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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