Symbiogenesis: the holobiont as a unit of evolution

ABSTRACT

Symbiogenesis is the result of the permanent coexistence of various bionts to form the holobiont (namely, the host and its microbiota). The holobiome is the sum total of the component genomes in a eukaryotic organism; it comprises the genome of an individual member of a given taxon (the host genome) and the microbiome (the genomes of the symbiotic microbiota). The latter is made up of the genes of a variety of microbial communities that persist over time and are not eliminated by natural selection. Therefore, the holobiome can also be considered as the genomic reflection of the complex network of symbiotic interactions that link an individual member of a given taxon with its associated microbiome. Eukaryotic individuals can be analyzed as coevolved, tightly integrated, prokaryotic communities; in this view, natural selection acts on the holobiont as if it were an integrated unit. The best studied holobionts are those that emerged from symbioses involving insects. The presence of symbiotic associations throughout most of the evolutionary history of insects suggests that they were a driving force in the diversification of this group. Support for the evolutionary importance of symbiogenesis comes from the observation that the gradual passage from an ancestral to a descendant species by the accumulation of random mutations has not been demonstrated in the field, nor in the laboratory, nor in the fossil record. Instead, symbiogenesis expands the view of the point-mutation-only as the unique mechanisms of evolution and offers an explanation for the discontinuities in the fossil record («punctuated equilibrium»). As such, it challenges conventional paradigms in biology. This review describes the relationships between xylophagous insects and their microbiota in an attempt to understand the characteristics that have determined bacterial fidelity over generations and throughout evolutionary history (AU)

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