U.S. Department of Agriculture.

The above story is reprinted (with editorial adaptations by ScienceDaily staff) from materials provided by Cornell University. The original article was written by Krishna Ramanujan.

Journal Reference:

1. M. de Vos, W. Y. Cheng, H. E. Summers, R. A. Raguso, G. Jander. Alarm pheromone habituation in Myzus persicae has fitness consequences and causes extensive gene expression changes. Proceedings of the National Academy of Sciences, 2010; DOI: 10.1073/pnas.1001539107

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)-β-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.