A primer on symbiosis

In this lecture, I will introduce you to the “classical” concept of symbiosis, established by the 19^th century scientist Anton de Bary. This scheme categorizes symbiosis into three broad categories: mutualism, where both partners benefit, parastitism, where one partner benefits at the expense of the other, and commensalism, where neither partner benefits or is harmed. Despite this scheme being very popular and widespread, it is, in many ways, a distorted view of the phenomenon of symbiosis.

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Here, we will delve into the details of a “classical” symbiotic association: the mutualism between fungi and photosynthetic micro-organisms that we know as the lichen. The classical story of the lichen is that it is a mutualism. The photosynthetic partners provide carbohydrates to the fungi and the fungi provide a moist shelter for the photosynthesizers. A detailed look at how lichen function reveals that the supposed mutualism looks more like a parasitism. This underscores the difficulty of trying to fit symbiosis into neat categories like mutulism or parasitism.

Symbiosis is better defined by the physiological interaction between the symbiotic partners than by trying to jam an association into a neat category. Symbiosis is ultimately a manipulation of matter and energy flows through their partners, and this leads us to a definition of the “symbiotic organism”: an association of different organisms that is like an organism physiologically. Symbiosis is sustained by “open-loop” flows of matter and “closed loop” flows. “Open loop” flow is illustrated by the cycling of nitrogen through microbial mat communities. “Closed loop” flow is illustrated by the cycling of nitrogen between coral polyps and their photosynthetic symbionts, their zooxanthellae.

A physiological conception of symbiosis allows us to characterize symbiosis by the effect of the partnership on metabolism of the respective partners. This makes symbiosis not a matter of categories (i.e. mutualism, parasitism, commensalism), but a balance of physiological costs and benefits. Because these can change depending upon circumstance, this means that the nature of a symbiotic association is dynamic, capable of shifting from one state to another. This is illustrated by the phenomenon of coral bleaching, where the coral polyps expel their photosynthetic partners en masse, and try to re-establish a new suite of symbiotic partnerships.

Symbiosis is not just a physiological association, it is an evolutionary one. As such, the formation, dynamics, permanence and function of a symbiosis has been subject to natural selection. The “classical” conception of symbiosis imagined that symbiotic associations followed a predictable arc from parasitism to mutualism or commensalism as they evolved, the argument being that it was in the selective interests of all partners not to kill or disadvantage the other. Parasites would, therefore, always evolve toward “accommodation” with their hosts. This neat story not only misunderstands the nature of Darwinian natural selection, it obscures the complex selective games that play out in a symbiotic association. This is illustrated by the symbiosis between fig trees and fig wasps, which, depending upon circumstance and strain, can evolve either toward mutualism or parasitism.

Symbiosis has long been presented as a kind of “biological curiosity”, worthy of attention because they are supposedly rare and wonderful to behold. However, symbiosis is emerging as a fundamental property of life, with symbiosis playing a vital role in all aspects of life. This undermines not only our standard conception of the organism, it also undermines many of the presuppositions and tenets of modern Darwinism. This has led to the emergence of a radically new theory of evolution known as symbiogenesis, in which evolution is driven not by mutation and selection of genes, but by evolving associations of entire genomes. Symbiogenesis not only accounts for the ubiquity of symbiosis in the biosphere, it also provides a superior explanation for the major evolutionary events of life on Earth. I illustrate this with Lynn Margulis’ conception of the symbiogenic evolution of the eukaryotic cell.