The Organisms Fuzzy Boundary

The building of structures by animals is widespread, ubiquitous even. Sometimes these structures are humble: simple tunnels in the ground or small piles of rubble. Sometimes they are grand—the nests built by some species of termites to house their colonies are, in their own way, magnificent, even sublime. Sometimes they are built unintentionally—the tracks left by an animal passing over or through sand or mud, for example. Sometimes they are built with seeming intention, like the "fog catchment trenches" the Namib desert beetle Lepidochora uses to capture water wafted inland from the Atlantic by coastal fogs. An animal-built structure may be ephemeral, disappearing with the next tide or gust of vigorous wind, or it may be relatively permanent, solidified by mucus or reinforced with silken threads. Some edifices are the work of masons, made from grains of sand laboriously glued together one after another. Others are the work of sculptors, like the holes carved from sandstone by sea urchins. Others still are the work of miners, like the tunnels dug into trees by bark beetles, or of weavers, like the woven nests of birds or the webs of spiders. Sometimes the workmanship seems sloppy, as in the rather haphazard piles of logs and twigs in a beaver's lodge, but occasionally it reflects an orderliness and precision of technique—as in the hexagonal wax cells of a honeycomb—that simply makes your jaw drop in wonder.

This book is about animal-built structures, but it also is about a question of broader interest in the fields of biology, evolution, and ecology. Are such structures best regarded as external to the animals that build them, or are they more properly considered parts of the animals themselves? I am an advocate for the latter interpretation, but the argument I present in this book is one with a twist: that animal-built structures are properly considered organs of physiology, in principle no different from, and just as much a part of the organism as, the more conventionally defined organs such as kidneys, hearts, lungs, or livers.

The idea that external structures are properly parts of the animals that build them really is not a new idea: the notion of an "extended phenotype," as Richard Dawkins has so aptly termed it, is well established and has become respectable, if not universally accepted, wisdom in biology. My goal in this book is to bring a physiological perspective to the idea, one which, I hope, complements that of a Darwinian like Richard Dawkins. An evolutionary biologist sees the extended phenotype as the extension of the action of genes beyond the outermost boundaries of an organism and asks how these extended phenotypes aid in the transmission of genes from one generation to the next. A physiologist, however, sees an extended phenotype in terms of mechanism and asks how it works, how it alters the flows of matter, energy, and information through the organism and between the organism and its environment. Although these two perspectives certainly complement one another, I hope to show that they also lead to somewhat different conclusions about the nature of life.

The Two Biologies

The crux of the problem, for both Darwinian and physiologist, is how one perceives the organism. On the face of it, this seems an absurd statement. One of the most obvious features of the living world is that it is composed of organisms, living things that we can hold in our hands, pin down under a microscope slide, give names to, feed and care for, catalog and place in a museum case, admire from afar. In organisms we recognize individuality, intention, purposefulness, function, beingness. To entertain opinions on what organisms are seems about as rational as disputing the value of n.

Yet that is where biology in the twentieth century has brought us, to a point where it is not at all clear just what organisms are.

We have arrived at this point via two intellectual journeys, resulting, if you will, in two biologies. On one hand, modern biology has relentlessly pursued an understanding of life as a mechanism, as a special case of chemistry, physics, and thermodynamics. For the most part, this mechanistic biology has played out in the study of how cells work, even down to their uttermost details of molecular action. An unintended consequence of this inward focus has been the fading of the organism from relevance: the organism itself has become, at best, an unwelcome distraction from the fascinating cellular and molecular business at hand. It's understandable, really—the mechanistic approach to biology is hardly worth pursuing if it doesn't look for unifying principles of life, fundamentals that do not depend upon whether a living thing is plant, animal, fungus, or bacterium.

At the same time, the twentieth century has seen the emergence of neo-Darwinism as a coherent philosophy of biology. Here, too, the organism has faded from prominence, but for different reasons. To the neo-Darwinist, the organism has become essentially an illusion, a wraith obscuring the "real" biology of the selfish genes that actually run the show. An organism, to the neo-Darwinian, is at most a transient coalition of genes, bound together in a conspiracy to promote the genetic interests of its members.

Although the two biologies have each prospered in their own rights, I think it also fair to say that they have proceeded more or less independently on their respective journeys. I do not mean to say that each of the two biologies has developed in ignorance of the other—far from it. Darwinians are comforted to know, no doubt, how genes really work, what is the chemical basis of heritability and phenotypic variability, and so forth. The molecular biologist may also rest easier knowing that the question of where all life came from is firmly in the good hands of biologists who, like them, are unwilling to admit the arbitrary power of gods as explanatory tools. Nevertheless, mechanistic biology and evolutionary biology are still, more or less, independent. Let's be honest, now—to what extent, for example, have the quantum-mechanical details of protein folding really informed or challenged the thinking of evolutionary biologists? From the other side, to what extent has, say, the evolution of song dialects in sparrows really changed the course of research in cellular signaling pathways? I think an honest answer to these questions would be "Not very much." This is a pity, really, because until the two biologies merge, until fundamental questions in one challenge the fundamental assumptions of the other, there can be no claim that we are even approaching a unified science of biology.

Beyond the Obvious Organism

The concept of the extended phenotype offers one way to bridge the divide between the two biologies. Using this bridge, however, requires that we think in yet another way about the organism, as illustrated by the question with which I opened this chapter: are animal-built structures properly things external to the animals that build them, or are they properly parts of the animals themselves? If we believe that animal-built structures are strictly external to their builders, we must posit an outer boundary to the organism, something which delimits it from (to use Boolean language) the not-organism. On the face of it, this seems an easy thing to do. The outer integument of the body— whether it be sheets of chitin, or woven socks of collagen, or shells of crystallized calcite or silica—seems to distinguish organisms quite obviously from their surroundings. But are we really justified in delimiting organisms in this way?

Well, yes and no. Certainly, the outer boundary of a living organism is a tangible, obvious thing, a wrapping of some material that keeps the organism contained nicely in a compact package. But it is worth remembering the etymology of the word obvious, which begins with the Latin obvius for "in the way" and ends with the modern, and really not very reassuring, usage of "evident without reasoning or observation." There is always the possibility that a thing's "obviousness" is literally "in the way," a mask that prevents us from recognizing the thing for what it is. We must be willing to look past the obvious and ask what might be lurking beyond an organism's "outer" boundary.

Let us begin with a well-worn analogy, the supposed similarity between a turbulent eddy in a flowing stream and an organism. Eddies are familiar features of everyday life: we see one every time we pull the plug in a sink or bathtub. They are also to be found in the turbulent wakes of ships or stationary objects in moving streams, like bridge pilings in a river. Eddies develop when the inertia of a flowing fluid becomes just powerful enough to overcome the viscous forces that keep fluids flowing smoothly. Once an eddy develops, it dissipates this excess inertia as heat, giving rise to smaller eddies, which in turn give rise to still smaller eddies that merge finally into the surrounding fluid.1

Eddies are popular analogues for organisms because, on a superficial level, they seem to be so very

1. The tendency of turbulent eddies to dissipate their energy by spawning smaller eddies is summarized in a delightful bit of doggerel by L. F. Richardson (1922):

Big whorls have little whorls, which feed on their velocity; and little whorls have lesser whorls, and so on to viscosity.

Richardson's verse itself is a parody of a poem that has become a favorite ditty of entomologists:

Big fleas have little fleas upon their backs to bite 'em And little fleas have lesser fleas, And so, ad infinitum.

I am told by R. E. Lewis, the editor of The Flea Newsletter, that the original authorship of this poem has been lost. In all likelihood, though, it was inspired by Jonathan Swift, who published this rather more elegant poem in his On Poetry: A Rhapsody (1733):

So naturalist observe, a flea

Hath smaller fleas that on him prey;

and these have smaller still to bite 'em;

And so proceed ad infinitum.

Thus every poet, in his kind is bit by him that comes behind.

similar. An eddy is a highly organized entity, seemingly self-contained, whose "purpose" is to dissipate excess inertia as heat. Likewise, an organism takes in energy in the form of light or chemical fuel and uses that energy to construct orderliness, eventually dissipating it as heat. An eddy is a transient phenomenon, persisting only as long as energy is fed into it. So too is an organism—take the fuel away, and a short time later the organism ceases to exist. Of course, one can only stretch an analogy so far before it breaks. One obvious weak point is the seemingly tangible boundary separating an organism from its surroundings. You can take a knife and cut open an organism: you cannot do that with a turbulent eddy.

Now, I confess I have laid a trap for you. If we assert that the boundary of an organism confers on it an identity, a beingness that makes it distinctive from the rest of the world, must we conclude that, because an eddy lacks a distinctive boundary, it cannot have identity?

The Whirlpool

The Whirlpool

River

Devils Hole Rapids

Whirlpool Rapids

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