The “Cheshire Cat” escape strategy of the coccolithophoreEmiliania huxleyiin response to viral infection

<jats:p>The coccolithophore<jats:italic>Emiliania huxleyi</jats:italic>is one of the most successful eukaryotes in modern oceans. The two phases in its haplodiploid life cycle exhibit radically different phenotypes. The diploid calcified phase forms extensive blooms, which profoundly impact global biogeochemical equilibria. By contrast, the ecological role of the noncalcified haploid phase has been completely overlooked. Giant phycodnaviruses (<jats:italic>Emiliania huxleyi</jats:italic>viruses, EhVs) have been shown to infect and lyse diploid-phase cells and to be heavily implicated in the regulation of populations and the termination of blooms. Here, we demonstrate that the haploid phase of<jats:italic>E. huxleyi</jats:italic>is unrecognizable and therefore resistant to EhVs that kill the diploid phase. We further show that exposure of diploid<jats:italic>E. huxleyi</jats:italic>to EhVs induces transition to the haploid phase. Thus we have clearly demonstrated a drastic difference in viral susceptibility between life cycle stages with different ploidy levels in a unicellular eukaryote. Resistance of the haploid phase of<jats:italic>E. huxleyi</jats:italic>provides an escape mechanism that involves separation of meiosis from sexual fusion in time, thus ensuring that genes of dominant diploid clones are passed on to the next generation in a virus-free environment. These “Cheshire Cat” ecological dynamics release host evolution from pathogen pressure and thus can be seen as an opposite force to a classic “Red Queen” coevolutionary arms race. In<jats:italic>E. huxleyi</jats:italic>, this phenomenon can account for the fact that the selective balance is tilted toward the boom-and-bust scenario of optimization of both growth rates of calcifying<jats:italic>E. huxleyi</jats:italic>cells and infectivity of EhVs.</jats:p>