INTRODUCTION
To maximise reproductive success, most angiosperms are tasked with
attracting pollinating mutualists whilst also evading herbivore
antagonists (Strauss 1997; Lucas-Barbosa 2016; Kessler & Chautá 2020).
However, plant interactions with pollinators and herbivores, and the
traits that mediate these interactions, are often inter-linked (Theiset al. 2007; González-Teuber & Heil 2009; Galen et al.2011; Kessler et al. 2019; Rusman et al. 2019). Such
linkages typically lead to ecological trade-offs for plants. For
instance, pollinators often preferentially forage on larger, more
apparent flowers and inflorescence displays (Conner & Rush 1996;
Parachnowitsch & Kessler 2010). Yet greater visual or olfactory
apparency can also come at the cost of increased herbivore damage when
co-opted as shared signals (Halitschke et al. 2008; Sletvold &
Grindeland 2008; Theis & Adler 2012; Knauer & Schiestl 2017;
Santangelo et al. 2019). Plant-herbivore interactions can
likewise bear large consequences for pollination success (Kessleret al. 2011; Muola et al. 2017). The presence and action
of herbivores, and in particular their damage to leaves (folivory) and
flowers (florivory), can deter pollinators via a range of direct and
indirect mechanisms (Jacobsen & Raguso 2018; Moreira et al.2019; Haas & Lortie 2020). These include visually (e.g. modification of
floral aesthetics; reduced resource allocation to floral rewards and
displays (McCall & Irwin 2006)), olfactorily (e.g. release of
herbivore-induced plant volatiles (Kessler & Chautá 2020)), and
gustatorily (e.g. upregulated expression of unpalatable defensive
compounds in floral nectar (Adler et al. 2006)). Hence given the
multiple routes by which these ecological effects can manifest for
plants, the net outcome for fitness is thereby expected to be highly
context-specific e.g. (Gegear et al. 2007).
Yet despite growing appreciation of the ecology of
plant-herbivore-pollinator systems, it remains poorly understood how
these interactions ultimately affect phenotypic selection on traits at
the microevolutionary scale. The high degree of ecological linkage and
specificity inherent in these systems suggest that pollinator and
herbivore selection may often be conflicting (i.e., exerted in opposing
directions) and diffuse (i.e., context-dependant on the presence or
ecological effects of the other) (Strauss et al. 2005; Sletvoldet al. 2015; Knauer & Schiestl 2017; Ramos & Schiestl 2019;
Sletvold 2019). However, although herbivory is known to potentially
constrain floral evolution (Johnson et al. 2015; Jogesh et
al. 2017; Ramos & Schiestl 2019; Santangelo et al. 2019), a
recent meta-analysis by Caruso et al. (2019) revealed an almost
categorical lack of studies which simultaneously quantify pollinator-
and herbivore-mediated selection on the same trait. Further studies are
hence required to examine the relative importance and dynamics of
pollinator and herbivore selection on traits that link pollination and
herbivory. Beyond floral traits, these should also include direct and
indirect (i.e., natural enemy-mediated) defences. Few studies to date
have examined the potential for pollinators to select on defence traits
related to herbivory (Kessler & Halitschke 2009; Egan 2015; Ramos &
Schiestl 2019). Yet such selection may in fact be commonplace in plants
(Egan et al. 2016), especially as an adaptation to mitigate
herbivore deterrence of pollinators.
In this study we manipulated pollination and herbivory in a common
garden experiment with woodland strawberry (Fragaria vesca L.).
We examined phenotypic selection on several chemical traits previously
identified as markers of direct and indirect defence for this species
(see below and Weber et al. , 2020a; Weber et al. , 2020b),
alongside several morphological traits potentially important for
attraction of pollinators and herbivores. We tested and found at least
partial support for the hypotheses that: 1) pollinators and herbivores
positively select on defence-related traits – which in this system are
expected to aid against the direct and pollinator-mediated costs of
herbivory (Muola et al. 2017; Muola & Stenberg 2018; Weberet al. 2020a); 2) pollinators and herbivores impose conflicting
selection on plant attractive traits – as shared host-selection cues
potentially used by both agents; and 3) that the above selection regimes
are diffuse – i.e., that pollinator-mediated selection is modified (in
strength, and possibly direction) when herbivory is manipulated, and
vice versa. Investigations of this kind can thereby provide greater
insight into the eco-evolutionary dynamics of plant-herbivore-pollinator
interactions.