Abstract
The role of intraspecific variation in the magnitude and direction of plastic responses in ecology and evolution is increasingly recognized. However, the factors underlying intraspecific variation in plastic responses remain largely unexplored, particularly for the hypothesis that the herbivores’ phenotypic response to predators might vary amongst lineages associated with different host plants. Here, we tested whether plant-specialized lineages of the pea aphid, Acyrthosiphon pisum, differed in their transgenerational phenotypic response to ladybird predators (i.e., the asexual production of winged offspring by wingless mothers). In a full factorial laboratory experiment, we found that six aphid clonal lineages each specialized either on alfalfa or clover significantly differed in their transgenerational phenotypic response to predators. Some lineages produced an increased number of winged aphids in predator presence while others did not respond. Aphid lineages specialized on alfalfa had stronger phenotypic responses to predators than those specialized on clover. Although we tested only six aphid lineages from two biotypes, our results imply that intraspecific variation in prey phenotypic response of herbivores to predators differs amongst lineages specialized on different host plants. Our findings therefore raise the question of the influence of plant specialization in shaping herbivore phenotypic responses, and highlight the need to consider multi-trophic interactions to understand the causes and consequences of intraspecific variation in complex phenotypic traits.
Highlights
One promising avenue to better understand the ecology and evolution of plant-herbivore and herbivore-predator interactions is to go beyond bi-trophic interactions and consider adjacent trophic levels[1,2]
Our study sought to elucidate whether (1) genetically distinct aphid lineages differed in their transgenerational plastic response to predators, (2) biotypes characterised by different histories of host-plant specialization differed in their plastic responses and (3) aphid plastic response to predators depends on their vulnerability to predators
We found that the proportion of winged aphids was affected by the interaction between aphid lineage and predator treatment (χ2 = 75.17; df = 5; p < 0.0001)
Summary
One promising avenue to better understand the ecology and evolution of plant-herbivore and herbivore-predator interactions is to go beyond bi-trophic interactions and consider adjacent trophic levels[1,2]. Price et al.[1] emphasised the importance of considering plant traits, abundance, and spatial distribution to better understand predator-prey interactions and the evolution of herbivore traits This tri-trophic view has proven valuable for explaining intraspecific variation in herbivore resistance to pathogens and parasitoids[4,5]. Plastic responses to predators are common in many taxa and play an important role for predator and prey population dynamics and coevolution[14] These responses, often referred to as trait-mediated or non-consumptive effects[15,16], can encompass behavioural changes such as habitat shift, reduction in activity, altered feeding rate as well as changes in life history traits and morphology (e.g., defensive structure, colour, shape)[14,17,18,19,20,21,22,23]. Even in the absence of extensive lineage replication within biotypes allowing us to conclude and generalise on the evolutionary significance of this mechanism, we expected aphids from the Alfalfa biotype to show stronger plastic responses to predators than aphids from the Clover biotype
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