The crowding tax in parasites: linking dispersal behaviour to population growth in entomopathogenic nematodes

Abstract

1. Per capita fitness in group-living animals declines beyond an intermediate optimum, yet populations can overshoot this threshold if each newcomer still fares better in the group than alone. The resulting crowding tax (also known as Sibly tax) has been documented across free-living taxa, all of which retain the option of leaving a resource patch. 2. Parasites face a more constrained version of this trade-off. Once inside a host they cannot redistribute, and any overshoot in group size is fixed for the full reproductive bout. Whether macroparasites overshoot their fitness optimum, and what that costs the population, has remained difficult to quantify because it requires data on how parasites disperse among hosts, how they are distributed once there, and what individual fitness each of those burdens yields, all from the same system. 3. To tackle these challenges, we trace the causes and consequences of parasite dispersal behavior from individual-scale fitness to population-scale growth, using lab-experiments, mesocosms and field patterns paired with a model. We test these ideas in two species of entomopathogenic nematodes, Steinernema costaricense and S. kraussei, as a model system. 4. In mesocosms with standardized, equidistant hosts, both species dispersed as directional cohorts, generating heavy aggregation through this intrinsic behaviour. Dose-response experiments of infection, emergence and offspring production showed that per capita fitness peaks at low group sizes and drops sharply under the crowding that dispersal delivers, costing individuals 82% of their peak fitness in S. costaricense and 34% in S. kraussei. 5. Folding these fitness curves into an R0 model revealed that both species aggregate beyond the level that maximises population growth, realising 72% and 40% of their achievable R0. Applied to aggregation measured in a yearlong field survey, the model predicts that natural S. kraussei populations continue to pay this cost while natural S. costaricense populations, which aggregate far less, sit close to their own optimum. 6. Parasite aggregation in this system functions as a dispersal constraint that imposes a quantifiable fitness tax at the population level. Because the size of the tax depends on where the typical burden falls on each species' offspring curve, two species with similar dispersal behaviour can pay very different prices. The tension between individual and group interests that is central to social foraging theory therefore extends to macroparasites.