Luigi Pontieri:
Discrimination behavior in the supercolonial pharaoh ant

Date: 15-06-2014    Supervisor: Jes Søe Pedersen

The majority of eusocial insect species live in small, kin structured colonies that are mutually aggressive and rarely interact. By contrast, a restricted group of ant species show a peculiar social organization called unicoloniality, where colonies can grow to vast networks of geographically separated but mutually tolerant nests, also referred to as “supercolonies”. Many unicolonial ants are invasive, as their introduced supercolonies attain huge size and cause severe economic and ecological damage, affecting in particular species composition and functioning of ecosystems. There is therefore an increasing need to understand which factors promote the ecological dominance of these species, and particularly how the discrimination of both conspecifics and heterospecifics (including parasites) might influence structure and ecological success of invasive populations. In this PhD thesis I investigated the discrimination behavior of the invasive pharaoh ant (Monomorium pharaonis) as a model for other invasive and supercolonial ant species. The pharaoh ant is one of the few ant species that can be reared in the laboratory for many generations. Furthermore, the possibility to do controlled crosses of colonies provides the unique opportunity to establish colonies of different genetic composition. These traits make this species a suitable study subject to set up behavioral experiments that aim to investigate which factors, and to which extent, might influence the inter- and intraspecific discrimination abilities of invasive ants.

In the first chapter I focused on the nestmate recognition system of pharaoh ants, investigating whether the cues used for discrimination had a genetic origin and how different level of within-colony genetic diversity and relatedness influenced the discrimination abilities of the colonies. I show that, despite a general ability of discriminating nestmates from non-nestmates, the degree of relatedness between colonies did not influence the overall level of discrimination. Furthermore, I found that genetically low-diverse colonies displayed better discrimination abilities than high diverse ones and that low genetically diverse colonies discriminated high diverse non-nestmates better than vice versa.

In the second chapter I investigated whether the high genetic differentiation characterizing natural colonies of pharaoh ants is sufficient to prevent unrelated colonies to fuse and how different levels of genetic similarity shape the outcome. By pairing laboratory colonies in a fusion assay, I show that the majority of unrelated colonies fused despite high initial levels of aggression. Moreover, I also found that the initial aggression was positively correlated with the chemical and genetic distance between colony pairs, further confirming the important role of endogenous cues in the nestmate recognition of this species.

The third chapter presents a methodological study on the best procedures for identifying chemical compounds used for nestmate recognition in social insects. We first compiled datasets of cuticular hydrocarbons (CHCs) and aggression between colonies of three species of ants (Formica exsecta, Camponotus aethiops and Monomorium pharaonis) and a simulated dataset. Then, using the available information about the exact cues used for nestmate recognition in F. exsecta, we evaluated the power of different combinations of data transformation and chemical distance calculation in differentiating between true nestmate recognition (NMR) cues and other compounds. We found that particular combinations of statistical procedures are more effective in differentiating NMR cues from other compounds. We also developed a new method for centroid calculation that increased the power of the analysis and can therefore be used in future studies that aim to identify nestmate recognition cues in other species.

In the fourth chapter I investigated the nest site preference of pharaoh ant colonies and, specifically, their ability to avoid nests containing infectious pathogens as invasive, supercolonial ants are hypothesized to be particularly prone to disease. Using binary choice tests between three types of nests, I found that migrating colonies surprisingly preferred nest sites containing nestmate corpses overgrown with sporulating mycelium of the generalist fungus Metarhizium brunneum. This unexpected finding can provide new insight into the important co-evolution of social insects and their pathogens.