Pollinators and herbivores interactively shape selection on strawberry defence and attraction

Abstract

Tripartite interactions between plants, herbivores, and pollinators hold fitness consequences for most angiosperms. However, little is known on how plants evolve in response—and in particular what the net selective outcomes are for traits of shared relevance to pollinators and herbivores. In this study, we manipulated herbivory (“presence” and “absence” treatments) and pollination (“open” and “hand pollination” treatments) in a full factorial common‐garden experiment with woodland strawberry ( Fragaria vesca L.). This design allowed us to quantify the relative importance and interactive effects of herbivore‐ and pollinator‐mediated selection on nine traits related to plant defence and attraction. Our results showed that pollinators imposed stronger selection than herbivores on traits related to both direct and indirect (i.e., tritrophic) defence. However, conflicting selection was imposed on inflorescence density: a trait that appears to be shared by herbivores and pollinators as a host plant signal. However, in all cases, selection imposed by one agent depended largely on the presence or ecological effect of the other, suggesting that dynamic patterns of selection could be a common outcome of these interactions in natural populations. As a whole, our findings highlight the significance of plant‐herbivore‐pollinator interactions as potential drivers of evolutionary change, and reveal that pollinators likely play an underappreciated role as selective agents on direct and in direct plant defence.

Pollinator selection against toxic nectar as a key facilitator of a plant invasion

“…Where interactions involving mutualists and antagonists are mediated by the same trait in plants, rarely are pollinators implicated as predominant selective agents [63]. This study, therefore, represents the first evidence, to our knowledge, of pollinator-mediated selection acting on a defence-related compound in nectar.…”

Evolutionary Ecology of Plant-Arthropod Interactions in Light of the “Omics” Sciences: A Broad Guide

“…In response to the damage caused by herbivorous insects, plants have evolved both direct defenses (e.g., chemical compounds and physical barriers) and indirect defenses (e.g., volatile organic compounds, VOCs) that attract—or enhance the effectiveness of—herbivores’ natural enemies ( Kessler and Baldwin, 2002 ; Poelman et al, 2008 ; Mithöfer and Boland, 2012 ). Furthermore, defensive traits may also attract or repel pollinators ( Galen and Cuba, 2001 ; Ramos and Schiestl, 2020 ; Egan et al, 2021 ). Defensive traits can thus affect herbivores, their natural enemies, and pollinators ( Bukovinszky et al, 2008 ; Poelman et al, 2008 ).…”

“…Defensive traits can thus affect herbivores, their natural enemies, and pollinators ( Bukovinszky et al, 2008 ; Poelman et al, 2008 ). Recent evidence has shown that pollinators are also important selective agents of both plant defensive and reproductive traits ( Herrera et al, 2002 ; Strauss and Irwin, 2004 ; Kessler and Halitschke, 2009 ; Kessler et al, 2011 ; Adler et al, 2012 ; Campbell and Kessler, 2013 ; Muola et al, 2017 ; Ramos and Schiestl, 2019 , 2020 ; Rusman et al, 2019 ; Santangelo et al, 2019 ; Egan et al, 2021 ; Table 1 ). For instance, plants profit from large, colorful flowers that attract pollinators, but such attractive signals sometimes also attract herbivores, imposing an ecological trade-off on the signals’ evolution ( Ramos and Schiestl, 2019 ; Egan et al, 2021 ).…”

“…Recent evidence has shown that pollinators are also important selective agents of both plant defensive and reproductive traits ( Herrera et al, 2002 ; Strauss and Irwin, 2004 ; Kessler and Halitschke, 2009 ; Kessler et al, 2011 ; Adler et al, 2012 ; Campbell and Kessler, 2013 ; Muola et al, 2017 ; Ramos and Schiestl, 2019 , 2020 ; Rusman et al, 2019 ; Santangelo et al, 2019 ; Egan et al, 2021 ; Table 1 ). For instance, plants profit from large, colorful flowers that attract pollinators, but such attractive signals sometimes also attract herbivores, imposing an ecological trade-off on the signals’ evolution ( Ramos and Schiestl, 2019 ; Egan et al, 2021 ). Indeed, plant-pollinator-herbivore interactions, and the mediating traits, are often interdependent and have context-dependent ecological outcomes ( Kessler et al, 2011 ; Ramos and Schiestl, 2019 , 2020 ; Santangelo et al, 2019 ; Kessler and Chautá, 2020 ; Egan et al, 2021 ; Table 1 ).…”

“…For instance, plants profit from large, colorful flowers that attract pollinators, but such attractive signals sometimes also attract herbivores, imposing an ecological trade-off on the signals’ evolution ( Ramos and Schiestl, 2019 ; Egan et al, 2021 ). Indeed, plant-pollinator-herbivore interactions, and the mediating traits, are often interdependent and have context-dependent ecological outcomes ( Kessler et al, 2011 ; Ramos and Schiestl, 2019 , 2020 ; Santangelo et al, 2019 ; Kessler and Chautá, 2020 ; Egan et al, 2021 ; Table 1 ). Predators and parasitoids are also selective agents of plant defenses, especially indirect defenses ( Kessler and Heil, 2011 ).…”