The ecology, epidemiology, and evolution of parasites infecting ants (Hymenoptera: Formicidae)

Open Access
- Author:
- Quevillon, Lauren Elise
- Graduate Program:
- Biology
- Degree:
- Doctor of Philosophy
- Document Type:
- Dissertation
- Date of Defense:
- April 11, 2018
- Committee Members:
- David Peter Hughes, Dissertation Advisor/Co-Advisor
Andrew Fraser Read, Committee Chair/Co-Chair
Jessica Maral Conway, Committee Member
Peter John Hudson, Committee Member
Jessica Maral Conway, Outside Member - Keywords:
- Ants
social insects
epidemiology
evolution
ecology - Abstract:
- Ants (Hymenoptera: Formicidae) are one of the most ecologically dominant groups of organisms on Earth, despite being characterized by life histories that exacerbate the potential for infectious disease epidemics. Understanding how ants have interacted with their parasites over ecological and evolutionary time is crucial for understanding their ecological success. My dissertation aims to advance our knowledge by investigating three broad questions: (1) which parasitic organisms infect ants and what are their associated life history and ecological traits, (2) what are the epidemiological impacts of these parasites on colony functioning, and (3) how do ants mitigate the impacts of their interactions with parasitic organisms. First, I extensively survey the known pathogens, parasites, and parasitoids of ants (hereafter `parasites') and find that most parasites require the death of individual ant hosts as a developmental necessity, only need one ant host to complete their life cycle, and must leave the nest before transmitting to their next ant host. I find that most parasites infecting ants come from the Order Diptera, Phylum Fungi, and Order Hymenoptera, and there are very few viruses and bacteria known to infect ants. I also find that our knowledge of parasites infecting ants is very poor- out of 333 recognized ant genera, only 81 have parasites reported to infect them. Next, I model the epidemiological consequences of the most prevalent parasite transmission mode, parasites transmitting outside the nest, on ant colony dynamics. Using a deterministic modeling framework, I explore how colony birth rate, parasite infection rate, the proportion of the colony foraging, and parasite seasonality impact colony growth dynamics. I find that for biologically reasonable parameter values, colony collapse is not predicted to occur, suggesting that the majority of parasites known to infect ants may not be posing a significant threat to colony survival, though their impacts on colony-level phenotype and fitness remain unknown. I extend this work to model the consequences of the few parasites of ants known to use direct, nest-mate to nest-mate (`in-nido') transmission strategies by using a stochastic modeling approach. I find that contrary to the `ex-nido' parasites modeled previously, colony collapse is much more likely to occur. However, I find that collapse can be mitigated through the use of two behavioral defenses that ant colonies have in their arsenal: social avoidance and cadaver management. Finally, I investigate whether ant colony organization might be optimized to reduce the transmission of infectious diseases by using social network analysis to understand carpenter ant social and spatial organization in the absence of disease. I focus on trophallaxis, the oral sharing of food, as the key social interaction of interest because ant colonies must balance efficient food flow with reducing disease transmission. First, I assess whether forager ants, which serve as potential carriers of infectious agents, behave differently in their network interactions and nest spatial usage than their non-foraging nest mates. I find that foragers are both socially and spatially distinct from their non-foraging counterparts, and never engage in direct interactions with queens. Next, I extend this work by investigating whether the temporal structure of ant trophallaxis networks might be protective through either temporal or social filtering processes. I find that while foragers and queens are socially segregated, there is no evidence for nuanced organizational immunity through the temporal structuring of ant trophallaxis networks. This dissertation synthesizes our current knowledge of parasites infecting ants and provides theoretical models for how these parasites epidemiologically interact with their hosts, providing the foundation for future empirical studies.