How disease constrains the evolution of social systems

Abstract

Animal populations are occasionally shocked by epidemics of contagious diseases. The ability of social systems to withstand epidemic shocks and mitigate disruptions could shape the evolution of complex animal societies. We present a mathematical model to explore the potential impact of disease on the evolutionary fitness of different organizational strategies for populations of social species whose survival depends on collaborative efficiency. We show that infectious diseases select for a specific feature in the organization of collaborative roles-cohort stability-and that this feature is costly, and therefore unlikely to be maintained in environments where infection risks are absent. Our study provides evidence for an often-stated (but rarely supported) claim that pathogens have been the dominant force shaping the complexity of division of labour in eusocial societies of honeybees and termites and establishes a general theoretical approach for assessing evolutionary constraints on social organization from disease risk in other collaborative taxa.

Keywords: animal societies; demography; evolutionary resilience; infectious diseases; population modelling; social structure.

Figure 1.

The dynamics of task allocation and individual movement with different strategies. Individuals enter the population at time t = 0 and assigned to one of four tasks X = (x₁, x₂, x₃, x₄) either uniformly (fixed, random) or based on their age (discrete, repertoire). The duration of time spent in a task varies with different strategies. Explanatory example. Fixed: individuals remain in their natal task until death. Discrete: individuals spend a fixed amount of time in their natal task before progressing to a specific next task. Task switching occurs at the same time for all cohort members (e.g. age 0 → x₁, age 1 → x₂, and so on). Repertoire: individuals gain access to new tasks as they become older and switch among these tasks (uniformly) at stochastically chosen intervals during their lifetime. The ability to switch tasks is indicated by a line connecting the subpopulations. Random: individuals can change tasks at any point in life regardless of their age. The potential effects of social organization on pathogen transmission risks are also shown. At time t = 1, a single individual is chosen from the population and designated as infectious (red). The infection spreads with frequency-dependent transmission probabilities specified from an S-I epidemic model. The transmission risk is greater within tasks versus between tasks. The population-level impacts of disease will depend on the mobility of infected individuals as well as task-specific demographic rates. Births and deaths are not included in the figure. (Online version in colour.)

Figure 2.

Task switching maximizes demographic robustness in the absence of infections. We use Monte Carlo methods to evaluate how well different strategies perform under environmental exposure (i.e. non-infectious mortality risk). We ask whether a population's ability to produce collaborative benefits over an expected lifespan is differentially altered by strategies that constrain individuals' task roles (fixed, discrete) compared to strategies that allow for more flexible roles (random, repertoire). An evolutionarily favourable strategy should safeguard populations against stochastic extinction (i.e. avoidance of small population sizes). The plots show the median amount of benefits generated during simulations (y-axis) against the median size of surviving populations at the end of simulations (x-axis). The depth median for each strategy (indicated by crosses) is centred on a shaded ‘bag' region that contains 50% of the distribution. The outer polygon denotes convex hull that is 3 times the size of the bag region. Considering the location, spread and skew of the output distributions, we conclude that a strategy of randomized task switching can maintain populations within viable bounds without sacrificing productivity. (Online version in colour.)

Figure 3.

Task switching increases population vulnerability to stochastic epidemics. We test the robustness of different organizational strategies to outbreaks of a frequency-transmitted disease. Barplots summarize outputs of simulations with a disease outbreak (epidemic) compared simulations without an outbreak (baseline). Differences seen across strategies from baseline to infectious conditions are not the same for productivity (a) as for survival (b). (Note: this figure shows the subset of cases consistent with senescence theory in which older individuals undertake the riskier, but more beneficial tasks.)

Figure 4.

Risk exposure from epidemics is lowest in populations with age-based social organization. The expected cost of an epidemic is defined as the share of population assets (work output and population numbers) lost when an outbreak occurs (i.e. percentage difference from baseline conditions, in figure 3). Our model predicts a lower risk exposure for populations with age-determined task roles (discrete) compared to populations where individuals have lifetime task assignments (fixed). (Online version in colour.)