Cytoplasmic incompatibility in hybrid zones: infection dynamics and resistance evolution

J Evol Biol. 2022 Feb;35(2):240-253. doi: 10.1111/jeb.13974. Epub 2022 Jan 11.

Abstract

Cytoplasmic incompatibility is an endosymbiont-induced mating incompatibility common in arthropods. Unidirectional cytoplasmic incompatibility impairs crosses between infected males and uninfected females, whereas bidirectional cytoplasmic incompatibility occurs when two host lineages are infected with reciprocally incompatible endosymbionts. Bidirectional cytoplasmic incompatibility is unstable in unstructured populations, but may be stable in hybrid zones. Stable coexistence of incompatible host lineages should generate frequent incompatible crosses. Therefore, hosts are expected to be under selection to resist their endosymbionts. Here, we formulate a mathematical model of hybrid zones where two bidirectionally incompatible host lineages meet. We expand this model to consider the invasion of a hypothetical resistance allele. To corroborate our mathematical predictions, we test each prediction with stochastic, individual-based simulations. Our models suggest that hybrid zones may sustain stable coinfections of bidirectionally incompatible endosymbiont strains. Over a range of conditions, hosts are under selection for resistance against cytoplasmic incompatibility. Under asymmetric migration, a resistance allele can facilitate infection turnover and subsequently either persist or become lost. The predictions we present may inform our understanding of the cophylogenetic relationship between the endosymbiont Wolbachia and its hosts.

Keywords: Wolbachia; SLiM; host-parasite cophylogeny; intracellular endosymbionts; mathematical model; reproductive parasitism.

MeSH terms

  • Animals
  • Arthropods*
  • Cytoplasm
  • Female
  • Male
  • Reproduction
  • Symbiosis
  • Wolbachia*