Ítalo Mendes Delazari

Parasites frequently manipulate host behavior to increase their own fitness, but the proximal mechanisms underlying these manipulations remain poorly understood. In interactions between polysphinctine parasitoid wasps and spiders, hosts are induced to build modified and more resistant webs (cocoon webs). This construction is currently attributed to the activation of the host's innate ecdysis mechanism, based on the cocoon web's similarity to spider molting webs and the association with elevated levels of the hormone 20-hydroxyecdysone (20E) in Araneidae species. However, the only empirical evidence of 20E enhancement is taxonomically restricted, limiting generalization. In this study, we investigated this ecdysis-based manipulation mechanism in a Tetragnathidae spider host. Examining the interaction between the spider Leucauge volupis (Keyserling, 1893) and the polysphinctine wasp Hymenoepimecis cameroni (Townes, 1966), we compared the architecture of normal, molting, and cocoon webs of the spider, and quantified 20E levels across the spider’s group. Cocoon webs shared traits with molting webs, such as the absence of sticky spirals and increased reinforced radii. However, contrary to expectations, 20E levels were not elevated in behaviorally altered spiders compared to the other groups. Therefore, although cocoon webs resemble molting webs, ecdysone does not appear to be the proximate trigger of host manipulation in this system, suggesting that their structural similarity arises from alternative physiological or behavioral pathways yet to be identified.

Certain parasites improve their fitness by manipulating their host’s behaviour. Some evidence suggests that parasites exploit innate pathways in the host to manipulate their behaviour. Furthermore, phylogenetically unrelated parasites can generate similar behavioural changes in hosts from the same taxonomic group. Spiders are hosts for several parasites that appear to induce behavioural changes, such as building modified webs that may benefit the parasites. Additionally, some observations on spiders parasitized by Ichneumonidae wasps suggest that the construction of modified webs may merely result from activating the innate ecdysis process. Considering that different parasites may use similar manipulation pathways, we review and examine evidence in the literature that phylogenetically distant parasites (wasps, dipterans, and fungi) may converge on the manipulation mechanism of host spiders through activation of the preexisting mechanism of ecdysis. Also, we suggest that webs built by fungus-infected spiders represent an extended phenotype of these parasites. We conclude that the strategy of behavioural manipulation through activation of innate ecdysis in hosts may have converged in the different spider parasites, which have been favoured over evolutionary time. Therefore, we propose possible pathways for activating this mechanism, and provisions for future investigations to test these hypotheses.

Strategies to invade and exploit hosts for survival are an essential part of the parasitic lifestyle. Species of the Polysphincta genus group (Hymenoptera: Ichneumonidae), which utilize spiders as hosts, are examples of parasitoids that present several behavioral strategies in host immobilization and egg laying. In this study, we characterized the oviposition behavior of the Darwin wasp Hymenoepimecis cameroni Townes, 1966 (Hymenoptera: Ichneumonidae) on their host spider, performed the taxonomic description of the female, and redescribed the male parasitoid. We observed eight H. cameroni females endeavoring to parasitize young Leucauge volupis (Keyserling, 1893) spiders. Each female made up to 12 successive attempts at oviposition, totaling 36 observed attacks, with only two successful attacks. The main oviposition behavior of H. cameroni individuals consists of flying close to the web and performing a direct attack on the spider, which often results in the spider escaping into the vegetation. We observed that in seven events where the spiders fled into the vegetation, the individuals of H. cameroni adopted a second strategy, which consisted of hanging from the hind legs in the web hub. This observation showed that the females of H. cameroni have the ability to modulate the oviposition strategy after a failure in the initial attack. The pattern observed for the attack of H. cameroni indicates that the ability to adjust the approach could be specific to the behavioral habits of L. volupis.