Experimental insect suppression causes loss of induced, but not constitutive, resistance in Solanum carolinense

Abstract

Spatiotemporal variation in herbivory is a major driver of intraspecific variation in plant defense. Comparatively little is known, however, about how changes in herbivory regime affect the balance of constitutive and induced resistance, which are often considered alternative defensive strategies. Here, we investigated how nearly a decade of insect herbivore suppression affected constitutive and induced resistance in horsenettle (Solanum carolinense), a widespread herbaceous perennial. We allowed replicated horsenettle populations to respond to the presence or absence of herbivores by applying insecticide to all plants in half of 16 field plots. Horsenettle density rapidly increased in response to insecticide treatment, and this effect persisted for at least 4 years after the cessation of herbivore suppression. We subsequently grew half‐sibling families from seeds collected during and shortly after insecticide treatment in a common garden and found strong effects of insect suppression on induced resistance. Feeding trials in field mesocosms with false Colorado potato beetles (Leptinotarsa juncta), a common specialist herbivore, revealed that multiyear herbivore suppression drove rapid attenuation of induced resistance: offspring of plants from insect‐suppression plots exhibited a near‐complete loss of induced resistance to beetles, whereas those from control plots incurred ~70% less damage after experimental induction. Plants from insect‐suppression plots also had ~40% greater constitutive resistance compared with those from control plots, although this difference was not statistically significant. We nonetheless detected a strong trade‐off between constitutive and induced resistance across families. In contrast, the constitutive expression of trypsin inhibitors (TI), an important chemical defense trait in horsenettle, was reduced by 20% in the offspring of plants from insect‐suppression plots relative to those from control plots. However, TIs were induced to an equal extent whether or not insect herbivores had been historically suppressed. Although several defense and performance traits (prickle density, TI concentration, resistance against false Colorado potato beetles and flea beetles, biomass, and seed mass) varied markedly across families, no traits exhibited significant pairwise correlations. Overall, our results indicate that, whereas the divergent responses of multiple defense traits to insect suppression led to comparatively small changes in overall constitutive resistance, they significantly reduced induced resistance against false Colorado potato beetle.

A mechanistic framework of enemy release

“…one species has high defence and low growth, while another species has the opposite; Lind et al., 2013; Rotter & Holeski, 2018; Heckman et al., 2019) (but see Chauvin et al., 2018; Hinman et al., 2019), evidence for within‐species trade‐offs is weaker (Hahn et al., 2021; Heckman et al., 2019), yet this is more pertinent as host adaptation requires within‐species variation. However, specific plant organs can show trade‐offs related to defence and growth (Agrawal et al., 2012; Medina‐Villar et al., 2021), and there is evidence that some species can adaptively lower defence and increase growth in response to lower enemy pressure (Coverdale & Agrawal, 2022; Wolfe et al., 2004). Evolutionary changes in growth and defence because of enemy release should only benefit exotics that show strong growth–defence trade‐offs.…”

“…Exotics coming from low‐resource environments likely have a lower growth–defence ratio than co‐occurring natives (Endara & Coley, 2011; Figure 3f, blue line). If they are released from enemies and have more resources available, exotic plants will evolve to invest more in growth than defence (Coverdale & Agrawal, 2022). This adaptation can happen in as little as 150 growing seasons (Wolfe et al., 2004) and underpins the well‐known evolution of increased competitive ability (EICA) hypothesis (Blossey & Notzold, 1995).…”

Revisiting plant defense-fitness trade-off hypotheses using Solanum as a model genus

“…Along with oral secretions, excreta or oviposition fluids are also known to act as chemical cues perceived by transmembrane pore proteins in Solanum (Gandhi et al, 2021). More interestingly, the plants of Solanum carolinense has shown trade-offs between constitutive and induced defenses (Kariyat et al, 2013) where the insect suppression reduced the induced resistance significantly more than the constitutive defenses (Coverdale and Agrawal, 2022). The intraspecific variation in Solanum genus also can also lead to differential chemical defense induction (Campbell et al, 2013;Calf et al, 2018;Müller et al, 2020) in herbivores with similar feeding habits.…”

Intensity of herbivory correlates with stronger constitutive and weaker induced defenses for non-native plant species -- another mechanism for EICA?

“…For example, a common garden survey found that different non-native species suffered from 0% to more than 40% leaf herbivory from generalists (Agrawal & Kotanen, 2003). Variation in herbivore pressure should lead to variation in defense traits (Coverdale & Agrawal, 2022;Wan et al, 2022) and less intense and less frequent herbivory is theorized to select for allocation to induced defenses (Bixenmann et al, 2016). However, how this variation in generalist herbivore pressure affects any potential tradeoffs in constitutivevs.…”