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The Hologenome Theory of Evolution: the Origins, Logic and Implications of ‘Cloud Genetics’

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The Hologenome Theory of Evolution: the Origins, Logic and Implications of ‘Cloud Genetics’ RA Jefferson “Hologenome Theory” Abstract, Gordon Conference on Animal Microbe Symbioses, June 2015 The Hologenome Theory of Evolution: The origins, logic and implications of ‘cloud genetics’ Richard A. Jefferson, Professor of Biological Innovation, Queensland University of Technology (QUT), Brisbane, QLD Australia & Cambia, GPO Box 3200, Canberra, ACT 2601 Australia [email protected] The hologenome theory of evolution developed by Jefferson (1994, 2007) proposes that natural selection occurs at the level of a holobiont comprising the population of microbial constituents together with a replication- competent macro-apobiont; in essence a populated scaffold. It asserts that the genetic composition of the holobiont comprises the contributions of the micro- and macro-biota in a form called the hologenome and that this ‘hologenotype’ is optimized by natural selection for its performance and persistence over time, but also for its plasticity and responsiveness to change. The origins of the theory hinge on studies of glucuronide metabolism by diverse vertebrate-associated microbes. The concentration and bioavailability of virtually all the steroid hormones that modulate, regulate or control reproductive performance, mate choice and ontogeny of vertebrates depends on the microbial processing and resorption of conjugated intermediaries, generally glucuronides. This process occurs in microbially-rich complex ecosystems including intestine and surface epithelia, and is mediated by glucuronidases, arylsulfatases and other enzymes encoded by the microbial constituents, and allows levels ratios of these circulating hormones and other metabolites to be adjusted by action of a dynamic population of microbes that are sampled from the environment and respond to the environment. Aspects of this phenomenon of ‘enterohepatic circulation’ have been known for decades, but had previously been viewed as an ancillary effect of detoxification and excretion of metabolites and xenobiotics The implications from this premise are many, and are non-trivial. The ability to alter and modulate, amplify and suppress, disseminate and recruit new capabilities as microbially-encoded ‘traits’ means that sampling, sensing and responding to the environment become intrinsic features and emergent capabilities of the holobiont, with mechanisms that can provide rapid, sensitive, nuanced and persistent performance changes. Hologenome theory is essentially probabilistic. The population of microbes associated with the performant microbiome of a holobiont is neither fixed nor necessarily predictable, with the holobiont behaving as an indeterminate, temporally persistent standing wave. Just as quantum theory (quantum field theory and quantum mechanics) allows a more accurate and generalizable description of physical phenomena at small and large scale both in time and space, so hologenome theory accommodates observations of the ubiquity and function of microbial populations, but also exposes observational and cognitive bias that has hitherto dominated our thinking about evolution and life sciences and their applications to society and the environment. This includes obvious impacts on health and agricultural improvement strategies, but curiously also economics and social institutions. The now classical ‘New Synthesis’ of evolution is by extension, basically a ‘Newtonian’ view of evolution and has fostered a scholarship of symbiosis that focuses on individual interactions rather than probabilistic, synergistic and dynamic populations and the complex and resilient systems these produce. At this poster, I will review the biochemical and molecular genetic experimental work underlying the articulation of the theory, and describe some of the implications of its probabilistic nature that neither require nor support the intellectual construct and memes of ‘host’ and ‘symbiont’. RA Jefferson (1994) The Hologenome in “'A Decade of PCR: Celebrating 10 Years of Amplification,' Proceedings of a Symposium” Video released by Cold Spring Harbor Laboratory Press, 1994. ISBN 0-87969-473-4. RA Jefferson (2007) “The Hologenome & Hologenomics: a Different lens on evolution” in Science as Social Enterprise. http://blogs.cambia.org/raj/2007/09/06/the-hologenome-hologenomics/ .
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