Cost-benefit allocation
Optimal defense theory assumes that organisms are under strong natural selection to allocate resources to optimize their cost-benefit ratio in terms of fitness (Stamp, 2003; Alba et al., 2012). Much of this research has focused on a proposed evolutionary tradeoff where invasive plants experience relaxed selection on herbivore defense and evolve greater allocation to growth and competitive ability - the Evolution of Increased Competitive Ability hypothesis (EICA) (Zhang et al., 2020; Callaway et al., 2022). Generalist herbivory can mediate defensive strategies and resource allocation (Müller-Schärer et al., 2004). Thus, we suggest that the costs and benefits of induced defenses should differ in low-versus high-damage risk environments. Such damage pressure-dependent defensive strategies could drive strong selection on developmental defensive strategies (Maron et al., 2019) in ways that optimize plant defense and maximize plant fitness components for each non-native species. In this context, constitutive defense was lower whereas induced defense was higher for non-native species than native congeners, respectively. The striking positive relationship between herbivory experienced by different non-native species in the field and constitutive defense, and negative relationship between herbivory experienced by non-native species and induced defense imply that introduced plants may adopt a cost saving strategy between constitutive defense and induced defense in response to generalist pressure.
Plant species commonly show a strong trade-off between defense and growth (Lazzarin et al., 2021), but herbivore-driven changes in defensive strategy might alter the cost-benefit ratios of defense and growth allocation. Maintaining constitutive defense at high levels appears to require plants to invest substantial resources, potentially increasing the total cost of chemical defenses. If induced defenses are less costly than constitutive defenses, perhaps relaxed selection on constitutive defense could allow greater growth, and such a tradeoff might contribute to the dominance of some non-native species. To our knowledge, no study of EICA has experimentally integrated potential increased growth tradeoffs of non-native plants derived from a shift from constitutive to induced defenses. Our results support the defense strategies that have proposed such tradeoffs between constitutive defense and induced defense where cheaper induced defenses allow greater growth and reproduction (Mumm & Hilker, 2006; Mauch-Mani et al., 2017). Altogether, the results suggest that the defense strategy of stronger protection against generalist herbivores is a factor contributing to invasion success.
An important caveat is that we only used one generalist herbivore,S. littoralis , to explore the defensive strategy of non-native plants. Other studies indicate that generalist preferences and impacts can vary a great deal among herbivore species (Inderjit et al., 2021). Our non-native plants were occupied by many species of generalists in the field, thus, to better understand patterns of defense strategies when non-native plants face generalist herbivore pressure, several generalist herbivore species should be included in future testing of plant defenses. We emphasize that our binary approach to herbivore diet (generalist vs. specialist) was heuristic, and thus too simplistic (Hardy et al., 2020), but appeared to have allowed us to detect some fundamental ecological phenomena. Finally, the best tests of hypotheses such as ours compare the same species in native and non-native ranges (Sheng et al., 2022), and it should be noted that studying defense-related tradeoffs among native and non-native species in the same non-native range provides strong, but not the best, evidence for defense adaptations (Van Kleunen et al., 2010). However, including many non-native and native congeners increases the strength of our results.
Integrating herbivore-related hypotheses for non-native species invasion
Interactions between non-native plants and herbivores have improved our understanding of plant-herbivore interactions, underlying mechanisms, and rapid evolution of these dynamics (Müller-Schärer et al., 2004; Lin et al., 2021). Two key hypotheses derived from non-native invasions are the Enemy Release Hypothesis - that non-native species escape much of the herbivory experienced in their native ranges, primarily by specialists, and the related Shifting Defense Hypothesis - that non-native invaders increase defenses, chiefly qualitative, against generalists. However, we do not know how constitutive and induced defenses might respond to generalist-dominated herbivore communities or the intensity of attack by these communities. Our results show a shift to induced defenses by non-native plants, and that as herbivore pressure intensifies on non-native species, so does the strength of their constitutive defenses. Finally, our results suggest new ways to consider the Evolution of Increased Competitive Ability Hypothesis - perhaps the “cheaper” induced strategy adopted by non-natives allows more allocation to growth and competitive ability. Thus, our results suggest that all three hypotheses may be surprisingly integrated (Figure 6). These results expand our understanding of fundamental tradeoffs in constitutive and induced defenses and provide novel insight into how variation in herbivore communities might affect defense allocation in plants.
Acknowledgments : We thank Hongwei Yu and Sichong Chen for data analysis. We thank the assistance for secondary metabolism from Shanghai BIOTREE Biological Technology Co., Ltd., Shanghai, China. This work was supported by National Natural Science Foundation of China (U21A20190, 32071658, 32071660, 31822007, 32001239), Henan Province University Innovation Talents Support Program (22HASTIT039), Young Talent Support Project of Henan Province (2021HYTP034). RMC was supported by National Science Foundation EPSCoR Cooperative Agreement OIA-1757351.
Competing interest statement : The authors have declared that there is no conflict of interests.
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