The Red Queen and King in finite populations

Proc Natl Acad Sci U S A. 2017 Jul 3;114(27):E5396-E5405. doi: 10.1073/pnas.1702020114. Epub 2017 Jun 19.

Abstract

In antagonistic symbioses, such as host-parasite interactions, one population's success is the other's loss. In mutualistic symbioses, such as division of labor, both parties can gain, but they might have different preferences over the possible mutualistic arrangements. The rates of evolution of the two populations in a symbiosis are important determinants of which population will be more successful: Faster evolution is thought to be favored in antagonistic symbioses (the "Red Queen effect"), but disfavored in certain mutualistic symbioses (the "Red King effect"). However, it remains unclear which biological parameters drive these effects. Here, we analyze the effects of the various determinants of evolutionary rate: generation time, mutation rate, population size, and the intensity of natural selection. Our main results hold for the case where mutation is infrequent. Slower evolution causes a long-term advantage in an important class of mutualistic interactions. Surprisingly, less intense selection is the strongest driver of this Red King effect, whereas relative mutation rates and generation times have little effect. In antagonistic interactions, faster evolution by any means is beneficial. Our results provide insight into the demographic evolution of symbionts.

Keywords: Müllerian mimicry; antagonism; mutualism; rate of evolution; symbiosis.

MeSH terms

  • Animals
  • Biological Evolution*
  • Game Theory*
  • Host-Parasite Interactions
  • Humans
  • Models, Biological
  • Mutation*
  • Population Density
  • Population Dynamics
  • Selection, Genetic
  • Symbiosis*