Trade-offs and tritrophic consequences of host shifts in specialized root herbivores

1. Trade-offs in an herbivore’s ability to feed, avoid predation and succeed on alternative hosts are thought to be major driving factors in host specialization. In this study, we compared how two closely related milkweed beetles (Tetraopes spp.) that have specialized on separate Asclepias species respond to host switching to alternative milkweed plants. By additionally examining effects on the beetles’ entomopathogenic natural enemies, we test whether host plant specialization is driven by plant–herbivore interactions alone or whether there is a role for the tritrophic interactions. 2. Tetraopes beetles feed on milkweed roots as larvae and on milkweed shoots as adults, and they sequester toxic cardenolides from their host plants. We predicted that growth and sequestration would be compromised on alternative hosts as a consequence of specialization. Larvae of each Tetraopes species were reared on their native host plant, the host plant of the other species and two closely related Asclepias species that do not typically host Tetraopes. 3. Regardless of beetle specialization, survival of both beetles was highest on A. syriaca, which has the second-to-lowest levels of root cardenolides and is the native host for T. tetraophthalmus. Larval growth was not affected by host plant for T. texanus, but T. tetraophthalmus grew best on A. exaltata, a close relative of A. syriaca that does not typically experience beetle feeding. 4. We found that larval sequestration of cardenolides largely mirrored host plant values in the roots, with the exception of T. texanus on A. asperula, which sequestered a low proportion of the cardenolides from this host. Although all larvae were susceptible to entomopathogenic nematodes (EPNs), the number of EPNs emerging from cadavers depended on the beetle–plant combination, with more EPNs produced when beetles were feeding on native compared to non-native hosts. 5. The observed consequences for tritrophic interactions did not fit expectations for specialized herbivores (i.e. EPN predation was highest when beetles were on their native hosts), suggesting that specialization may be driven primarily by a plant–herbivore interaction in this system, not by a tritrophic effect.