Competitor Displacement by an Herbivore that Manipulates Plant Defences

Abstract

Tetranychus evansi is an herbivorous mite specialised on solanaceous hosts, although it has also been observed to colonise non-solanaceous species. It has the ability to suppress the defences of tomato (Solanum lycopersicum), and it can displace competitors from this host using a diverse array of traits. T. evansi is an invasive species in Africa and Europe, where it often displaces native species. While recent evidence suggests that T. evansi can also suppress defences of non-solanaceous hosts, there is a lack of understanding of the molecular changes induced upon mite infestation on hosts other than tomato, as well as how these changes may impact populations of competing herbivores. Here, we investigate the transcriptomic and metabolomic responses of bean (Phaseolus vulgaris) to T. evansi infestation and to T. urticae infestation, a cosmopolitan congeneric that often competes with T. evansi for hosts in areas of co-occurrence. We ask whether the presence of T. evansi facilitates bean colonization for T. urticae, and whether the spatial distribution of mite feeding sites depends on the presence of competitors on bean leaves. We examine whether this facilitation is attributed to jasmonic acid (JA) or salicylic acid (SA) defences by treating plants with exogenous SA and JA and comparing the transcriptomes and metabolomes of bean exposed to either phytohormones or to mite feeding. Finally, we measure phytohormone concentrations and the expression of JA- and SA-responsive genes in plants infested with either mite species or co-infested with both, at different spatial scales. We found that, as previously observed on tomato, T. urticae benefits from the suppression of bean defences when sharing a leaf with T. evansi. Phytohormone treatments revealed that the reproductive performance of both species decreases with artificially induced JA defences, irrespective of the presence of SA. We found that the molecular suppression and induction of defences is mostly, but not exclusively restricted to the leaf area from where the mites feed. In full leaves co-infested with both mites, levels of marker gene induction were comparable to the inducer mite T. urticae, although not as prominent, while in smaller feeding arenas where both species fed closely to each other, the expression of a JA-responsive proteinase inhibitor was suppressed. When residing alone on a leaf, both mites had distinct preferred feeding sites with only partial overlap, but when sharing a leaf, T. evansi retained its preferred feeding site and T. urticae moved away from its own. We argue that the suppression of defences by T. evansi is mostly, although not exclusively, locally restricted, and thus the spatial distribution of individuals on the leaf is a strong determinant of competitor facilitation. This suggests that traits that displace competitors from plant tissues with suppressed defences would be under selection to co-evolve together with defence suppression.