Pathogens, parasites, and parasitoids of ants: a synthesis of parasite biodiversity and epidemiological traits

Abstract

1.AbstractAnts are among the most ecologically successful organisms on Earth, with a global distribution and diverse nesting and foraging ecologies. Ants are also social organisms, living in crowded, dense colonies that can range up to millions of individuals. Understanding the ecological success of the ants requires understanding how they have mitigated one of the major costs of social living-infection by parasitic organisms. Additionally, the ecological diversity of ants suggests that they may themselves harbor a diverse, and largely unknown, assemblage of parasites. As a first step, we need to know the taxonomic and functional diversity of the parasitic organisms infecting ants. To that end, we provide a comprehensive review of the parasitic organisms infecting ants by collecting all extant records. We synthesize major patterns in parasite ecology by categorizing how parasites encounter their ant hosts, whether they require host death as a developmental necessity, and how they transmit to future hosts.We report 1,415 records of parasitic organisms infecting ants, the majority of which come from order Diptera (34.8%), phylum Fungi (25.6%), and order Hymenoptera (25.1%). Most parasitic organisms infecting ants are parasitoids (89.6%), requiring the death of their host as developmental necessity and most initially encounter their hosts in the extranidal environment (68.6%). Importantly, though most parasitic organisms infecting ants only need a single host to complete their life cycle (89.2%), the vast majority need to leave the nest before transmission to the next ant host can occur (88.3%), precluding ant-to-ant transmission within the nest. With respect to the host, we only found records for 9 out of 17 extant ant sub-families, and for 82 out of the currently recognized 334 ant genera. Though there is likely bias in the records reported, both host and parasite ecological traits and evolutionary histories underlie the pattern of ant-parasite association reported here. This work provides a foundation for future work that will begin to untangle the ecological drivers of ant-parasite relationships and the evolutionary implications thereof.

Modeling the impact ofex-nidotransmitted parasites on ant colony dynamics

“…Our investigation of colony dynamics in the presence of exnido parasites, i.e. parasites that require a developmental period outside of the nest before transmission to new hosts, is motivated by the biology of the most prevalent type of antinfecting parasite that we find from our extensive review of the literature (13), parasite records in (12,29,(33)(34)(35)(36)(37), among many others). We model a parasite that encounters and infects a forager ant in the extranidal (outside of the nest) environment, causes the mortality of that ant after some developmental period, and ultimately transmits to its next host in the extranidal environment (i.e.…”

“…Note that infected foragers are included in the calculation of the total colony size and we assume that there are no infection-related changes in individual or colony-level behavior. In addition, infected foragers are always assumed to die (there is no recovery from infection), which is realistic given that most parasites known to infect ants require ant death as developmental necessity (13 most results we assume that the parasite is constantly present in the environment, though we also explore the potential impacts of seasonality in the force of infection term β, which may arise due to seasonal fluctuations in parasite population size or prevalence. We also formally explore the impacts of changing the parasite-induced mortality rate in Fig.…”

“…Only foragers are exposed to ex-nido parasites.. We are investigating parasites infecting ant colonies via an ex-nido mode of transmission, which requires extranidal parasite exposure in order to become infected (13). In many ant societies, this means that only foragers are at risk because only foragers leave the relatively protected confines of the nest.…”

“…Additionally, neighboring colonies overlap in their foraging ecology and compete for the same food resources, enhancing the potential for inter-colony transmission (10,11). Indeed, social insects are host to a diverse range of pathogens, parasites, and parasitoids (hereafter 'parasites') (12,13). However, ants and other social insects have achieved incredible ecological success (14,15), and effectively managing their disease burden could be one underlying reason for their continued success over evolutionary time.…”

“…However, the majority of parasite species that infect ants have lifecycles that require a period of development outside of the colony ('ex-nido'), often as free-living stages or in other host species, before they are able to infect new hosts ( Fig. 1) (12,13). The amount of time such parasites need before they are capable of infecting a new ant host varies considerably, from days to months or even years.…”