Parasites, by definition, decrease host fitness and the introduction of a parasite into one or more competing host species can substantially alter the ecological landscape resulting in or preventing the extinction of one competitor(24, 25). Symbionts that are parasitic in the absence of inter-species host competition but which increase the competitiveness of infected hosts (for example, through allelopathy(26)) establish a seemingly surprising, mutualistic relationship. Similarly, host competition can admit the persistence of a parasite under conditions where persistence within a single host population is not supported(25). Furthermore, even within a single host species, symbionts that are parasitic in one environment can provide a fitness advantage due to specialized adaptations in another environment, for example, promoting resistance to drought(27).
Parasitic interactions can also substantially alter intra-species competition due to variability in tolerance or transmissibility influenced by genomic or nongenomic factors including host density(28) and age. In previous human epidemics, advanced age has been commonly associated with increased(4, 5) or occasionally decreased(5, 6) morbidity and mortality. More generally, species lifespans are likely influenced by pathogen interactions. Populations of species with short lifespans are able to clear pathogens faster, and being short-lived decreases the probability of crossing the species barrier, which typically requires major adaptations to emerge within the first infected novel host to mediate efficient transmission(29).
Age structure substantially alters transmission dynamics, and can reduce the likelihood of an epidemic while increasing the magnitude in the event of an outbreak(30). The presence of immune post-reproductive hosts decreases the density of susceptible hosts and reduces the rate of infection; however, susceptible, and senescent, post-reproductive hosts can increase the cumulative number of mortalities. The disparity in predicted outcomes between homogenous (which may already lead to diverse results(31, 32)) and age-structured populations is exacerbated in the event of vaccination(33).
Here we demonstrate that host age structure, associated with differential susceptibility to a parasite, can determine whether a virulent pathogen, as defined by its relationship with individual hosts, is a parasite or a mutualist with respect to the population as a whole. In competitive populations where older, post-reproductive hosts share resources with younger, potentially reproductive hosts, virulent pathogens that disproportionately affect non-reproductive hosts increase the population growth rate. Conversely, in collaborative populations where older, post-reproductive hosts aid in the reproduction of younger hosts, the cost of the loss of a non-reproductive host can be even greater than that of a young host.
Although post-reproductive lifespans appear to be rare, even among mammals(7), most if not all cellular life forms exhibit some form of senescence(8–12). Therefore, although advanced social roles for post-reproductive members have not yet been identified outside of mammals, costs and potentially benefits associated with the presence of senescent hosts are likely widespread even for unicellular life. Among prokaryotes, horizontal gene transfer from dead, maximally senescent, cells can prevent irreversible genomic deterioration, Muller’s rachet(34). In addition to chronological age, altering the stationary cell cycle phase distribution(35, 36) can modify the fitness landscape by altering phase-dependent gene expression(37) potentially delegating different functions to individuals in different phases. Thus, collaborative populations might be far more common across the diversity of life than is immediately obvious.
These, often complex, impacts of age structure have to be taken into account prior to formulating a strategy for intervention against a pathogen, mitigation of invasive species, or preservation of an endangered population(38). For example, food provisioning both increases resource availability and host aggregation, potentially amplifying pathogen invasion(39). Thus, in the context of competition, which may itself be magnified as a result of host aggregation, the effect of a pathogen likely enhances conservation efforts, whereas in the case of collaboration, this straightforward intervention could lead to population decline.