Experimental assemblage of novel plant-herbivore interactions: ecological host shifts after 40 million years of...

Geographic isolation is the first step in insect herbivore diet specialization. Such specialization is postulated to increase insect fitness, but may simultaneously reduce insect ability to colonize novel hosts. During the Paleocene-Eocene, plants from the order Zingiberales became isolated either in the Paleotropics or in the Neotropics. During the Cretaceous, rolled-leaf beetles diversified in the Neotropics concurrently with Neotropical Zingiberales. Using a community of Costa Rican rolled-leaf beetles and their Zingiberales host plants as study system, we explored if previous geographic isolation precludes insects to expand their diets to exotic hosts. We recorded interactions between rolled-leaf beetles and native Zingiberales by combining DNA barcodes and field records for 7450 beetles feeding on 3202 host plants. To determine phylogenetic patterns of diet expansions, we set 20 field plots including five exotic Zingiberales, recording beetles feeding on these exotic hosts. In the laboratory, using both native and exotic host plants, we reared a subset of insect species that had expanded their diets to the exotic plants. The original plant-herbivore community comprised 24 beetle species feeding on 35 native hosts, representing 103 plant-herbivore interactions. After exotic host plant introduction, 20% of the beetle species expanded their diets to exotic Zingiberales. Insects only established on exotic hosts that belong to the same plant family as their native hosts. Laboratory experiments show that beetles are able to complete development on these novel hosts. In conclusion, rolled-leaf beetles are pre-adapted to expand their diets to novel host plants even after millions of years of geographic isolation.