BIOLOGICAL INDIVIDUALITY
(c) Ronald de SousaNo cow’s like a horse,
And no horse like a cow;
That’s one similarity
Anyhow.”
Piet Hein
Most living things are very unlike you and me. We humans have traditionally thought of ourselves as some sort of evolutionary pinnacle; but all we are really entitled to claim is that we are an oddity, an eccentric by-way in the history of life. Part of what makes us different is that we come in portions that are self-contained, complex packages of differentiated cells, sexually engendered, ephemeral, unique, never to recur; we are, in short, individuals. How did we come to be that way? As a result of what evolutionary strategies? How does it make us different from other living things? And what more is there to being a biological individual than could be figured out more or less a priori, as necessary and sufficient conditions for being a countable, particular thing? Such are the questions I propose to address.
Criteria of individuation that work well enough for metazoan animals like ourselves are problematic when we try to identify and count biological organisms in other phyla. A priori discussions of strange cases derived from imagination, frequently found in the literature on persons, are unhelpful, not only because the preoccupation with persons biases the notion of individual towards issues of personality rather than biological entities, but also because millions of years of evolution are likely to have done a better job in setting out the possible alternatives than even the liveliest imagination.[1] In the light of bizarre cases, we have a choice between insisting on a weak criterion of individuality that will fit the entire gamut of biological diversity, and a strong one which will exclude most living things. The second view, I will argue, casts the clearer light on the living world as a whole and on ourselves in particular.
The question of the nature of biological individuals also touches on a still simmering debate in evolutionary biology, concerning the units of selection. On this, I shall say only very little, in a coda mainly intended to suggest that the debate is grounded on equivocation, or that perhaps, as has recently been argued by Denis Walsh (2004), there is really no real issue at all, but just a false problem based on erroneous presupposition about the logical status of natural selection.
Apart from its intrinsic interest, a clarification of the concept of biological individuality can be expected to help sharpen the philosophical understanding of individuality, which is of interest in other areas, particularly the vigorous ongoing discussion about externalism, the extent to which we can understand psychological predicates to supervene on properties possessed intrinsically by individuals, without the need for contributions from communal facts or causal histories. This too, I shall entirely leave aside, after firing off a quick drive-by shot in the footnote to the present sentence.[2]
Particularity, Specificity, Uniqueness
In order to isolate the contribution that biology can make to our conception of individuality, we need first to ask how far logic, or the sort of mix of logic and common sense that Strawson (1963) called “descriptive metaphysics”, can take us. That turns out to be surprisingly far, as may be suggested by a quick tour through some traditional puzzles and the maneuvres they have inspired.
Identity and difference, individuality and particularity, have long given rise to puzzles, some trivial, some deep. Nothing is more common than uniqueness. All things are alike in being just their particular selves. And as Leibniz insisted, all things are alike in being different from every other.
Individuals are particular, specific, and often unique. These properties are distinct, but often confused. One cause, or perhaps symptom, of confusion is that we often say: ‘that specific one,’ when we mean that particular, or ‘nothing in particular’, when we really mean nothing specific. Yet specificity and particularity are entirely distinct: specificity qualifies descriptions and admits of degrees, particularity is a logical property that qualifies entities and is absolute. As for uniqueness, we make fun of people who say: “He’s very unique!”, yet since uniqueness admits of, or indeed requires, to be relativized to respects, comparatives do make sense in that one thing might be unique in more ways than another.
Depending on which aspect of individuals is being stressed, what is important about individuals may look very different.[3]
A thing is a particular thing though it exist in a million copies; indeed, if something logically cannot be copied (the number 5, for example), that is a sign that it is not an individual. The fact that the number 5 cannot be cloned might be thought to make it unique, but that is a unique sort of uniqueness, for ordinary uniqueness is contingent (it is always logically possible for there to be another thing just like this one), but the number 5 is necessarily the only thing that's just like that.
Since something can be unique only in some respects, a judgment of uniqueness requires us to distinguish which, among the infinite properties of a material object, are the ones that count as making the object unique. This presupposes a normative criterion: a judgment of uniqueness is meaningless in the absence of respects you care about, at least in the minimal sense of being those you are interested in for the purposes at hand. Insofar as individuals are held to be unique, this minimal element of normativity will infect any judgment that something is an individual. Here, then, biology may get its first toe-hold in the discussion. For as theological sources of normativity have withered away, evolutionary biology seems to promise a substitute, demystified form of intelligible teleology, in the concept of biological function, defined in terms of the shaping force of natural selection. Philosophers formerly appealed to metaphysical ideas to supplement and give bulk to logical or analytical concepts; so the inevitability of substantive judgments may provide a natural opportunity to look to biology for an elaboration of the concept of individual.
The Paradox of Change.
Before we come to that, however, we may note that the puzzles mentioned above all have the annoying sophistical flavour of an early Socratic dialogue. While there may be more profit in pursuing them than at first appears,[4] I will not let them detain us here. But one more puzzle is worth a detour, because it introduces the crucial dimension of time, and can be thought of as the implicit common root of both Presocratic and Aristotelian metaphysics. This is the paradox of change.
The Ionian philosophers are often credited with having invented the difference between the “manifest image” and the “scientific image” of underlying reality.[5] One fact of experience that drives this preoccupation is the fact of change, the very concept of which involves this paradox: For anything to change, it must remain the same. If there is no enduring subject, there is nothing to which the change can be attributed. Some, like Whorf (1973) and “process metaphysicians” such as Whitehead, have contended that this is a mere prejudice bequeathed us by the dominant trend in Greek thought, which smothered the Heracleitean insight; but even if it is true that everything flows, the flowing must be ascribed either to a base of unchanging properties or to a grid of unchanging locations (Plato taught us this lesson in the Theaetetus). Otherwise looking around a fixed and unmoving environment becomes indistinguishable from a judicious combination of change of place with protean transmutation. So if the paradox of change is inescapable, as I believe, then one is forced into some choice among potential constants. The choice may or may not settle on individuals among the constants: Platonic forms are constants without being individuals, and so is a mere spatio-temporal grid.
Strawson and Aristotle
Some years ago, P. F. Strawson (1959) argued that reference to individuals presupposes the capacity to reidentify physical particulars in a space of physical particulars, of which some at least can be picked out in terms of “token reflexives”—terms such as I, now, or here, which are understood in terms of the punctual location of the speaker. But the capacity for identification involved itself presupposes the solution to some prior problems. In order for something to count as an identifiable individual, it must have boundaries and be capable of independent existence in some stretch of space-time, allowing for re-identification as distinct from the identification of qualitative similarity. Thus, as Aristotle noted, it might be possible to identify the whiteness of this paper, but that presupposes that we can reidentify this paper.[6] The paper exists independently of its whiteness, but not vice versa.
This obvious and seemingly innocuous fact poses three closely related problems.
First, dependency can admit of degrees, and so the requirement of independence presupposes a further decision as to what is sufficiently independent to count as a full-fledged individual. (We are forced, again, into a normative judgment.)
Second, it requires a prior decision to regard the whiteness of the paper as accidental, so that the paper could be, while the whiteness could not be, the thing that stays the same while it changes colour. (Plato might have said instead that the whiteness stays ever constant even while it switches substrates.)
Third, when I have identified essential characteristics of an individual, I can identify conditions that would amount to destroying them. This suffices to sort events or processes according to their relation to the interests of the individual in question. The distinction between essential and accidental properties is therefore one step away from attributions of teleology, for once interests have been identified one can ask whether anything occurs because of them.
All three of these issues, which are roughly those that motivated Aristotle’s quest for substance, have been powerful engines of metaphysical diligence.
Both Spinoza and Leibniz took the criterion of independence most seriously. For Spinoza this leads, more geometrico, to the inference that there can be only one substance, since there can be at most one thing the existence of which is completely independent (Spinoza 1985). If there were two, each would limit the other, and thus contradict the hypothesis of their full independence. For Leibniz, it yields the even more gloriously mad view that while the “true atoms of nature” are many, they can have neither parts, nor beginning, nor end, nor interaction with one another (Leibniz 1991). Had Aristotle taken the requirement of independence to similar extremes, he no doubt would have been as little interested in biology as were Leibniz and Spinoza. For since each individual part of God-or-Nature is subsumed under the teleology of the whole, any residual individual purposes can be of only minor interest. Instead Aristotle thought of biological organisms as sufficiently independent to count as genuine substances; and while the universe as a whole might have borne some analogy to a huge and deathless organism, “Nature”, with its own inherent ends, the paradigm substances were things whose “natures” contained in themselves their principle of change but were nevertheless liable to dissolution and death. What was more, it was precisely in the part of the individual that guaranteed its capacity for dissolution and death, namely in its matter, that Aristotle located the particularity of the individual: thus he remarked that Socrates and Callias, being alike in form, could differ only in their matter (Aristotle 1984, Metaphysics 34a6). All this brings Aristotle’s conception of the nature of substances remarkably close to our own common-sense conception of an organism, though one element is implicit which Aristotle and Strawson forbore explicitly to mention:[7] competition and the possibility of conflict. I therefore propose this characterization of minimal individuals:
(MI) Minimal individuals occupy determinate chunks of space-time, therefore can dislodge one another. The minimal concept of an individual includes the possibility of competition for existence in space.
The inclusion of the possibility of competition at this rock-bottom level of the characterization of individuals is distasteful to many. But I don't see how it can be evaded. Attempts to ignore the economic point of view quickly show their incoherence. Witness, for example, Margulis & Sagan who charge that “vogue words like ‘competition’, ‘cooperation’, ‘mutualism’, ‘mutual benefit’, ‘energy costs’, and ‘competitive advantage’ have been borrowed from human enterprises and forced on science from politics, business, and social thought.” (Margulis and Sagan 2002, 16). According to them, “members of the thought collectives of sociobiology, population genetics, or population ecology” are merely using the “jargon” of “bioeconomic just-so stories.” (Margulis and Sagan 1986, 6-7). Yet a few pages after the latter passage they remark that “autopoeisis is not an option for a living being—it is an imperative.” That claim, like the hypothesis endorsed by Margulis and Sagan (1986) that sex began as a DNA repair mechanism, presupposes that there were already “minimal individuals.” For both “self-construction” and “repair” imply a distinction between functioning and malfunctioning, which must relate to the interests of some entity. This implies a distinction between what is this or that individual entity and what is not, and in any world not blessed with infinite space and wealth it follows that two such individuals might make a bid for the same location or resources. To that extent, the concept of an individual organism is actually less a product of specifically scientific thinking in biology than it is the outcome of ratiocination more or less a priori on the basis of meditating on the paradox of change in the light of the common-sense notion of a changing thing.
Characterizations of biological individuals by contemporary biologists and philosophers give us little more than we could have garnered from Aristotle's metaphysical quest for a definition of primary substance. Stephen J. Gould (1990), for example, in a lecture about biological individuals, lists five defining characteristics: birth, death[8], “relative stability”, offspring, and inheritance (p.29). Of these, only the last goes beyond the features deducible from the concept of a countable thing. David Hull says: “By ‘individuals’ I mean spatio-temporally localized cohesive and continuous entities” (Hull 1978, 336); Leo Buss (1987) initially characterizes an individual as “a physiologically distinct discrete organism.” (Preface, fn.2).
How much contingency?
Though it is physics, rather than biology, which has traditionally been thought most likely eventually to merge with mathematics, the idea that what characterizes biological individuals is actually a set of properties that can be deduced more or less a priori from common sense makes it look as though the nature of life is not, after all, contingent. For the features of (MI) derivable from conceptual analysis are roughly those summarized by Gould (2002, 602-603) as constituting the “vernacular” concept of individuality: discreteness, change, continuity, and functional organization. And yet many biologists have stressed that the existence of life as we know it, and especially of intelligent life, is utterly contingent, a cosmic historical accident. (Gould 2002, 133-43). To see why, we need to look at the properties that characterize biological individuals in addition to those of what I have called “minimal individuals.” In his last work, (Gould 2002, 608-610) added four other properties specific to biological individuals in the full sense, the inclusion of which is motivated by the fact that they play a crucial role in the processes of evolution. These are reproduction, inheritance, variation, and interaction. Similarly Jack Wilson, in addition to the basic properties of particularity, historicity, and functional integrity, lists having a common genotype, being a product of developmental process, and functioning “as an important unit in an evolutionary process.” (Wilson, J. 1999).
Once these properties are added to our list, it becomes clearer that there might have existed no biological individual in the full sense, no individual-as-we-know-it (IAWKI). But what precisely are the alternatives to a world of biological individuals? How, if at all, could there have been life without individuals?
I have already alluded to Plato’s demonstration in the Theatetus that there couldn’t be a changing world without some dose of constancy. But this doesn’t tell us what needs to be constant and what can be allowed to change. In the real world of biology, the two logical alternatives mentioned above—a mere spatio-temporal grid, or Platonic Forms—are of no interest because they don't allow for even minimal individuals. But there are unclear cases, and they can yield the beginnings of an answer to the question of where, exactly, lies the contingency that underlies the existence of individuals as we know them. Before I come to list a few of these, however, it is worth noting a real example of the paradox of change leading to perplexity in biological thinking.
A real world example of the paradox of change.
The example comes from a paper by Marcel Weber (1966). The problem Weber sets himself is whether there could be selection for the existence of molecular variety generators (MVG). (These are genes which somehow make mutations more likely in specified regions). George C. Williams had argued a priori that this would be impossible, since any MVG would automatically increase the likelihood of its own mutation into extinction. The only conceivable direction for selective pressure would be towards a mutation rate of zero (Williams 1966, 139, quoted Weber p.70.) So there is first a problem about what continuing individual type might be favoured by such increased mutation rates. Weber finds an ingenious way around this, pointing out that the presence of an MVG might, in heterogeneous environments, increase the probability of survival of members of the lineages or clans issued from it, whether they be genetically identical with it or not. But this, he points out, raises a graver difficulty:
The concept of a heterogeneous environment implies that there are factors that vary over space and time in this environment.... However, the concept also implies that there are some invariable properties that distinguish a particular environment from other environments. (Weber 1996 p.83)
In other words, what we are trying to identify here is a specific changing environment: but what criteria can we offer for the reidentification of the same changing environment? Environments are not substances, even when they are regimented to qualify as niches, if only because niches are constructed in reciprocity with the organisms that inhabit them (Laland, Odling-Smee and Feldman 1998, 2000) . Weber’s discussion of the possibility of what we might more poetically call selection for mutability thus presents an intriguing real-life example of the paradox of change. Because the environment isn't an individual, the problem in this form does not seem susceptible of receiving a non arbitrary solution.
Unclear Cases
The world is not divided neatly into clear cases of individuals, and other things. The properties of the clear cases, which are substances in the Aristotelian sense as exemplified by IAWKI can be summarized as follows::
1 spatio-temporal continuity;Note that (i) and (ii) are a priori elaborations of the notion of a particular substance; I have argued that rightly understood these in effect entail (iii) and (iv), which I take to be something like Aristotle's view. Conditions (v) to (viii) are contingent, and their existence cries out for scientific explanation.
Jack Wilson notes that this list does not apply to every kind of living thing, and argues that we must “reform the concept of individuality in biology, so that it is applicable to all living things.” (J. Wilson 1999, 59). But why should we? The alternative is to concede that while a minimal notion of individuality must indeed be available to count whatever evolutionary theory finds it useful to count, not all living things are individuals. It makes sense to look for a more elaborate type of individuality which belongs exclusively to a limited branch of the evolutionary tree, and for which it is plausible to seek a special explanation. But first, by way of contrast, here are a few notoriously unclear cases of entities about which the criteria just listed yield unclear, inconsistent or counterintuitive answers to the question of individuality.
(1) Ant hills and beehives. To the “naked eye”, individual ants or bees can be clearly individuated: they are spatially separate from one another, and each has a definite point of birth and death. They satisfy (i)-(viii). But the degree of interdependence of those individuals and the overall teleological organization of their activities points to the hive or hill as the individual unit. Also the sometimes advanced functional differentiation or division of labor among different types of individuals resembles the functional differentiation of cells in a multi-cellular organism. So the hill or hive, while not meeting (iv) or (vi)-(viii), does as well or better than individual ants or bees on (iii) and (v).[10]
(2) Bacteria. There is a line of thought that “defines an individual as the sexual propagule and all of its asexually produced daughter cells, however they are arranged .... the motivation for this view is that asexual representation is analogous to the growth of a metazoan body.” (J. Wilson 1999, 26). For mitosis doesn't interrupt spatio-temporal continuity; so (i) and (ii) are met, if only in a loose sense. But on that view, there would be no individual bacteria, or rather, bacteria that are genetically identical lineages are going to form large individuals. In short, it's not clear whether (i) and (ii) designate individual bacteria or lineages. Bacterial lineages also fail of (vi) and (vii).
(3) Cellular Slime Molds pose a different sort of problem concerning the maintenance of individuality through time. They are amoebas that go their own way most of the time, but form a remarkable simulacrum of a slug when food runs out. At that time they come to resemble a sort of mobile fungus that has a firm and characteristic shape and which exhibits phototaxis—thus meeting, at least for a time, conditions (i)-(iii) and (vi). Since it’s crucial to the standard characterization of an individual that it persists through time, the identity criteria for slime molds (always referred to in their non-committal plural) seems to require an entirely arbitrary decision.[11] Siphonophora, such as the Portuguese man-of-war, are even more bizarre. They are colonies of single-celled organisms that form what look like jellyfish, with fairly elaborate cell specialization for coordinating locomotion, and for ingestion and distribution of nutrients. These “societies,” in the words of E.O. Wilson, “can be viewed equally well as a superorganism or even as an organism" (Wilson, E.O. 1975,á383).
(4) Caterpillars and Butterflies
While a butterfly is genetically homogeneous with the caterpillar that precedes it, the metamorphosis that changes one into the other makes it problematic whether (i), (ii), and (iv) are satisfied. Rather than a continuous modification of the caterpillar body plan, the metamorphosis involves the growth of an entirely new body from groups of undifferentiated cells that are encapsulated in the caterpillar's body, and which feed on the caterpillar body as they differentiate and grow (Wilson, J. 1999,á7–8). Again, the listed criteria give no unequivocal answer to the question whether a caterpillar is the same individual as the butterfly into which it is transformed.
(5) Lichens. Some things that are commonly identified as organisms are really symbionts that belong to different species or even different phyla. Lichens are an example, as they are made up of some type of fungus and a cyanobacterium in symbiosis. They have been experimentally separated, exhibiting very different characteristics on their own, but are not known to exist separately in nature. (Ramellini 1998; Margulis and Sagan 2002, 13-14). Obviously these fail of several of our criteria, but in particular they show that condition (viii) must be qualified in the best of cases. For symbiosis is ubiquitous, and genetic homogeneity does not imply that there is, throughout the organism classified as an individual, just one single genome. “The estimate is that any person is about ten percent dry weight symbioses.” (Margulis and Sagan 2002, 18).
(6) Species. In recent years, several authors including Ghiselin (1974), Hull (1976, 1978)[12] have argued that species, while traditionally paradigms of natural kinds, are actually better viewed as extended individuals. While this view should perhaps be taken merely as contradicting the assumption that species are natural kinds picked out by universals, the view has been taken in a stronger sense. So taken, one of its counterintuitive aspects is that while a species may be said to have a beginning and an end in time, as well as an extent in space, the birth and death points of a species are not only usually vague,[13] but also impossible to determine except in retrospect. (As a stabbing may or not be a killing, depending on consequences that can be long in coming.) Another consequence of the inclusion of species among the class of individuals is that they exhibit a rather different relationship with their component sub-individuals—organisms—than hold between the latter and their sub-individuals, cells. The major disanalogy is that the bond between the parts of a species is even looser than between the amoebas that constitute a fruiting body in slime molds. Specimens of a species are not differentiated according to any principle resembling a division of labor, and as each one dies, others do not step in, as do cells of the same type in an organism, to succeed them in the specific function they serve for the whole organism—for they have no such specific differential functions. Furthermore, species fail to meet criteria (iv)-(viii), and opinions differ as to whether a certain measure of species constancy is maintained by homeostatic mechanisms of some sort, which would justify the claim that species satisfy the functional integration criterion (iii). (J. Wilson 1999, 84; Gould 2002 ).
There are other odd and complicated cases.[14] But it is time to focus on the strangeness of the most familiar paradigm. The case of cooperating cells in a multicellular organism has already served as a prototype in comparison to some of the examples just given. The even more elementary case of the complexity of a single cell also deserves notice.
(7) Complex Cells. Since any living thing (above the level of a virus) requires to be capable of both metabolism and reproduction, even a single prokaryotic cell is necessarily already a machine of considerable complexity. Some have suggested that eukaryotic cells are the result of symbiotic cooperation that might have begun in ways that could be described in the language of invasion, consumption, and competition. Lynn Margulis has convinced most biologists that mitochondria (the organelles that energize our every cell) were originally independent free-living organisms, which may even have reproduced sexually. (Margulis, 1986, 66; see also Margulis and Sagan 2002).[15] Either they were ingested, but not digested, by anaerobic cells which then were saved from extinction by the mitochondria’s capacity to use oxygen, or they resulted from an originally parasitic invasion by the once free mitochondria, with the same result. De Duve (1996) tells a similar story.
The logic sketched above constrains our interpretation of such stories: the primitive organisms that entered into symbiosis were already, in my sense, “minimal individuals” instantiating (MI). While they themselves had a specific and limited life span, their types—there could at that point be no distinction between genotype and phenotype—gave rise to further entities of the same type only if they chanced upon the right environment. In the first and greatest extinction in the history of life—the eradication of most anaerobic life forms by the toxic spread of oxygen generated by the so-called blue-green algae—survival was likely to depend on such symbiotic compromises. But compromises they were, from the point of view of each of formerly independent entities now become dependent. Moreover, from the point of view of the original types, such symbiotic arrangements amounts to actual extinction insofar as only the symbiotic types subsist. The only type of mitochondrial entities that remain are those that don't (normally) engage in sex and lives in the cytoplasm of the female sex cell. These are the mitochondria themselves. Since these are replicated by way of the reproduction of the organisms in which they now live, it has been suggested by at least one scholar that mitochondria, not genes, individuals or groups, are in fact the only ultimate beneficiaries of evolution. (Hattiangadi, unpub.)
Sex and death
According to this line of thought, sex is often equivalent to death. When sex doesn’t involve reproduction but merely consists in an exchange or transfer of genetic material, it is sometimes lethal for the actual cells involved; but in other cases, while it may leave the cells involved alive, it has changed the genome of the recipient bacteria, whether or not reproduction is involved, for after the injection of additional genetic material the bacterium’s genome is no longer the same. So insofar as having the same genome is an essential condition of continuing to be the same substance (criterion (viii)), the original bacterium no longer exists. By contrast, the type of clonal reproduction common in prokaryotes and protists preserves at least the type of the individual that replicates even if the original cell “token” is deemed no longer to exist. From this point of view, the exception to the dictum that sex is death is the gene itself: for while sex mixes and recombines, yielding a type that is necessarily different from itself, parts of it are replicated in the process and survive, in the context of a larger “vehicle” which is itself expended at every generation.
William Clark (1996) has argued for a further connection between sex and death: a causal, not merely a conceptual one. According to him, sex, death and IAWKI are causally linked as part of the same system. Senescence and programmed death are concomitants of sexual reproduction, necessitated by precisely the same evolutionary strategy as the segregation of sex from somatic DNA.[16] The somatic DNA is kept busy handling the affairs of the cell, whereas the sex cells alone continue to look to the repair and maintenance of intact DNA which are favoured by sex. The segregation of expendable somatic DNA represents a strategy for preserving the rejuvenating benefits of sex, which the hard-working somatic DNA does not share in. So the individual in the thick sense (IAWKI) is both produced by sex and doomed by it.
This is the logic that leads to the conclusion (so abhorred of anti-sociobiologists) that evolutionary biology is committed to the view of nature as “red in tooth and claw”. In fact, there just isn’t any alternative to conceiving of basic individuals of the type characterized by (MI) in terms of competition, long before any IAWKI was possessed of either tooth or claw. On the contrary, by the time teeth and claw appear, the metaphor applies in an already much attenuated form. The attenuation comes from the fact that strategic cooperation is one of the mechanisms that individuals hit upon to enhance their competitiveness, though some, in the process, lose their individuality. This, at any rate, seems to be the inference we are led to draw, if we follow Leo Buss in his exploration of the evolution of individuality. It is to this that I now turn.
Individual Metazoans: Buss on the Evolution of Individuality.
The originality of The Evolution of Individuality (Buss 1987) lies in driving home with great force the contingency of IAWKI—of the sort of individuality generally taken for granted when biologists focus on higher orders of animals. Prokaryotes and protists, he points out, are not built on the same pattern, and therefore the fact that some things (an absolute minority of living species) are so built requires an evolutionary explanation.
Buss begins with two rather unobvious observations. The first concerns the significance of Weismann’s doctrine of the sequestration of the germ line. This is generally taught as a basic dogma of biology which absolutely precludes any kind of “Lamarckian” inheritance of acquired characteristics. But Buss’s first observation about it has a different focus: “Weismann’s great contribution was the recognition that heritability is controlled by development” (p.3; p.13)[17]. This is, on the face of it, a puzzling statement, which raises two questions:
1. What exactly does it mean? and
2. What does it have to do with individuality?
The second unobvious observation is that “individuality is a derived character, approximated closely only in certain taxa.” (p.20). Hence a third question:
3. If individuals are particulars, and particularity is, as I claimed above, logical and absolute, then how could individuality be a matter of degree?
The three questions must be answered together. What the first observation means is that Weismann’s dogma is true only in virtue of a process of cell differentiation from “totipotent” cells (which can give rise to cells of any type) to specialized cells, of which the somatic lineages produce by mitosis only cells of the same type. Specialized somatic cells lose the capacity to pass their genome on to the next generation. Where this developmental process does not take place, “Weismann’s barrier” does not exist.
It is natural to ask for some explanation for the existence of that process. Differentiation might take place earlier, later or not at all. If we adopt the assumption that the concept of the full-fledged individual is one that includes the sequestration of the germ cells, it follows that individuality itself is a matter of degree, which was question 3. And this is surely news about the nature of individuality, which answers question 2.
The additional assumption just mentioned is again not obvious, and I shall return to it in a moment. But first let us look at Buss’s illustration of the point about the contingency of the Weismann barrier.
Hydra and Drosophila.
As Buss describes it (Buss p.15ff.), the first stages of the development of the long-suffering laboratory fruit fly drosophila melanogaster involves thirteen nucleic cleavages entirely under the control of the maternal DNA, before any cell division takes place. The unique “coenocytic” cell remains “totipotent”, that is, it can yet give rise to any kind of cell in the future embryo, whether germ or somatic.[18] During that time, the replicating nucleus might undergo mutation; and if so the mutation could be transmitted to the somatic cell of the developing individual. That individual would then be different from its parents in unique ways which could not be accounted for by the combination of parental DNA and could, in turn, be passed on to the next generation. But over only thirteen divisions a mutation is unlikely. Immediately thereafter, the cells divide and are now segregated: the sex cells can no longer give rise to somatic cells, and the somatic cells can have no influence on the sex cells.
Contrast the freshwater Hydra:
The zygote gives rise to an embryo composed of two distinct populations of cells: the interstitial (or I-cells) and somatic cells. The I-cells are a multipotent cell lineage which may, under the proper stimulus, give rise to any of the various somatic cell types.... When local conditions deteriorate, Hydra may be induced to cease reproduction by asexual iteration, and instead I-cells differentiate into gametes..... In contrast to Drosophila, where totipotency is limited after thirteen nuclear divisions, the I-cells of Hydra remain multipotent and mitotically active through the potentially great life span of the animal. (Buss 1916-17)
As a consequence, Buss continues:
“In ... Drosophila, it is appropriate to view the individual as a unique, genetically homogeneous, unit. It is highly unlikely that genetic variation will arise and gain access to the gametes within a single generation. In the hydroids, however, the number of divisions of the totipotent cell line intercalated between each sexual generation is so high that it is very likely that genetic variation will both arise and be inherited. (p.19)
This makes it clear why IAWKI is a matter of degree: “an ideal which is approximated to varying degrees in different taxa” (p.19). What is not yet clear is the rationale for the additional assumption: that sex-cell segregation is necessary for full-fledged biological individuality.
Note first that the issue of concern here is not, unlike most contexts in which Weismann’s barrier is raised, the question of Lamarckism, either in the form originally raised by Lamarck himself or in the form raised again a couple of decades ago by Ted Steele (1981). If it were, the existence of a long line of totipotent cells would not be of much interest. The reason is that it lacks both of the controverted ideas associated with Lamarckism: first, there is no transfer of information from the somatic cells to the germ cells, since ex hypothesi the totipotent cells are not yet somatic cells in the relevant sense; second, there is no suggestion that any of the changes to which the totipotent cells may be susceptible could arise by some sort of “striving” for adaptation by the individual organism.[19]
So Buss’s concern with Weismann’s barrier has nothing to do with Lamarckism. It is relevant only to his enriched concept of “the individual as a unique, genetically homogeneous, entity ... an ideal, however, that is only approximated in real organisms.” (13) To Buss’s minimal definition already quoted (“a physiologically distinct discrete organism”), this last statement stresses two features: uniqueness, and genetic homogeneity. The latter already forms part of our notion of full biological individuality. What is the rationale for the addition requirement of uniqueness for IAWKI?
Uniqueness
As I see it, the rationale is two-fold. First, uniqueness can be regarded as part of our common-sense conception of an individual. “Genetic homogeneity” merely trails in its wake, as a marker of uniqueness. We have become used to speaking of our DNA as a kind of genetic fingerprint. But recall that uniqueness cannot be assessed without appealing to normative criteria: in this case, DNA is clearly held to be more significant than fingerprints, for two reasons. The first is that DNA is not a mere marker, but at least one half of what actually makes us unique. The other half comprises the accidents of our personal history. That other half needs to be kept in mind too, lest we conclude from Buss’s definition that any pair of twins is but a single individual. As Jack Wilson points out, we must distinguish between genetic and functional individuality: what stops clones, such as twins, from being merely separate parts of a single individual, is that they are not the same functional individual and lack a common boundary. (Wilson, J. 1999, 60; cf. Smith and Brogaard 2003, 47). The genetic homogeneity in question is synchronic, in the sense that at any particular time any of our cells carries the mark of our complete genetic identity.[20] But more importantly it is also diachronic: though Buss doesn’t actually say so, he must surely have in mind that only if the organism retains its genetic identity through time—in spite of what might be great morphological differences, especially in metamorphosing species—can it be clearly marked off in its identity as well as its uniqueness from all other members of its species.
In addition, since the individual phenotype is essentially constituted by an aggregate of somatic cells which can neither be a copy of either parent, nor pass on its characteristics directly to any offspring, each phenotype is the only token of that (pheno-)type. This is a characteristic not shared by asexually reproducing organisms: insofar as uniqueness is a definitional feature of individuals, then, only those entities engendered by sexual reproduction are full biological individuals.
The Origin of Biological Individuals.
The second rationale for the importance of uniqueness in individuality arises from the complex story of the evolutionary origin of IAWKI—of germ-line-sequestered, multicellular organisms. Thus Buss asks: “Why, though, has individuality evolved? Lacking in the Modern Synthesis, in evolutionary theory altogether, is an approach to this problem. Why, for example, does a mouse sequester its germ line and a hydroid not?” (Buss 1986, 25)
There are two strands to this story. The first links individuality to conflict, the second braids together multicellularity, sex, germ-cell segregation, and death.
“ Harmony from Discord”while the cooperative model is an appealing characterization of development in extant taxa, it is inappropriate to view the processes which gave rise to developmental programs as cooperative. The opposite is more likely the case..... The... complex interdependent processes which we refer to as development are reflections of ancient interactions between cell lineages in their quest for increased replication. Those variants which had a synergistic effect and those variants which acted to limit subsequent conflicts are seen today as patterns in metazoan cleavage, gastrulation, mosaicism, and epigenesis. (Falk and Sarkar 1992, 29).
Two cases, one benign, the other harmful for the individual, will serve as illustrations of this approach.
First, consider the origin of gastrulation in simple metazoans. Gastrulation is the process whereby cells migrate to the interior of a multicellular structure. The simplest metazoans (multicellular organisms) were apparently developed from (single-celled) protists. Most protists, however, operate under a constraint which results from the fact that they have just one “microtubule organizing center” (MOC). This MOC is capable of producing a flagellum or cilium, enabling it to locomote, or else it is capable of powering cell division—but not both. Gastrulation, Buss surmises, “is the metazoan solution to the requirement of simultaneous development and movement.” (Buss 1986, 44): since some of the cells need to keep reproducing, but can't do so while also contributing to the mobility of the whole, they migrate inward while the ciliated cells continue to take care of locomotion. Two features of this case are to be noted. First, it illustrates the essential conservatism of evolution: the cells’ behaviour are bound by certain innate constraints, which mutant versions sometimes exist to evade, but which in most cases must be accommodated in some other way. Second, the process illustrates the fact that as cells multiply, they may form different lineages with different properties; if those lineages can only perpetuate themselves if they make a contribution to the survival of a larger individual type, then they will survive in that collaborative framework as a result of being in competition with alternative cell lineages. In such cases, as Buss puts it, “a cell lineage in pursuing its own replication incidentally favors the individual in which it arose.” (p. 89).
In the harmful type of case, a cell lineage enters into direct conflict with the individual in which it arises. A typical case is cancer, “a grim reminder that genetic variants can indeed arise in cell lineages within an organism.” (p. 51). Like any parasite that kills its host, a cancerous cell lineage will become extinct; but then so will all the somatic cells of its host, so there can arise, at best, only an indirect selective pressure against the likelihood of cancer. But by the time a particular cancer has attacked a particular individual, it is too late for selective pressure to do away with it.
Sex and Death Revisited
The second strand of Buss’s argument should finally make clear why Weismann’s barrier is inseparable from IAWKI. We already have most of the elements required to state it, so it can be quickly summed up. The one new fact involved is that there are no multicellular, cellular-differentiating organisms without sex:
Exclusively asexual, cellular-differentiating organisms are, however, known. The mode of reproduction in such forms is, without question, derived from an ancestral sexual state. The ubiquity of sex invites a simple historical interpretation: sex is common because sex is ancestral in all organisms with cellular differentiation.... Sex may have been a necessary precondition for the evolution of cellular differentiation. (Buss 1986, 125)
The probable reason for this is that without sex, differentiating cells will be at a disadvantage, and that given sexual reproduction and the cellular specialization it entails, individual death is necessary as well. Here is Buss’s argument, which incidentally provides a nice further illustration of interlineage competition. Suppose that a differentiating variant of a cell remained totipotent:
It would nonetheless produce far fewer propagules than those neighboring cells which expended no effort in producing somatic tissue. Variants which display cellular differentiation in a multicellular organism are at a severe competitive disadvantage in the somatic environment.... [moreover,] back-mutations which reverse the state of differentiation ... are inevitable: an organism must periodically free itself of them if it is to persist. However, asexual organisms have no mechanism for purging themselves of mutations, short of the extinction of the clone itself. (p. 126).
In other words, sex is essential to the persistence of differentiated organisms. But as we saw above, there is no sexual reproduction without segregation of sex and somatic cells, with the attendant necessity for the somatic cells eventually to die. At this point, then, we have found the rationale not only for the incorporation of Weismann’s barrier into the characterization of the (metazoan) biological individual, but also for the one aspect of Gould’s definition—the necessity for death—which remained unexplained on the basis of the concept of the minimal individual.
The two strands come together to yield the two core groups of properties of IAWKI, the “modern” (metazoan) biological individual. One is the ubiquity of competition; the other is the tight relation between cellular differentiation, uniqueness, sex, somatic-cell segregation, and death. The difference between these two strands is that competition and “harmony out of discord”, merely get more complicated: they are ubiquitous properties even of minimal individuals. On the other hand, sex, multicellularity, and Weismann’s barriers are evolutionary innovations of IAWKI in relation to minimal individuals defined by (MI).
Units of Selection.
We saw above that in some cases a multicellular organism can become the vehicle of its constituent cell lineages’ success. The vehicle metaphor was made famous by Dawkins (1976), who applied it to the individual organism in relation to the gene. It applies equally, however, to other parts of the organism whose ancestors might have competed for independent existence and then hitched their fate to a containing organism. This is why Buss can describe as his “central thesis” the hypothesis that “the suite of adaptations that we refer to as development arose as a direct consequence of the transition from one unit of selection, that of the cell, to another, that of the individual.” (p.179) In one respect, however, this is misleading, since it suggests that once metazoans arose the individual organism became the only unit, or perhaps the decisive unit, to deserve the title of “unit of selection.” Yet this is a view that most biologists reject, whether because they hold that genes alone are units of selection, or on the contrary because they insist that there are units of selection at many levels of analysis and causality.
So what exactly is it to be a unit of selection? The term suggests several non-equivalent ideas. One relates to the causal role played by various units in the process of natural selection. Based on that notion, Gould (2002, 656) has characterized units of selection as those that are undergo “differential proliferation ... based on interaction between their traits and the environment.” As was first clearly pointed out by David Hull, it is phenotypes that are typically directly affected by the causal processes that lead to the success or failure of any lineage of genes. They are interactors, while genes are replicators (Hull 1980; cf. Brandon 1998). This has led Gould to claim that the “gene-centric” view advocated by Dawkins commits a “logical mistake” consisting in the “confusion of bookkeeping with causality.... people confused a need for measuring the results of natural selection by counting the differential increase of some hereditary attributes (bookkeeping) with the mechanism that produces relative reproductive success (causality).” (Gould 2002, 614, 619; cf. 632 ff.)
But in fact a slight change of perspective leads to a point of view from which it becomes clear that bookkeeping, not causality, is precisely what we should be interested in. Individuals are indeed typical interactors. But while interactors are involved in the mechanism of evolution, Dawkins's gene-centric view was intended to provide the answer to a different question: namely the teleological question—or what can coherently be said to remain of the teleological question in a world the springs of which wholly lack point or intentionality—“cui bono?”: the question of who benefits from the processes of natural selection. And since the only wholly naturalistic measure of “benefit” is precisely replication, it is clear that only the right sort of “bookkeeping” can provide the answer. From this perspective, one can readily accept—as indeed Dawkins (1982) seems to do—that there may be, as Brandon (1980) and Gould (2002) among others have urged, a hierarchy of units capable of causal interactions that may affect the fitness of the replicators on whose behalf they act. Derivatively, a kind of fitness, namely trait fitness can be attributed to properties of interactors, and interactors may well be as varied as “genes and cells through organisms to colonies, demes, and possibly entire species.” (Hull 1994,á627). But individuals cannot be beneficiaries of selection, for the simple reason that biological individuals (in the special sense, IAWKI, which fully characterizes only metazoan organisms) are never replicated. It is therefore logically impossible that individual organisms such as ourselves should be units of selection in the second sense, of being the beneficiaries of replication.
Nevertheless, both individuals and replicators are potentially involved in conflict or competition. As I stressed above, even minimal individuals invite normative judgments (How important is this or that characteristic? How much independence should we require?) and lend themselves to a primitive sort of teleological explanations (If the ancestors of this individual hadn't adopted this evolutionary strategy, it wouldn't exist now). Cancerous growth exemplifies a failure of a lineage of cells, or of some interacting network of which they are a part, to constrain them to minimally cooperative behaviour (See Moss 2003, chapter 4). At many other levels, any units that retain the potential to enter into competition—i.e. to be differentially selected in preference to some competing unit—can play the role of units of selection: whether genes, gametes, segregation distorters, selfish DNA, immune system cells, molecules, organelles, or demes and even populations, not to mention the molecular variety generators (MVG’s) discussed above. (cf. e.g. Dawkins 1982, Lloyd 1994, Gould 2002, Hattiangadi unpub.). Without entering into that debate here, therefore, it seems plausible to conclude that the ink that has flowed in passionate defense of this or that entity as the proper units of selection was mostly spilled in vain.[21] For Buss’s theory illustrates the fact that while the individual in Buss’s full-fledged sense does indeed emerge out the conflict among its very own constituent parts, and can be a unit of competitive interaction, the more primitive as well as some more inclusive units can still be expected to compete among themselves as well as even against the lower-level individuals that comprise them.
Philosophically, these reflections yield a metaphysical perspective on our nature as metazoan animals which is pertinent to our self-knowledge as human beings. Biological individuals in the full sense, organisms such as ourselves—the most elaborate kinds of relatively independent functional units—have been so constructed by evolution as to be necessarily subject to death, by the very logic of the process, sexual recombination, to which we owe our existence. The natural teleology that underlies these processes is entirely alien to our individual goals and purposes and frequently in conflict with them. Each one of us, like every biological individual, is literally a dead-end, a sterile twig in the great bush of evolution. Whatever it is that evolution happens for, it isn't us IAWKI's. To explore our own goals and aims, therefore, we should look not to Nature but away from it, through the lens afforded us as individuals by our capacity for making that very distinction between our own goals and those of nature[22]
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