UC Berkeley

Parasites contribute greatly to the generation of the planet's biodiversity, exploiting all levels of the biological hierarchy. Examples range from selfish DNA elements within genomes to social parasites that invade whole societies. Slave-making ants in the genus Polyergus are obligate social parasites that rely exclusively on ants in the genus Formica for colony founding, foraging, nest maintenance, brood care, and colony defense. To acquire their slave labor, Polyergus workers raid neighboring Formica colonies for brood to bring back to their colony. In this dissertation, I explore the interaction between North American Polyergus slave-making ants and their slaves in the genus Formica to gain a better understanding of the possible coevolutionary dynamics between them.

In the first dissertation chapter, I investigate how enslavement by Polyergus breviceps affects the nestmate recognitions system of its hosts, Formica altipetens. To do this I compared the chemical, genetic and behavioral characteristics of enslaved and free-living Formica colonies. I found that enslaved Formica colonies were both more genetically and chemically diverse than their free-living counterparts. Enslaved Formica workers were also less aggressive towards non-nestmates compared to free-living Formica. These results suggest that parasitism by Polyergus dramatically alters both the chemical and genetic context in which their kidnapped hosts develop such that it may affect how they recognize nestmates.

In the second chapter of my dissertation, I study how the presence of multiple host species in sympatry shapes the chemical and genetic structure of a single population of Polyergus breviceps. To successfully adapt to a particular host, slave-making ants may mimic or camouflage themselves with the species-specific chemical cues that their slaves use to recognize and accept nestmates. If such host specialization should continue through several generations, genetic structuring according to host may occur. I collected both chemical and genetic data from Polyergus colonies from the same locality parasitizing three different species of Formica. I concluded that the Polyergus from this location can be distinguished chemically according to host species and there is sufficient genetic evidence from both maternally and biparentally inherited markers to propose that host-races have formed in this species of slave-maker.

My final chapter examines the phylogeography and population structure of two currently recognized species of North American Polyergus (P. breviceps and P. lucidus) and the hosts that they enslave (Formica spp). I used sequence from one mitochondrial gene (cytochrome oxidase I) and three nuclear genes (28S, elongation factor 1-alpha, arginine kinase) to reconstruct the ancestor-descendent relationships between several populations of Polyergus and the different species of Formica they enslave. Additionally, I subjected the DNA sequence data to a Bayesian method of species delimitation to explore North American Polyergus species boundaries. Lastly, I use the mitochondrial DNA sequence data to consider the relative effects of geography and host species on the population genetic structure of P. breviceps and P. lucidus. On the whole, North American Polyergus populations generally follow a broad west-east phylogeographic pattern, and can be divided into three distinct species: P. breviceps as two species and P. lucidus as it is currently recognized. Although population structuring of P. breviceps can be primarily explained by geography and to some extent host species, P. lucidus population structure is more strongly dictated by host association and not by geographic distribution.

Overall, the results from my dissertation provide insight into the interaction between a social parasite and its host at both ecological and evolutionary timescales. Because of their ecological diversity, widespread distribution and unique evolutionary trajectory, Polyergus slave-makers and their Formica hosts present a unique case study of possible host-parasite coevolution.