Weak sinks could cradle mutualistic symbioses - Strong sources should harbour parasitic symbioses

Abstract

Using a population model of selection on an obligate symbiont and its host, we evaluate how demographic differences across geographical landscapes can produce selection mosaics in interacting species. The model assumes that the host populations vary geographically from demographic sources to sinks in the absence of effects by the symbionts, and that a virulent and a relatively avirulent form of the symbiont compete with one another across all habitats. Our results indicate that productivity gradients can create selection mosaics across habitats, resulting in complex fitness landscapes over which evolution occurs. We find that relatively virulent symbionts only persist if they have an advantage over avirulent strains or species in terms of interference (i.e. competition, and/or cross-transmission) interactions. When such a trade-off exists, we predict that the more virulent symbiont is most likely to be found in habitats where host population growth is highest, whereas the more avirulent symbiont should tend to persist in more marginal habitats or even habitat sinks for symbiont-free hosts. Demographic sinks may be the habitats most likely to favour the origin of new mutualisms. Very productive mutualisms can be exploited by hyperparasites or cheaters. We discuss our findings in terms of geographical scenarios for the emergence of mutualisms, and the long-standing debate about geographical patterns in the maintenance of sex.