Transcriptional responses to short-term and long-term host plant experience and parasite load in an oligophagous beetle.

Abstract

Oligophagous herbivores must adjust their enzymatic machinery to the different host plant species they consume. If different hosts are used from one generation to the next, adaptation may be highly plastic, while if a single host is used over several generations, there may be a longer-term response due to natural selection. Using an experimental evolutionary approach, we investigated effects of long-term experience vs. short-term responses to different host plants in the oligophagous mustard leaf beetle Phaedon cochleariae. After 26 generations of continuous feeding on either Brassica rapa, Nasturtium officinale or Sinapis alba, freshly hatched larvae were kept on these plants or moved to one of the other host plants for ten days. Global transcriptional patterns as shown by microarrays revealed that between 1% and 16.1% of all 25,227 putative genes were differentially expressed in these treatments in comparison with the control line constantly feeding on B. rapa. A shift back from S. alba to B. rapa caused the largest changes in gene transcription and may thus represent the harshest conditions. Infection rates with a gregarine parasite were intermediate in all lines that were constantly kept on one host, but much lower or higher when short-term shifts to other host plants occurred. In conclusion, transcriptional plasticity in genes related to metabolism, digestion and general cellular processes plays a key role in long- and short-term responses of the beetle to changing host plant conditions, whereby the specific conditions also affect the interactions between the beetle host and its gregarine parasite.