Microbiome - Hologenome Theory of Evolution

Hologenome Theory of Evolution

The hologenome theory proposes that the object of natural selection is not the individual organism, but the organism together with its associated microbial communities.

The hologenome theory originated in studies on coral reefs. Coral reefs are the largest structures created by living organisms, and contain abundant and highly complex microbial communities. Over the past several decades, major declines in coral populations have occurred. Climate change, water pollution and over-fishing are three stress factors that have been described as leading to disease susceptibility. Over twenty different coral diseases have been described, but of these, only a handful have had their causative agents isolated and characterized. Coral bleaching is the most serious of these diseases. In the Mediterranean Sea, the bleaching of Oculina patagonica was first described in 1994 and shortly determined to be due to infection by Vibrio shiloi. From 1994 to 2002, bacterial bleaching of O. patagonica occurred every summer in the eastern Mediterranean. Surprisingly, however, after 2003, O. patagonica in the eastern Mediterranean has been resistant to V. shiloi infection, although other diseases still cause bleaching. The surprise stems from the knowledge that corals are long lived, with lifespans on the order of decades, and do not have adaptive immune systems. Their innate immune systems do not produce antibodies, and they should seemingly not be able to respond to new challenges except over evolutionary time scales. The puzzle of how corals managed to acquire resistance to a specific pathogen led Eugene Rosenberg and Ilana Zilber-Rosenburg to propose the Coral Probiotic Hypothesis. This hypothesis proposes that a dynamic relationship exists between corals and their symbiotic microbial communities. By altering its composition, this "holobiont" can adapt to changing environmental conditions far more rapidly than by genetic mutation and selection alone. Extrapolating this hypothesis of adaptation and evolution to other organisms, including higher plants and animals, led to the proposal of the Hologenome Theory of Evolution.

The hologenome theory is still being debated. A major criticism has been the claim that V. shiloi was misidentified as the causative agent of coral bleaching, and that its presence in bleached O. patagonica was simply that of opportunistic colonization. If this is true, the basic observation leading to the theory would be invalid. Nevertheless, the theory has gained significant popularity as a way of explaining rapid changes in adaptation that cannot otherwise be explained by traditional mechanisms of natural selection. For those who accept the hologenome theory, the holobiont has become the principal unit of natural selection.