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The microbe-stuffed gut, rather than the genome, represents the most dynamic gene reservoir within complex, multicellular metazoa (animals). Microbes are known to confer increased metabolic efficiency, increased nutrient recovery, and tolerance of ocean acidity to basal taxa such as sponges, arguably the extant taxa most comparable to the first metazoan. We hypothesize that metazoan origins may be rooted in the capability to compartmentalize, metabolize, and exchange genetic material with a modulated microbiome. We present evidence that the most parsimonious adaptive response of clonal eukaryotic colonies experiencing oligotrophic (nutrient-limited) conditions that accompanied Neoproterozoic glaciation events, which were broadly contemporaneous with metazoan origins, is to evolve a morphological volume to harbor a densified microbiome. Dense microbial communities housed within a cavity would increase instances of horizontal gene transfer between microorganisms and host, accelerating evolutionary innovation at the genetic and epigenetic levels for the holobiont. The accelerated tempo of genetic exchange would continue until the host’s metabolic and reproductive cells became spatially and temporally segregated from one another, at which point the process is effectively suppressed with the emergence of specialized gut and reproductive tissues. This framework may lead to new, testable hypotheses regarding metazoan evolution on Earth and a more tractable means of estimating the pervasiveness of complex, multicellular animal-like life with convergent morphologies on other planets.
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