Introduction
Non-native plant invasions have provided remarkable insights into rapid
adaptation in defense allocation (Callaway & Maron, 2006; Waller et
al., 2020). In part, this is because non-native plant species are
typically released from specialist enemies in introduced ranges but
continue to be attacked by generalists - the Enemy Release Hypothesis
(Keane & Crawley, 2002). Thus, the most predictable change in herbivore
communities in non-native ranges, at least until biological control
agents are introduced, is the loss of specialists and disproportionate
exposure to naive generalists. Generalist-dominated communities in
non-native ranges commonly correspond with exotic species developing
greater qualitative chemical defenses against generalists, relative to
conspecifics in the native range - the Shifting Defense Hypothesis
(Joshi & Vrieling, 2005; Zhang et al., 2018). These qualitative
defenses may be constitutive or induced, but little is known about
selection on constitutive versus induced defenses in non-native ranges.
Theory and hypotheses that specifically focus on how constitutive and
induced defenses might respond to generalists in native and non-native
ranges have not led to clear predictions (Orians & Ward, 2010), which
is barrier to understanding successful invasion.
Plants are thought to maximize their fitness by balancing resource
allocation to defense with other functions (Rotter & Holeski, 2018;
Mertens et al., 2021), and this allocation can be affected by herbivore
pressure (Stamp, 2003). Constitutive defenses protect plants from attack
without a time lag, but constitutive defenses are thought to be costly
in the absence of herbivores (Wittstock & Gershenzon, 2002; Ali &
Agrawal, 2012; Aljbory & Chen, 2018). Thus, when herbivore pressure is
low, plant fitness might be maximized by investing less in constitutive
defenses. In contrast, induced defenses appear to be cost-saving
strategies where defenses are expressed only in response to herbivore
pressure (Gatehouse, 2002; Agrawal & Hastings, 2019).
From the “quagmire” (Stamp, 2003) of hypotheses for defense allocation
in plants, a few possibilities emerge for how induced and constitutive
defenses might evolve in plant species in their non-native ranges. In a
review of invasive plants, Orians & Ward (2010) suggested that induced
defense should evolve to be more prevalent in non-native ranges where
the cost of defense is high and plants are attacked infrequently
(Bixenmann et al., 2016; Agrawal & Karban, 1999). Different non-native
species often experience very different degrees of generalist herbivore
pressure (Zou, 2008; Sims-Chilton et al., 2009), providing opportunities
to test Orian & Ward’s idea. 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. induced defensive strategies among non-native plant species
is unknown.
Growth-defense tradeoffs appear to derive from plasticity or adaptive
variation in allocation that maintains fitness in a variable environment
(Monson et al., 2022). Increased investment in defense may result in
reduced growth (Hahn et al., 2021), leading to differential investment
in growth or defense by species based on their evolutionary responses to
environmental conditions - the Resource Availability Hypothesis (Coley
et al., 1985). Most studies have focused on how variation in herbivore
pressure across geographical clines shapes evolution of plant defense
(Woods et al., 2012; Moreira et al., 2018). However, these studies have
not generally considered how biogeographical shifts in defense
strategies might constrain growth.
Non-native species provide a good system for studying induced and
constitutive defenses. If non-native species are attacked less by
generalists than native species, we can test the prediction that (i)
non-natives increase expression of cheaper induced defenses and decrease
expression of expensive constitutive defenses (Figure S1A and S1B). If
non-native species are attacked disproportionately by generalists, then
this disentangling of generalist and specialist effects might permit a
cleaner opportunity to test another prediction (ii), that the herbivore
pressure a species experiences will increase expression of constitutive
defenses and decrease induced defenses (Figure S1A and S1B). We can then
test the prediction (iii) that allocation to less expensive induced
defense allow allocation to greater growth (Figure S1C).
To explore these predictions, we first carried out large spatial scale
measurements of herbivore intensity on 27 non-native and 59 co-occurring
native species in a field survey in northern China (Table S1, S2 and
S3). We then quantified herbivore intensity on 12 pairs of non-native
species and native congeners in a common garden. Finally, we conducted
measurements of constitutive and induced defenses as well as plant
growth on these pairs of common garden species (Table S4).