Wholobionts and Viruses
摘要
Host-associated communities are increasingly studied through the holobiont concept, which has been valuable for integrating hosts with their microbial partners across ecology and evolution. Here, we clarify its application by separating an evolutionary scale, where animals protect the germline and inherit a genome-encoded platform for managing microbial exchange through hypervariable elements and fixed genetic modules, from a within-and-across lifetime scale, where host interfaces assemble open communities from environmental pools through combinatorial elements. We restore and formalize the term “wholobiont” to name this state-dependent ecological arena of viruses, microbes, and hosts, preserving the original coral framing of the host as habitat while avoiding claims that the entire association functions as a unit of selection or a collectively inherited genome. Using corals as a focal system, we synthesize evidence for compartmentalized and context-dependent viromes and microbiomes, limited consortium-level inheritance, and stress-linked transitions to dysbiosis. We propose hypervariability and selection as unifying mechanisms: hosts deploy combinatorial elements of surface chemistry (mucins, antimicrobial peptides, diverse glycans) that bias attachment, persistence, and invasion, while viruses concentrate at boundary layers and drive transient gene fluxes that generate interaction diversity, regulate microbial mortality, mediate gene flow, and shape immune ecology at mucus and tissue interfaces. By distinguishing heritable host interface capacity from within-lifetime community assembly, the wholobiont framework explains how host-associated systems remain coherent through hypervariability and selection, with viruses acting as central regulators of stability and stress-driven transitions.