A keeper of many crypts: a behaviour-manipulating parasite attacks a taxonomically diverse array of oak gall wasp species

Abstract

Parasites of animals and plants can encounter trade-offs between their specificity to any single host and their fitness on alternative hosts. For parasites that manipulate their host's behaviour, the added complexity of that manipulation may further limit the parasite's host range. However, this is rarely tested. The recently described crypt-keeper wasp, Euderus set , changes the behaviour of the gall wasp Bassettia pallida such that B. pallida chews a significantly smaller exit hole in the side of its larval chamber and ‘plugs’ that hole with its head before dying. Euderus set benefits from this head plug, as it facilitates the escape of the parasitoid from the crypt after it completes development. Here, we find direct and indirect evidence that E. set attacks and manipulates the behaviour of at least six additional gall wasp species, and that these hosts are taxonomically diverse. Interestingly, each of E. set 's hosts has converged upon similarities in their extended phenotypes: the galls they induce on oaks share characters that may make them vulnerable to attack by E. set . The specialization required to behaviourally manipulate hosts may be less important in determining the range of hosts in this parasitoid system than other dimensions of the host–parasitoid interaction, like the host's physical defences.

Diversity, Host Ranges, and Potential Drivers of Speciation Among the Inquiline Enemies of Oak Gall Wasps (Hymenoptera: Cynipidae)

“…Conservation of host gall morphology suggests that Synergus specialization conforms to the "Enemy Hypothesis" (Bailey et al 2009). That is: galls with similar qualities will exclude certain natural enemies and therefore similar galls will tend to be attacked by the same or similar species (Ward et al 2019). Brookfield (1972) similarly suggested that inquilines and parasitoids of galls depend more on gall morphology than other factors such as gall wasp species or tree host (note, however, that this last is belied by our data).…”

Arthropod Community Associated With the Asexual Generation of Bassettia pallida (Hymenoptera: Cynipidae)

“…This behavior facilitates E. set's escape from the crypt following completion of development (Weinersmith et al 2017). Six other cynipid gall wasp hosts of E. set have recently been identified, all residing on different oak species than B. pallida, and all of which appear to be manipulated to facilitate parasitoid emergence (Ward et al 2019).…”

“…The parasitoid subsequently emerges from the host's head capsule (Weinersmith et al 2017). E. set infects and manipulates at least six additional cynipid gall wasp hosts infecting other oak species (Ward et al 2019). The finding that E. set manipulates a broad range of cynipid gall wasps (Ward et al 2019), suggests that the mechanism E. set uses to manipulate its host either does not require extreme specialization on host physiology or involves a mechanism common to many gall wasp residents.…”

“…E. set infects and manipulates at least six additional cynipid gall wasp hosts infecting other oak species (Ward et al 2019). The finding that E. set manipulates a broad range of cynipid gall wasps (Ward et al 2019), suggests that the mechanism E. set uses to manipulate its host either does not require extreme specialization on host physiology or involves a mechanism common to many gall wasp residents. A more careful look at the gallers, inquilines, and parasitoids residing in live oak galls is warranted to determine if E. set is infecting and manipulating more hosts than just B. pallida in this system.…”

“…These live oaks are home to at least six (Egan et al 2013) and potentially twelve (Egan, unpublished data) cynipid gall wasp species, which are in turn attacked by a community of parasitoids and inquilines (Bird et al 2013, Forbes et al 2016. The cynipid gall wasps and their communities of natural enemies associated with the live oak lineage are emerging as powerful systems for answering a broad set of ecological and evolutionary questions on local adaptation (Egan and Ott 2007), natural selection (Egan et al 2011), speciation , Egan, Hood, Feder, et al 2012, Egan et al 2013, developmental plasticity (Hood and Ott 2010), and novel species interactions (Egan et al 2017, Ward et al 2019. However, the extent to which these speciesrich natural enemy communities on gall wasp host species overlap is currently unclear, and even documentation of the species present in these communities is far from complete.…”