Ant-like Traits in Wingless Parasitoids Repel Attack from Wolf Spiders

Jeffrey A Harvey,Jacintha Ellers,Jonathan Gershenzon,Janine Marien,Marl Lammers,Rieta Gols,Paul J Ode,Robin Heinen,Bertanne Visser

doi:10.1007/s10886-018-0989-2

Abstract

A recent study showed that a wingless parasitoid, Gelis agilis, exhibits a suite of ant-like traits that repels attack from wolf spiders. When agitated, G. agilis secreted 6-methyl-5-hepten-2-one (sulcatone), which a small number of ant species produce as an alarm/panic pheromone. Here, we tested four Gelis parasitoid species, occurring in the same food chain and microhabitats, for the presence of sulcatone and conducted two-species choice bioassays with wolf spiders to determine their degree of susceptibility to attack. All four Gelis species, including both winged and wingless species, produced sulcatone, whereas a closely related species, Acrolyta nens, and the more distantly related Cotesia glomerata, did not. In two-choice bioassays, spiders overwhelmingly rejected the wingless Gelis species, preferring A. nens and C. glomerata. However, spiders exhibited no preference for either A. nens or G. areator, both of which are winged. Wingless gelines exhibited several ant-like traits, perhaps accounting for the reluctance of spiders to attack them. On the other hand, despite producing sulcatone, the winged G. areator more closely resembles other winged cryptines like A. nens, making it harder for spiders to distinguish between these two species. C. glomerata was also preferred by spiders over A. nens, suggesting that other non-sulcatone producing cryptines nevertheless possess traits that make them less attractive as prey. Phylogenetic reconstruction of the Cryptinae reveals that G. hortensis and G. proximus are ‘sister’species, with G. agilis, and G.areator in particular evolving along more distant trajectories. We discuss the possibility that wingless Gelis species have evolved a suite of ant-like traits as a form, of mimicry to repel predators on the ground.

Highlights

To eat or be eaten; that is one of the major paradigms among predators and their prey in ecology
We argue that the expression of ant-like traits in wingless Gelis species might be a form of ant mimicry and show that sulcatone in particular acts as a putative defense against cursorial predators like wolf spiders
G. proximus – C. glomerata, z = 4.01, P < 0.0001; G. proximus – A. nens, z = 3.54, P < 0.0001; G. hortensis – C. glomerata, z = 3.49, P < 0.0001; G. hortensis – A. nens, z = 4.17, P < 0.0001; A. nens – C. glomerata, z = 4.29, P < 0.0001. Both wingless Gelis species (G. proximus, G. hortensis) were almost completely ignored by the wolf spiders which instead fed on C. glomerata or A. nens (Fig. 2)

Summary

Introduction

To eat or be eaten; that is one of the major paradigms among predators and their prey in ecology. In a co-evolutionary framework, predators evolve adaptations that enable them to locate, subdue, and consume their prey more successfully, whereas their potential victims have evolved a suite of defenses to avoid, escape, or resist attack. Selection imposed by predators has led to a staggering array of adaptations that reduce prey susceptibility. Some species seek habitats where they are less prone to attack from natural enemies, a process known as ‘enemy-free-space’ (Jeffries and Lawton 1984; Mulatu et al 2004; Stamp 2001). Many invertebrates are cryptically colored and blend into the background of the habitat in which they are found, making it hard for visually foraging predators to locate them (Endler 1981; Starrett 1993).

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