The Evolution of Individuality

by Leo W. Buss

"This is the most stimulating book about evolution I have read for a long time."--JOHN MAYNARD SMITH, The University of Sussex `Leo Buss's ideas are almost totally new and exceedingly important. In my view this book will be a milestone in the study of evolution."-JOHN TYLER BONNER, Princeton University Leo Buss expounds a general theory of development through a simple hierarchical extension of the synthetic theory of evolution. He perceives innovations in development to have evolved in ancestral organisms where the germ line was not closed to genetic variation arising during the course of ontogeny. Variants that favor both the proliferation of the cell lineage and the organism harboring them were sequentially incorporated in an increasingly sophisticated epigenetic program. In contrast, variants that favor the replication of the cell lineage at the expense of the individual were eliminated and ultimately favored the fixation of variants that limited the production and/or expression of subsequent variation, creating a stable developmental system. The author traces the origin of the modern preoccupation with the individual as a unit of selection to its historical foundations in the works of August Weismann, exposing defects in the translation of the nineteenth-century germ-soma doctrine into modern evolutionary language. Recognizing that the germ-soma barrier is a derived evolutionary state, Professor Buss illustrates how patterns in embryonic cleavage, gastrulation, mosaicism, induction, and competence arise as a consequence of the often conflicting evolutionary interests of cells and individuals. Building on this foundation, he argues that evolution of controls over the heritability of cell lineages have come to fix developmental programs and establish heterochrony as the principal vehicle of evolutionary change. Finally, Professor Buss argues that the perspective applied to development can be generalized and applied to other transitions between units of selection that have occurred in the history of life. Leo W. Buss is Associate Professor of Biology at Yale University.

Genres: Biology

224 pages, Paperback

First published January 1, 1987

Reviews

[Samuel Rosean · Rating 4 out of 5]

If you want to begin thinking about the hierarchy of and the orders of selection, I think this is probably one of the strongest places to start. Mainly focuses on a particular hierarchy between the interests of the cell and the interests of the “individual”, but ends with a lovely expansion that extends the work to all layers of evolutionary analysis.

[Gabe Thornes · Rating 4 out of 5]

A superb little book that perhaps suffers from a now-outdated inducement to consider multi-level selective forces below the levels of population and individual organism. This was indeed a problem at the time the book was written, but has since been wholeheartedly addressed within the fields of genome evolution, cell biology and biochemistry. To give him credit though, this may indeed be a result of his book and others like it engendering change in conceptual evolutionary paradigms, meaning this treatise achieved what it set out to do. In terms of style, some of the figures are quite poor, and the legends are very sparse. The many voluminous footnotes also break the reader's flow in numerous places, with some pages containing more footnote than main body of text. Given how interesting the content of some of these notes is, I feel that Buss could have incorporated them into the main text at no detriment to the clarity of his thesis. His exposition of how individuality likely arose is highly engaging and draws on many eukaryotic examples. Four stars.

[Nate Gaylinn · Rating 5 out of 5]

A short cell biology text describing the transition from single-cellular to multi-cellular life, and the complex evolutionary dynamics at play in that moment.

In this book, Leo Buss gives his take on how to deal with the "units of selection" problem in evolution. The traditional story of evolution focuses on the individual organism as the place where selection happens. But Buss points out how "individuals" as we think of them didn't exist at first, and had to evolve from single cells, so selective pressures on individuals can't possibly explain that transition. That story of evolution also can't explain many important quirks of multicellular organisms, such as their vast (yet limited) diversity, many strange and elaborate forms of sexual reproduction, and complex multi-stage lifestyles.

Most of this text is a deep dive into the minutia of how differentiated multicellular life evolved. Buss talks about specific ancestral species, their biological quirks and limitations, and how these severely constrained life's search for possible lifestyles going forward, establishing precedents that persist to this day. He points out that multicellular life is, in fact, quite unnatural for cells and was not obviously beneficial in the very beginning. There were particular challenges to overcome, and Buss explores the biology of many species to show how life solved those problems, and to find patterns that suggest what sorts of solutions were possible or not. The story that emerges is one of collaboration by competition, aligned incentives, and mutual constraint. Each multicellular individual is the result of a tenuous and actively managed truce between cell lines and the individual they make up. Evolution is the force that built up this mechanism, and also a force to be managed, lest it break the truce and cause multicellular life to dissolve back into colonies of single cells.

I found this book equally challenging and engaging. It's quite short, but it's also incredibly dense with cell biology and highly technical discussion of evolutionary dynamics. On the other hand, Buss's theory of evolution is refreshingly new and eye-opening. It gives a powerful new perspective on a familiar problem, much like the Selfish Gene. However, Buss makes a solid argument for why his perspective is more enlightening and practically useful for evolutionary biologists. In short, these two models are compatible. The selfish gene theory lets us justify why certain counterintuitive evolutionary innovations were able to take hold. But Buss's hierarchical selection model also lets us predict what sort of innovations are possible (or not), and gives us new tools for analyzing life's great transitions.

This book blew my mind repeatedly. The world of cells is so alien and wildly complex. The challenges of survival and evolutionary pressures are totally different from what we experience at our scale. And yet, we are made of autonomous cells and we evolve by our cells evolving. There's something very powerful in understanding how and why cells came together in the first place, and how that change reshaped the evolutionary landscape on this planet.

This book gives a breathtaking new perspective on strange and complex phenomena in the microscopic world, and how they shape life at our scale. It's a technical, complicated, and mind-boggling journey, but if you stick with it, you will gain a transformative new perspective on evolution and life itself.

[J.D. Steens · Rating 3 out of 5]

Buss states that the dominant “modern synthesis” perspective provides an incomplete picture of evolutionary processes. In that view, as articulated best by Dawkins, the unit of heredity (DNA) is the same as the unit of selection.

Buss separates the unit of selection from DNA and argues that selection has occurred at each of the major transitions in life’s development, from sub-cellular (self-replicating molecules, etc.), to cells, and then to multi-cellular bodies such as ours. There is a synergistic effect at each stage between the older and newer units of selection. The new unit is a vehicle for the older and directly interacts with the environment to take advantage of new environmental niches. Yet, Buss states that the older unit of selection, while once on the front line of interaction with the environment but now removed from direct contact with the outside world, exerts a conservative force as the new unit must meet the internal test of what the older unit requires. That older unit, in effect, “says” that whatever the new unit does, it cannot jeopardize the older unit’s viability. But, in a reverse way, variation (through mutations) within the lower unit cannot jeopardize the new unit’s viability in interacting with the environment. In this way, a life form adapts to the external world by blending the old and new units of selection. Each acts on the other and makes a life form viable in the face of both internal change (mutation) and external requirements (natural selection). The end result is that our DNA is encased (and protected) in a series of “vehicles,” arranged hierarchically, that combine conservative protection of gene structure yet allow new vehicles to serve that structure by effectively dealing with the external environment.

A good part of Buss’s book is more on the technical side, but his last chapter provides a general, non-technical overview of his argument that I’ve summarized. If this summary is within the ballpark of general accuracy, then it might have elements of the following as implications for how we see ourselves: (a) The selfish interest of the gene is protected throughout this evolutionary selection process. It starts with the self-replicating molecules at our core and such self interest is extended outward in a series of “vehicles,” ending with the self interest of the human body (and ourselves). As a question, are we a “layered” self encased, in Buss’s words, in “an ever-increasing wardrobe of ‘vehicles’”? (b) The selfish interest at our core is counter-balanced by synergistic effects between higher and lower units that function together in a cooperative, utilitarian sort of way. This is also an interesting version of whole-part interaction because there’s a two-way governing and directing causality involved as the part (lower unit) limits the whole (higher unit) but the whole also limits the part. (c) As genetic variation is inherent at each unit of selection, might this have a bearing on the question of inborn character differences? The title of Buss’s book refers to the levels of evolutionary development that end up with the individual, as today’s widely understood unit of selection, but does Buss’s account also form the basis for our individuality as biological beings?