Department of Integrative Biology, University of Guelph, Guelph, Ontario, N1G 2W1, Canada.
Ecology. 2021 Dec;102(12):e03506. doi: 10.1002/ecy.3506. Epub 2021 Aug 31.
Indirect species interactions are ubiquitous in nature, often outnumbering direct species interactions. Yet despite evidence that indirect interactions have strong ecological effects, relatively little is known about whether they can shape adaptive evolution by altering the strength and/or direction of natural selection. We tested whether indirect interactions affect the strength and direction of pollinator-mediated selection on floral traits of the bumble-bee pollinated wildflower Lobelia siphilitica. We estimated the indirect effects of two pollinator predators with contrasting hunting modes: dragonflies (Aeshnidae and Corduliidae) and ambush bugs (Phymata americana, Reduviidae). Because dragonflies are active pursuit predators, we hypothesized that they would strengthen pollinator-mediated selection by weakening plant-pollinator interactions (i.e., a density-mediated indirect effect). In contrast, because ambush bugs are sit-and-wait predators, we hypothesized that they would weaken or reverse the direction of pollinator-mediated selection by altering pollinator foraging behavior (i.e., a trait-mediated indirect effect). Specifically, if ambush bugs hunt from plants with traits that attract pollinators (i.e., prey), then pollinators will spend less time visiting those plants, weakening or reversing the direction of selection on attractive floral traits. We did not find evidence that high dragonfly abundance strengthened selection on floral traits via a density-mediated indirect effect: neither pollen limitation (a proxy for the strength of plant-pollinator interactions) nor directional selection on floral traits of L. siphilitica differed significantly between high- and low-dragonfly abundance treatments. In contrast, we did find evidence that ambush bug presence affected selection on floral traits via a trait-mediated indirect effect: ambush bugs hunted from L. siphilitica plants with larger daily floral displays, reversing the direction of pollinator-mediated selection on daily display size. These results suggest that indirect species interactions have the potential to shape adaptive evolution by altering natural selection.
间接种间相互作用在自然界中普遍存在,其数量往往超过直接种间相互作用。尽管有证据表明间接相互作用对生态有很强的影响,但对于它们是否可以通过改变自然选择的强度和/或方向来塑造适应性进化,人们知之甚少。我们测试了间接相互作用是否会影响传粉媒介介导的对熊蜂授粉的野生花卉半边莲的花部性状的选择强度和方向。我们估计了两种具有不同捕猎模式的传粉者捕食者的间接效应:蜻蜓(蜻科和齿蛉科)和伏击性臭虫(Phymata americana,猎蝽科)。由于蜻蜓是主动追逐捕食者,我们假设它们会通过削弱植物-传粉者相互作用来增强传粉媒介介导的选择(即密度介导的间接效应)。相比之下,由于伏击性臭虫是坐等捕食者,我们假设它们会通过改变传粉者的觅食行为来削弱或改变传粉媒介介导的选择的方向(即性状介导的间接效应)。具体来说,如果伏击性臭虫从吸引传粉者的植物(即猎物)上捕猎,那么传粉者将减少访问这些植物的时间,从而削弱或改变对有吸引力的花部性状的选择方向。我们没有发现高蜻蜓丰度通过密度介导的间接效应来增强对花部性状的选择的证据:花粉限制(植物-传粉者相互作用强度的代理)或半边莲花部性状的定向选择在高和低蜻蜓丰度处理之间没有显著差异。相比之下,我们确实发现伏击性臭虫的存在通过性状介导的间接效应影响了对花部性状的选择:伏击性臭虫从半边莲植物上捕猎时,会选择花朵更大的植物,从而改变了传粉媒介介导的对每日花朵大小的选择方向。这些结果表明,间接种间相互作用通过改变自然选择有潜力塑造适应性进化。