The evolution of environmentally mediated social interactions and posthumous spite under isolation by distance

Charles Mullon, Jorge Peña, and Laurent Lehmann


Many social interactions happen indirectly via modifications of the environment, e.g. through the secretion of functional compounds or the depletion of renewable resources. Here, we derive the selection gradient on a quantitative trait affecting dynamical environmental variables that feed back on reproduction and survival in a finite patch-structured population subject to isolation by distance. Our analysis shows that the selection gradient depends on how a focal individual influences the fitness of all future individuals in the population through modifications of the environmental variables they experience, weighted by the neutral relatedness between recipients and the focal. The evolutionarily relevant trait-driven environmental modifications are formalized as the extended phenotypic effects of an individual, quantifying how a trait change in an individual in the present affects the environmental variables in all patches at all future times. When the trait affects reproduction and survival through a payoff function, the selection gradient can be expressed in terms of extended phenotypic effects weighted by scaled relatedness. We show how to compute extended phenotypic effects, relatedness, and scaled relatedness using Fourier analysis, which allow us to investigate a broad class of environmentally mediated social interactions in a tractable way. We use our approach to study the evolution of a trait controlling the costly production of some lasting commons (e.g. a common-pool resource or a toxic compound) that can diffuse in space and persist in time. We show that indiscriminate posthumous spite readily evolves in this scenario. More generally, whether selection favours environmentally mediated altruism or spite is determined by the spatial correlation between an individual’s lineage and the commons originating from its patch. The sign of this correlation depends on interactions between dispersal patterns and the commons’ renewal dynamics. More broadly, we suggest that selection can favour a wide range of social behaviours when these have carry-over effects in space and time.

Published in

PLOS Computational Biology, vol. 20, n. 5, May 2024