A radiation of Psylliodes flea beetles on Brassicaceae is associated with the evolution of specific detoxification enzymes

Flea beetles of the genus Psylliodes have evolved specialized interactions with plant species belonging to several distantly related families, mainly Brassicaceae, Solanaceae, and Fagaceae. This diverse host use indicates that Psylliodes flea beetles are able to cope with different chemical defense metabolites, including glucosinolates, the characteristic defense metabolites of Brassicaceae. Here we investigated the evolution of host use and the emergence of a glucosinolate-specific detoxification mechanism in Psylliodes flea beetles. In phylogenetic analyses, Psylliodes species clustered into four major clades, three of which contained mainly species specialized on either Brassicaceae, Solanaceae, or Fagaceae. Most members of the fourth clade have broader host use, including Brassicaceae and Poaceae as major host plant families. Ancestral state reconstructions suggest that Psylliodes flea beetles were initially associated with Brassicaceae and then either shifted to Solanaceae or Fagaceae, or expanded their host repertoire to Poaceae. Despite a putative ancestral association with Brassicaceae, we found evidence that the evolution of glucosinolate-specific detoxification enzymes coincides with the radiation of Psylliodes on Brassicaceae, suggesting that these are not required for using Brassicaceae as hosts but could improve the efficiency of host use by specialized Psylliodes species.

Funding was provided by the Max Planck Society, the International Max Planck Research School, and the Daimler & Benz Foundation (project number 32-01/14). Harald Letsch was funded by the Austrian Science Fund (FWF) project P32029-B. Part of the genetic results presented here were achieved in the frame of the German Barcode of Life, a project of the Humboldt Ring, grant funded by the German Federal Ministry for Education and Research (GBOL1: BMBF #01LI1101A/#01LI1501A).

Peer reviewed