Chemical and ecological analyses of host specificity in the facultative kidnapper ant, Formica aserva (Hymenoptera, Formicidae)

ABSTRACT/nChemical and ecological analyses of host specificity in the facultative kidnapper ant, Formica aserva (Hymenoptera, Formicidae)/nby/nKelsey Jean Scheckel/nDoctor of Philosophy in Environmental Science, Policy, and Management/nUniversity of California, Berkeley/nProfessor Neil D. Tsutsui, Chair/nKidnapper ants are specialized social parasites that exploit entire societies for resources such as brood care, foraging, and defense. These parasites raid nests of other ant species, steal the developing young, and rear them as a workforce in the kidnapper ant colony. Kidnapper ants in the genus Formica are facultative social parasites that depend exclusively on other Formica host species for initiating new colonies, but become less reliant on those same hosts over time. Facultative species have retained the ability to forage, nurse brood, and construct nests, unlike the obligate parasites that must continually replenish their population of captive hosts throughout the colony life cycle. This intermediate level of dependence on hosts suggests that facultative kidnapper ants represent a crucial step in the evolution of obligate kidnapping behavior in ants. In this dissertation, I explore the evolution of host specificity in the North American facultative kidnapper ant, Formica aserva, and how the chemical and ecological mechanisms involved in acquiring and maintaining a host population can help inform the evolutionary origins of this bizarre parasitic lifestyle. In my first chapter, I investigate the ecological groundwork of host choice in facultative kidnapper ants, as well as their effect on host community composition within the areas immediately surrounding F. aserva colonies. To do so, I measured the abundance of Formica species (hosts and non-hosts) collected at our field site in northern California, in areas were F. aserva colonies were present and in areas where they were not. I found that there was no effect on Formica species diversity based on the presence or absence of a parasite colony. Within ecological plots containing parasite colonies, there was a general preference for two of the four potential host species available to F. aserva, and parasite colonies using F. accreta as hosts were located in areas where F. accreta was the most abundant host species in the community. These findings suggest that facultative kidnapper ants do not have an effect on the overall community composition of other Formica species. However, within areas that contain parasite colonies, some host species are more abundant than others and F. aserva may be selecting hosts based on their ecological availability. In my second chapter, I examine the chemical ecology of mixed-species colonies containing F. aserva workers and their captive hosts and compare them to free-living colonies of host and non-host Formica species to assess the chemical similarity between parasite workers and their preferred hosts. Overall, F. aserva cuticular hydrocarbon profiles were distinct from all the other Formica species (free-living hosts and non-hosts) at our field site, and host species were just as chemically different as non-host species from F. aserva workers. Chemical comparisons of captive and free-living host species revealed stark differences in the overall cuticular hydrocarbon composition between these groups, and captive species were more chemically similar to their heterospecific nestmates than they were to their free-living conspecifics. Based on these results, captive hosts appear to be assimilated into a parasite-centric recognition odor profile. I conclude that F. aserva has not evolved to mimic host recognition odors, like obligate kidnapper ants do, but instead, retains its specific recognition cues which are then shared with cohabitating host workers. In the third chapter of my dissertation, I study the chemical deception techniques used by facultative kidnapper ants for maintaining mixed-species colonies. We separated F. aserva workers from their Formica hosts by creating experimental nests containing pure species groups, then examined the cuticular hydrocarbon profiles of parasite and host workers before and after separation. I report a significant difference in the hydrocarbon profiles of captive hosts before and after removal from physical contact with their parasitic nestmates. In contrast, the chemical profiles of F. aserva workers underwent only small changes after separation from host species. These chemical changes also corresponded with behavioral changes, such as greater displays of aggression between heterospecific nestmates when reintroduced after a long period of physical separation. The minor changes we observed in the chemical profiles of parasites after removal from hosts relative to the greater changes we observed within the host species suggest that facultative kidnapper ants are using a parasite-centric strategy for manipulating captive host workers. It appears that the parasites homogenize the mixed-colony odor with their dominant odors, effectively dampening the species- and colony-specific cues of their hosts through the physical transfer of hydrocarbons. The results of my dissertation provide an understanding of the mechanisms involved in the host choice and chemical deception strategies of facultative kidnapper ants. Studies like this, that investigate the chemical ecology and life history of facultative parasites, will facilitate a better understanding of the evolution of social parasitism overall, as well as provide general insights into the coevolution of hosts and parasites.

Advisor: Tsutsui, Neil D.