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Predicting distributions of Wolbachia strains through host ecological contact -- who's manipulating whom?
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  • Clive Darwell,
  • Daniel Souto-Vilaros,
  • Jan Michalek,
  • Sotiria Boutsi,
  • Brus Iusa,
  • Mentap Sisol,
  • George Weiblen,
  • Vojtech Novotny,
  • Simon Segar
Clive Darwell
National Science and Technology Development Agency
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Daniel Souto-Vilaros
Charles University Faculty of Science
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Jan Michalek
Czech Academy of Sciences
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Sotiria Boutsi
Harper Adams University College Department of Crop and Environment Sciences
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Brus Iusa
New Guinea Binatang Research Center
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Mentap Sisol
Binatang Research Center
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George Weiblen
University of Minnesota
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Vojtech Novotny
Institute of Entomology, Czech Academy of Sciences
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Simon Segar
Harper Adams University College Department of Crop and Environment Sciences
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Abstract

Barriers to gene-flow within populations, typically in response to divergent selection, are often mediated via third-party interactions. Under these conditions speciation is inextricably linked to ecological context. We present a novel framework for studying arthropod speciation as mediated by Wolbachia, a microbial endosymbiont capable of causing host cytoplasmic incompatibility (CI) via alternative strain associations. Building on empirical findings, our model predicts that sympatric host sister-species harbour paraphyletic 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 may provide an adaptive advantage when coupled with reduced hybrid fitness (via trait mismatching), by facilitating assortative mating between co-occurring divergent phenotypes – the contact contingency hypothesis. To test this, we applied a custom-built predictive algorithm to empirical data from host-specific pollinating fig wasps, achieving ≤88.46% accuracy. We then considered post-zygotic offspring mortality during CI matings by developing a model featuring fitness clines across oviposition resources. This oviposition trade-off model, tested through simulation, favoured CI at realistic conspecific mating frequencies 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 hybridisation.