This blog post is provided by L Marescot, M Franz, S Benhaiem, H Hofer, C Scherer, M L East, and S Kramer-Schadt and tells the #StoryBehindThePaper for the paper “‘Keeping the kids at home’ can limit the persistence of contagious pathogens in social animals” which was recently published in the Journal of Animal Ecology.

In 2015, Stephanie Kramer-Schadt, head of the Ecological Dynamics Department and Marion East, head of the Serengeti Spotted Hyena Research project at the Leibniz Institute for Zoo and Wildlife Research in Berlin, welcomed Lucile Marescot, Sarah Benhaiem and Mathias Franz as postdocs to study the role of social and demographic processes in controlling epidemic dynamics in the context of a DFG-funded project. This project was partly based on field-data on a virulent epidemic of canine distemper virus (CDV) in a social carnivore, the spotted hyena (see Marescot, Benhaiem et al. 2018 and Benhaiem, Marescot et al. 2018). Extending from this case study, a theoretical modelling approach was then used to investigate the role of communal nurseries in limiting the spread of infectious pathogens in group-living species, resulting in the present study.

The spotted hyena: a model species to study complex social processes

Field-data from spotted hyenas in the Serengeti National Park, Tanzania, originated from a long-term research project initiated in 1987. Spotted hyenas live in clans, which are social units that can reach up to 100 individuals and which defend territories. Each clan member acquires through social processes a social rank in a linear dominance hierarchy, in which adult females and their offspring dominate adult immigrant males. Females are philopatric and nurse their cubs for at least the first 12 months of life. During this denning period, juveniles stay in the vicinity of the clan’s communal den(s).

From the age of one year juveniles start accompanying their mothers on long-distance foraging trips outside the clan territory. During these “commuting trips”, the risk of encountering hyenas from other clans increases, which elevates the risk of infection of individuals and more generally pathogen transmission between clans.

CDV: a model of respiratory disease with airborne transmission mode

CDV is one of the most infectious diseases of carnivores and is considered a threat to wild carnivores worldwide. Contrary to covid-19 for instance, it confers lifelong immunity to individuals who survived infection. Juveniles often contribute the most to pathogen spread as they are less likely to be immune than older individuals. When most adults in the population have acquired  immunity to a pathogen, its chance of spreading or persisting will be curtailed, especially if only adults participate in between-group contacts. This regulating process is called herd immunity. It occurs when there are sufficient immune individuals to ensure epidemic fade-out. The role of herd immunity in preventing pathogen spread can be strengthened and accelerated by locking down and/or vaccinating certain individuals, particularly so-called “superspreaders”. In species that rear their offspring in communal burrows, dens, lairs or crèches within group territories or home ranges (“communal nurseries”) such as the spotted hyena, juveniles have limited interactions with adults from other groups during their development, which may slow down the spread of the pathogen.

A theoretical study bringing insights for the understanding of pathogen transmission in social networks

Despite the evolutionary advantages of sociality, such as foraging, predatory defence or thermoregulation, life in groups is often associated with fitness costs associated with an increased risk of pathogen spread. In this context, empirical and theoretical studies showed that pathogens can exert a selective force on social and behavioural traits such as group-size, division of labour, mating systems or even dominance and may thereby play a role in the evolution of social interactions in highly organized societies. However, the effects of communal nurseries on pathogen persistence is unclear, as are the mechanisms explaining the potential benefits of this form of  protection against infection, i.e. the prolonged communal housing of young, regardless of their degree of relatedness to visiting  adults. Such species include spotted hyenas, yellow-bellied marmots Marmota flaviventris, where all males and most females leave the colony one year after birth, grey wolves Canis lupus, where juveniles stay in communal burrows for six months and begin to hunt, potentially encountering members of other groups after about ten months of age, sperm whales Physeter macro-cephalus, whose calves less than one year old stay at the surface with related females while the mother dives to hunt or Nile crocodiles Crocodylus niloticus which keep their offspring in crèches for about two years.

In the present study, a Susceptible-Infected-Recovered (SIR) model was developed to assess the impact of communal nurseries in social hosts on pathogen transmission and persistence. The results indicated that for any pathogen which confers lifelong immunity, regardless of its degree of virulence, whether highly infectious or not, for a long or short infection period, epidemics were always more likely to fade out in hosts rearing their young in communal nurseries than in group-living species where young could contact members of other groups from an early age, such as European rabbits Oryctolagus cuniculus.

In the “One Health” goal context advocated by the WHO, individuals with high contact rates to members of their own group are often targeted for vaccination to control pathogen spread. Our results suggest that considering heterogeneity of contacts in the social network is another important factor to account for in epidemiological surveillance, and that interventions focused on individuals with high between-group contact may be particularly effective at limiting pathogen spread in some social species. However, as the study remains theoretical, this idea remains to be validated with clinical data from various host-pathogen systems. Variation in the durations of the communal nursery, period of pathogen incubation or of the protective period from immunisation could also be further investigated, to include more realistic and complex aspects.

Read the paper

Read the full paper here: Marescot, L., Franz, M., Benhaiem, S., Hofer, H., Scherer, C., East, M. and Kramer-Schadt, S. (2021), ‘Keeping the kids at home’ can limit the persistence of contagious pathogens in social animals. J Anim Ecol. Accepted Author Manuscript. https://doi.org/10.1111/1365-2656.13555