Predicting distributions of Wolbachia strains through host ecological contact-Who’s manipulating whom?

Abstract

Reproductive isolation in response to divergent selection is often mediated via third-party interactions. Under these conditions, speciation is inextricably linked to ecological context. We present a novel framework for understanding arthropod speciation as mediated by Wolbachia, a microbial endosymbiont capable of causing host cytoplasmic incompatibility (CI). We predict that sympatric host sister-species harbor paraphyletic Wolbachia strains that provide CI, while well-defined congeners in ecological contact and recently diverged noninteracting congeners are uninfected due to Wolbachia redundancy. We argue that Wolbachia provides an adaptive advantage when coupled with reduced hybrid fitness, facilitating assortative mating between co-occurring divergent phenotypes-the contact contingency hypothesis. To test this, we applied a predictive algorithm to empirical pollinating fig wasp data, achieving up to 91.60% accuracy. We further postulate that observed temporal decay of Wolbachia incidence results from adaptive host purging-adaptive decay hypothesis-but implementation failed to predict systematic patterns. We then account for post-zygotic offspring mortality during CI mating, modeling fitness clines across developmental resources-the fecundity trade-off hypothesis. This model regularly favored CI despite fecundity losses. We demonstrate that a rules-based algorithm accurately predicts Wolbachia infection status. This has implications among other systems where closely related sympatric species encounter adaptive disadvantage through hybridization.