Transcriptional profile and differential fitness in a specialist milkweed insect across host plants varying in toxicity

Abstract

Interactions between plants and herbivorous insects have been models for theories of specialization and co-evolution for over a century. Phytochemicals govern many aspects of these interactions and have fostered the evolution of adaptations by insects to tolerate or even specialize on plant defensive chemistry. While genomic approaches are providing new insights into the genes and mechanisms insect specialists employ to tolerate plant secondary metabolites, open questions remain about the evolution and conservation of insect counterdefences, how insects respond to the diversity defences mounted by their host plants, and the costs and benefits of resistance and tolerance to plant defences in natural ecological communities. Using a milkweed-specialist aphid (Aphis nerii) model, we test the effects of host plant species with increased toxicity, likely driven primarily by increased secondary metabolites, on aphid life history traits and whole-body gene expression. We show that more toxic plant species have a negative effect on aphid development and lifetime fecundity. When feeding on more toxic host plants with higher levels of secondary metabolites, aphids regulate a narrow, targeted set of genes, including those involved in canonical detoxification processes (e.g., cytochrome P450s, hydrolases, UDP-glucuronosyltransferases and ABC transporters). These results indicate that A. nerii marshal a variety of metabolic detoxification mechanisms to circumvent milkweed toxicity and facilitate host plant specialization, yet, despite these detoxification mechanisms, aphids experience reduced fitness when feeding on more toxic host plants. Disentangling how specialist insects respond to challenging host plants is a pivotal step in understanding the evolution of specialized diet breadths.

Expression plasticity and evolutionary changes extensively shape the sugar‐mimic alkaloid adaptation of nondigestive glucosidase in lepidopteran mulberry‐specialist insects

“…To herbivores, expression plasticity could also be indispensable in their adaptation to host plants, leading to higher detoxification potential, and even reducing the production of plant defence compounds (Dermauw et al., ; Wybouw et al., ). Moreover, in oligophagous and monophagous insects, feeding on host plants with increased secondary metabolites will lead to a narrow and targeted gene upregulation in canonical digestion and detoxification processes, including cytochrome P450s, UDP–glucuronosyltransferases and ABC transporters (Birnbaum et al., ; Muller, Vogel, & Heckel, ). For example, the expression levels of CYP6AE14 and CYP6AB3, members of critical detoxifying enzyme cytochrome P450, can be induced by gossypol and furanocoumarins in lepidopterans, respectively (Mao, Rupasinghe, Zangerl, Schuler, & Berenbaum, ; Mao et al., ).…”

“…Certain insect species can feed on diverse plant families with distinct phytochemicals. However, the overwhelming majority of phytophagous insects are specialists that feed on one or a few plant species characterized by particular phytochemicals (Birnbaum, Rinker, Gerardo, & Abbot, ; Forister et al., ). The mechanisms that drive the ecological specialization are starting to become understood in recent years (Petschenka & Agrawal, ; Züst, Agrawal, & Lee, ).…”

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

“…Indeed, aphids had lower masses and per capita growth rates on plants under medium AMF availability (Figure 2), which had greater foliar cardenolide concentrations than plants without AMF (Figure 4). Although A. nerii tolerate cardenolides, they are negatively affected by high cardenolide concentrations (Agrawal, 2004;de Roode et al, 2011;Birnbaum et al, 2017). Nonetheless, we interpret the regressions with caution due to low sample sizes and plant species-specific differences in traits.…”

“…Oleander aphids tolerate cardenolides through regulation of a narrow set of genes involved in canonical detoxification processes (Birnbaum et al, 2017). Monarch caterpillars, in contrast, have NA + /K + -ATPases that are insensitive to cardenolides (Dobler et al, 2012;Petschenka and Agrawal, 2015).…”

“…Monarch caterpillars, in contrast, have NA + /K + -ATPases that are insensitive to cardenolides (Dobler et al, 2012;Petschenka and Agrawal, 2015). Despite being able to tolerate cardenolides, both oleander aphids and monarch caterpillars exhibit reduced performance on host plants with high concentrations of cardenolides (Zalucki et al, 2001a;Agrawal, 2004Agrawal, , 2005Rasmann et al, 2009;de Roode et al, 2011;Colvin et al, 2013;Tao et al, 2016b;Birnbaum et al, 2017). Furthermore, both oleander aphids and monarch caterpillars sequester cardenolides (Rothschild et al, 1970;Malcolm and Brower, 1989;Malcolm, 1990;Züst and Agrawal, 2016b), providing an effective defense against aphid predators (Pasteels, 1978;Malcolm, 1989Malcolm, , 1992Pappas et al, 2007;Mooney et al, 2008) and monarch predators and parasites (Brower et al, 1968;Reichstein et al, 1968;Brower and Moffitt, 1974;Sternberg et al, 2012).…”