Swarthmore College Works Biology Faculty Works Biology 12-1-2012 A Symbiotic View Of Life: We Have Never Been Individuals Scott F. Gilbert Swarthmore College, [email protected] J. Sapp A. I. Tauber Follow this and additional works at: https://works.swarthmore.edu/fac-biology Part of the Biology Commons Let us know how access to these works benefits ouy Recommended Citation Scott F. Gilbert, J. Sapp, and A. I. Tauber. (2012). "A Symbiotic View Of Life: We Have Never Been Individuals". Quarterly Review Of Biology. Volume 87, Issue 4. 325-341. DOI: 10.1086/668166 https://works.swarthmore.edu/fac-biology/165 This work is brought to you for free by Swarthmore College Libraries' Works. It has been accepted for inclusion in Biology Faculty Works by an authorized administrator of Works. For more information, please contact [email protected]. A Symbiotic View of Life: We Have Never Been Individuals Author(s): Scott F. Gilbert, Jan Sapp and Alfred I. Tauber Source: The Quarterly Review of Biology, Vol. 87, No. 4 (December 2012), pp. 325-341 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/10.1086/668166 . Accessed: 14/08/2015 15:20 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to The Quarterly Review of Biology. http://www.jstor.org This content downloaded from 130.58.65.13 on Fri, 14 Aug 2015 15:20:31 PM All use subject to JSTOR Terms and Conditions Volume 87, No. 4 THE QUARTERLY REVIEW OF BIOLOGY December 2012 A SYMBIOTIC VIEW OF LIFE: WE HAVE NEVER BEEN INDIVIDUALS Scott F. Gilbert Department of Biology, Swarthmore College Swarthmore, Pennsylvania 19081 USA Biotechnology Institute, University of Helsinki 00014 Helsinki, Finland e-mail: [email protected] Jan Sapp Department of Biology, York University Toronto, Ontario M3J 1P3 Canada e-mail: [email protected] Alfred I. Tauber Department of Philosophy, Boston University Boston, Massachusetts 02215 USA e-mail: [email protected] keywords symbionts, symbiosis, individuality, evolution, holobiont abstract The notion of the “biological individual” is crucial to studies of genetics, immunology, evolution, development, anatomy, and physiology. Each of these biological subdisciplines has a specific concep- tion of individuality, which has historically provided conceptual contexts for integrating newly acquired data. During the past decade, nucleic acid analysis, especially genomic sequencing and high-throughput RNA techniques, has challenged each of these disciplinary definitions by finding significant interactions of animals and plants with symbiotic microorganisms that disrupt the boundaries that heretofore had characterized the biological individual. Animals cannot be considered individuals by anatomical or physiological criteria because a diversity of symbionts are both present and functional in completing metabolic pathways and serving other physiological functions. Simi- larly, these new studies have shown that animal development is incomplete without symbionts. Symbionts also constitute a second mode of genetic inheritance, providing selectable genetic variation for natural selection. The immune system also develops, in part, in dialogue with symbionts and The Quarterly Review of Biology, December 2012, Vol. 87, No. 4 Copyright © 2012 by The University of Chicago Press. All rights reserved. 0033-5770/2012/8704-0003$15.00 325 This content downloaded from 130.58.65.13 on Fri, 14 Aug 2015 15:20:31 PM All use subject to JSTOR Terms and Conditions 326 THE QUARTERLY REVIEW OF BIOLOGY Volume 87 thereby functions as a mechanism for integrating microbes into the animal-cell community. Recogniz- ing the “holobiont”—the multicellular eukaryote plus its colonies of persistent symbionts—as a critically important unit of anatomy, development, physiology, immunology, and evolution opens up new investigative avenues and conceptually challenges the ways in which the biological subdisciplines have heretofore characterized living entities. N THE EARLY modern period, mirroring ceptions of the planet’s biosphere. They have Ithe appearance of the independent citizen, not only revealed a microbial world of much the notion of the autonomous individual agent deeper diversity than previously imagined, but framed a biology that was organized around also a world of complex and intermingled rela- the study of particulate, interacting, living enti- tionships—not only among microbes, but also ties (Taylor 1989). Anatomical, physiological, between microscopic and macroscopic life and developmental criteria were conceived (Gordon 2012). These discoveries have pro- solely in terms of individuals, and the Darwin- foundly challenged the generally accepted ian view of life regarded aggregates of individ- view of “individuals.” Symbiosis is becoming a uals of common ancestry as identifiable units core principle of contemporary biology, and it in competition with one another. With the un- is replacing an essentialist conception of “indi- derstanding that plants and animals are com- viduality” with a conception congruent with prised of living “cells,” a new orientation the larger systems approach now pushing the quickly developed concerning the integration life sciences in diverse directions. These find- of physiological processes and anatomic units, ings lead us into directions that transcend the but still these cells were understood as agents self/nonself, subject/object dichotomies that in constructing and sustaining a singular or- have characterized Western thought (Tauber ganism that would in turn maintain its auton- 2008a,b). omy and integrity. Only with the emergence of This reorientation is not new for the micro- ecology in the second half of the 19th century bial or botanical sciences. In the world of pro- did organic systems—comprised of individu- tists, hereditary symbiosis, the inheritance of als in cooperative and competitive relation- acquired symbionts is legion. In the microbial ships—complement the individual-based world, “you are what you eat” can be taken conceptions of the life sciences. literally. In botanical science, the concept of The development of such complex formu- the autonomous individual has also been lations of individuals and systems depends on challenged by discoveries concerning rhizo- myriad factors, of which technology constitutes bia, mycorrhizae, and endocytic fungae. a major component in the characterization Nonetheless, zoologists long subscribed to a process. We perceive only that part of nature more individualist conception of the organ- that our technologies permit and, so too, our ism, since the role of microbial symbionts theories about nature are highly constrained had been more difficult to document in an- by what our technologies enable us to observe. imal evolution (Sapp 1994, 2002, 2009). We But theory and technology act on each other report here that the zoological sciences are reciprocally: we construct those technologies also finding that animals are composites of that we think are important for examining a many species living, developing, and evolv- particular perspective of nature. The develop- ing together. The discovery of symbiosis ment of the microscope, for example, revealed throughout the animal kingdom is funda- the hitherto invisible microbial world of bacte- mentally transforming the classical concep- ria, protists, and fungi; and the descendants tion of an insular individuality into one in of that instrument further allowed the disco- which interactive relationships among spe- very of subcellular organelles, viruses, and cies blurs the boundaries of the organism macromolecules. New technologies such as and obscures the notion of essential identity. polymerase chain reaction, high-throughput Our aims in this overview are to: outline RNA analysis, and next generation sequencing the data demonstrating that animals are continue to dramatically transform our con- symbiotic complexes of many species living This content downloaded from 130.58.65.13 on Fri, 14 Aug 2015 15:20:31 PM All use subject to JSTOR Terms and Conditions December 2012SYMBIOTIC VIEW OF LIFE 327 together; demonstrate how a thoroughly resides). When this symbiosis is broken by a symbiotic perspective opens important ar- prolonged increase in sea-surface tempera- eas of research and offers fundamentally tures, corals “bleach.” They lose their algal sym- new conceptions of the organism; and ex- bionts and die. Similarly, the entity we call a plore what this new evidence means for cow is an organism whose complex ecosystem biology, medicine, and for the conserva- of gut symbionts—a diverse community of cel- tion of biodiversity. lulose-digesting bacteria, ciliated protists, and anaerobic fungi—informs its specialized anat- Criteria for Individuality omy, defines its plant-digesting physiology, reg- ulates its behaviors, and ultimately determines What would biological science be if symbio- its evolution (Kamra 2005). sis were seen as the rule, not the exception? In addition to the mitochondrial vestiges What scientific