Wolbachia-Induced Unidirectional Cytoplasmic Incompatibility and Speciation: Mainland-Island Model

Arndt Telschow,Matthias Flor,Yutaka Kobayashi,Peter Hammerstein,John H Werren

doi:10.1371/journal.pone.0000701

Abstract

Bacteria of the genus Wolbachia are among the most common endosymbionts in the world. In many insect species these bacteria induce a sperm-egg incompatibility between the gametes of infected males and uninfected females, commonly called unidirectional cytoplasmic incompatibility (CI). It is generally believed that unidirectional CI cannot promote speciation in hosts because infection differences between populations will be unstable and subsequent gene flow will eliminate genetic differences between diverging populations. In the present study we investigate this question theoretically in a mainland-island model with migration from mainland to island. Our analysis shows that (a) the infection polymorphism is stable below a critical migration rate, (b) an (initially) uninfected “island” can better maintain divergence at a selected locus (e.g. can adapt locally) in the presence of CI, and (c) unidirectional CI selects for premating isolation in (initially) uninfected island populations if they receive migration from a Wolbachia-infected mainland. Interestingly, premating isolation is most likely to evolve if levels of incompatibility are intermediate and if either the infection causes fecundity reductions or Wolbachia transmission is incomplete. This is because under these circumstances an infection pattern with an infected mainland and a mostly uninfected island can persist in the face of comparably high migration. We present analytical results for all three findings: (a) a lower estimation of the critical migration rate in the presence of local adaptation, (b) an analytical approximation for the gene flow reduction caused by unidirectional CI, and (c) a heuristic formula describing the invasion success of mutants at a mate preference locus. These findings generally suggest that Wolbachia-induced unidirectional CI can be a factor in divergence and speciation of hosts.

Highlights

Reproductive parasites like intracellular bacteria Wolbachia manipulate the reproductive system of their hosts to their own benefit
The results suggest that, if recurrent peripheral populations occur, it is the ones that lose their Wolbachia that are more likely to diverge into new species, and that unidirectional cytoplasmic incompatibility (CI) can select for premating isolation by reinforcement of mate discrimination
Following Fine [38], we describe the Wolbachia dynamic by three parameters: (a) the level of cytoplasmic incompatibility, lCI, defined as the fraction of offspring that die in matings between infected males and uninfected females, (b) the fecundity reduction, f, of infected females relative to uninfected females, and (c) the transmission rate, t, defined as the fraction of offspring which inherit the infection from their mother

Summary

Introduction

Reproductive parasites like intracellular bacteria Wolbachia manipulate the reproductive system of their hosts to their own benefit. It has been shown that two Wolbachia strains can stably coexist in parapatric host populations in the face of substantial migration [26], and that bidirectional CI reduces the gene flow of locally adapted alleles and selects for premating isolation even if the transmission of Wolbachia and the level of incompatibility are incomplete [6,27,28].

Results

Conclusion