Aurore Franco-Ricord

Symbiosis is a form of reticulate evolution that refers to ecological, physiological, and genomic associations between organisms from different species, resulting in interactions, bonds, coexistence, cohabitation, and partnerships. Symbiosis can lead to the emergence of new biological individuals, known as holobionts, that simultaneously function as new units and levels or life zones of evolution. When symbiosis becomes permanent and hereditary, it leads to symbiogenesis or evolution through symbiosis. This entry focuses on the history of the symbiosis theory. Symbiosis research emerged in the 18th century in both botany and zoology, driven by ecological studies of associations between different organisms. Ecological symbiosis research is intellectually rooted in the fields of natural philosophy and natural history. Like the theory of natural selection, theories of symbiosis were initially linked to sociocultural and political ideas about the organizational structure of society, as well as to debates on the nature and redistribution of “common goods” and the “division of labor” in the “economy of nature.” Symbiosis jargon, in part, drove the development of the biomedical and physiological sciences, where scholars commenced research on the influence microorganisms and viruses have on health and disease. Research on the evolutionary impact of symbiosis emerged in the late 19th century, following the discovery of intracellular symbiosis and its role in the origin of cellular structures. This helped pave the way for theories on symbiogenesis.

Symbiogenesis denotes host and/or symbiont evolution through long-term symbiosis. Studied and defined multiple times over in the early 20th century by independently working scholars, including Famintzin, Mereschkowski, Kozo-Polyansky, Wallin, and Lederberg, symbiogenesis was brought to the attention of contemporary evolutionary science from the 1960s onward through the comprehensive works of Lynn Margulis who defined symbiogenesis as “the origin of a new organ, metabolic pathway, behavior, tissue, or other feature as a result of long-term hereditary symbiosis, [. which] includes the process by which organelles of the eukaryotic cell evolved from ancient bacterial symbionts.” Symbiogenesis is today wellrecognized for underlying the evolution of mitochondria and chloroplasts, which are eukaryotic cell organelles that originated from bacteria that engaged in endosymbiotic relationships with some of the earliest nucleated cells, some 2 billion years ago. Not confined to that period in time, endosymbiosis, or the phenomenon where organisms live inside other organisms (endosymbionts live inside a host), is quite common amongst eukaryotic organisms that often carry varied microbial communities in their body cavities and, albeit to a lesser extent, inside specific cells (intracellular endosymbiosis). This entry details the events that led to the formulation and wider academic recognition of symbiogenesis theory, its opposition to certain tenets of the Neodarwinian synthesis, and its integration into the emerging Reticulate Evolution school. As such, this entry presents a historical account of what was once a marginal theory that has now become essential for understanding the evolution of life.