Data from: 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.) which 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 if there is a role for the tri-trophic 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.

1. 植食性动物在取食、躲避捕食以及在替代寄主上存活繁殖的能力权衡，被认为是驱动寄主特化的核心因素。本研究针对两种特化于不同马利筋属（Asclepias）物种的近缘乳草甲虫（Tetraopes spp.），比较其在转向其他乳草植物时的响应差异。此外，通过考察该类群的昆虫病原天敌（entomopathogenic natural enemies）所受的影响，我们验证寄主植物特化是否仅由植物-植食性动物互作驱动，抑或三营养级相互作用（tri-trophic interactions）亦发挥作用。
2. 乳草甲虫（Tetraopes spp.）的幼虫以乳草属植物根系为食，成虫则取食地上嫩茎，且可从寄主植物中富集有毒的强心苷（cardenolides）。基于特化的演化代价，我们预测甲虫在替代寄主上的生长与强心苷富集能力会受到抑制。本实验将两种该属甲虫的幼虫分别饲养于其原生寄主植物、异种甲虫的原生寄主，以及两种通常不会被该属甲虫寄生的近缘马利筋属物种上。
3. 无论甲虫的特化程度如何，两种甲虫在普通马利筋（A. syriaca）上的存活率均为最高；该植物的根系强心苷含量处于倒数第二低的水平，同时也是T. tetraophthalmus的原生寄主。T. texanus的幼虫生长不受寄主植物种类影响，而T. tetraophthalmus在高茎马利筋（A. exaltata）上生长最佳——后者是普通马利筋的近缘物种，通常不会被乳草甲虫取食。
4. 我们发现，幼虫的强心苷富集水平大体上与寄主植物根系的强心苷含量相符，唯有取食粗糙马利筋（A. asperula）的T. texanus例外：该类群从该寄主中富集的强心苷比例较低。尽管所有甲虫幼虫均对昆虫病原线虫（EPNs）易感，但从虫尸中逸出的线虫数量取决于甲虫-寄主植物的组合：当甲虫取食原生寄主时，产生的线虫数量多于取食非原生寄主的情况。
5. 本研究观测到的三营养级相互作用结果，并不符合特化植食性动物的预期（即当甲虫处于原生寄主上时，昆虫病原线虫的捕食压力最高），这表明在该实验系统中，寄主特化主要由植物-植食性动物互作驱动，而非三营养级效应。