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Holistic Darwinism
JOURNAL OF SOCIAL AND EVOLUTIONARY SYSTEMS, 20(4): 363-400.
INTRODUCTION: THE PERILS OF GROUP SELECTION The emotionally-charged group selection debate in biology -- which celebrated an unofficial 30th anniversary in 1996 -- provides a classic example of a controversy that arose from a misconception. To Darwin and many of his contemporaries, group selection was a perfectly respectable concept. Indeed, it was Darwin who first proposed, in The Descent of Man (1874/1871), the then unexceptional idea that differential group selection may have played an important role in human evolution, along with what he called "family" selection (now known as inclusive fitness or kin selection theory) and individual reciprocities (now called mutualism and reciprocal altruism). Darwin's "tripartite" explanation of human evolution was subtle, but his view of the role played by group selection is illuminated in this brief passage: "All that we know about savages, or may infer from their traditions and old monuments, the history of which is quite forgotten by the present inhabitants, show that from the remotest times successful tribes have supplanted other tribes" (p.147).1 Herbert Spencer, one of the outstanding theorists of the 19th century, expressed a similar view in The Principles of Sociology (1897/1874-82), and many of the pioneer anthropologists of that period also seemed to agree.2 In the first half of this century, the founding fathers of modern genetics and population biology, notably including Haldane, Wright, Fisher, Morgan, Dobzhansky, and others (plus some non-geneticists like Huxley, Mayr, and Simpson) redefined evolutionary theory in quantitative genetic terms. However, the so-called "modern synthesis" was also deemed to be compatible with group selection of various kinds. For instance, Sewall Wright at the University of Chicago coined the term "interdemic selection" -- i.e., selection between discrete breeding groups, or "demes" -- and developed what he called a "shifting balance" model, which he believed was of the utmost importance in producing evolutionary changes (Wright 1968-78). Ernst Mayr, likewise, speaks of evolutionary change as a population-level phenomenon, meaning that populations and species are the ultimate units of evolutionary change, not individuals. Mayr also developed what he calls the "founder principle," which envisions small, reproductively isolated groups as a significant source of evolutionary innovation (Mayr 1963; 1976). Meanwhile, various students of animal behavior, such as William Morton Wheeler and Warder C. Allee, stressed the co-operative aspect of animal behavior and social life. Wheeler (1927) also promoted the idea of "emergent evolution," and he borrowed from Spencer the idea that a socially-organized group can be likened to a "superorganism" (Wheeler 1928) (see below). A theoretical "punctuated equilibrium" occurred in 1962. In his subsequently much-maligned book Animal Dispersion in Relation to Social Behaviour, V.C. Wynne-Edwards made himself a stalking horse, in Edward O. Wilson's characterization, by propounding a seriously overstated version of the group selection hypothesis. Wynne-Edwards asserted that group-living animals regularly display behaviors which involve the curtailment of their own personal fitness for the good of the group (for example, through "conventional" controls on personal reproduction that serve to limit population densities). "The great benefit of sociality," he claimed in a companion article in Nature, "arises from its capacity to override the advantage of individual members in the interest of the survival of the group as a whole" (1963). Some of Wynne-Edwards's critics, playing loose with the facts, accused him of a Pollyanna-like naivete that violated Darwinian theory, but in fact he clearly stated that altruistic, group-serving behaviors could arise only if natural selection were to operate between social groups "as evolutionary units." Notwithstanding, Wynne-Edwards became a pariah in evolutionary biology and has been routinely chastised for his heresy ever since -- rather like the treatment accorded to Lamarck. Although the assault on group selection theory began with William D. Hamilton's now classic papers on "The Genetical Evolution of Social Behavior" (1964a,b), it was fully-elaborated in George C. Williams's New Testament -- Adaptation and Natural Selection (1966). Williams's near-legendary book was in many respects a therapeutic cold bath that served to purge evolutionary theory of some sloppy thinking. However, Williams also took an extreme position, from which he has since retreated, to the effect that selection at any higher level than that of an individual is essentially "impotent" and is "not an appreciable factor in evolution" (1966:8; cf., Williams 1992). Although E.O. Wilson was more moderate by comparison in his discipline-defining volume, Sociobiology (1975), he also (inadvertently) propagated a conceptual muddle that has caused no end of confusion and mischief in evolutionary theory.3 Wilson launched his massive synthesis with the startling assertion that altruism is "the central theoretical problem of sociobiology" (p.3). The implication, which guided much subsequent work in this new interdiscipline, was that social life is founded on altruism. Therefore, co-operative behaviors are inherently a theoretical "problem" that can be overcome only under extraordinary circumstances -- i.e., via group selection, kin selection and maybe Robert Trivers's (1971) "reciprocal altruism". In opposition to Wynne-Edwards, Wilson considered "pure" group selection -- i.e., among non-kin -- to be highly improbable, a rare occurrence confined to humans and perhaps a few other species. (His detailed, chapter-length discussion of group selection included a review both of the available evidence and of various formal models, but his conclusion was preordained by the assumption that "pure" group selection necessarily implied genetic altruism (1975:106-129). Another broadside against group selection theory occurred when Richard Dawkins published his ideologically-tinged popularization with the cunningly anthropomorphic title The Selfish Gene (1989/1976). "I think ‘nature red in tooth and claw' sums up our modern understanding of natural selection admirably," Dawkins wrote with evident relish (1989/1976:2). Not surprisingly, The Selfish Gene became a controversial best-seller. In retrospect, the selfish gene metaphor has proven to be a powerful heuristic tool. It has led to many new insights about the interactions within and among various functional units in nature and to much productive research. On the other hand, it also introduced a simplistic and seriously distorting perspective into evolutionary theory. The short-term consequence of this rancorous theoretical debate was a wholesale rejection of the concept of group selection. Nevertheless, for the past 20 years David Sloan Wilson (lately with the collaboration of Elliott Sober and with parallel efforts from a growing number of other workers) has been attempting to resurrect group selection on a new foundation. What Wilson calls "trait group selection" (D.S. Wilson 1975, 1980; Wilson and Sober 1989, 1994) refers to a model in which there may be linkages (a "shared fate") between two or more individuals (genotypes) in a randomly breeding population, such that the linkage between the two becomes a unit of differential survival and reproduction. Initially, Wilson assumed that one of the two was an altruist, for he was then intent on accounting for the evolution of altruism without recourse to kin selection. John Maynard Smith (1982) developed a similar model, which he dubbed "synergistic selection," in recognition of the fact that it implies a functional interdependency. (See also Matessi and Jayakar 1976; Wade 1977, 1985; and the discussion in Dugatkin et al., 1992.) The current revival of group selection theory may perhaps be attributed, in considerable measure, to the growing recognition that it can also entail "win-win" processes. Co-operating groups might provide mutual advantages for their members, so that the net benefits to all participants outweigh the costs. In other words, co-operation is not equivalent to altruism and does not by definition require sacrifices, or genes for altruism. (I refer to it as "egoistic co-operation," to distinguish it from altruism, and Maynard Smith has recently modified his usage of the term "synergistic selection" -- originally associated with altruism -- along the same lines.) This, in essence, is what game theory models of co-operation tacitly postulate (see Maynard Smith 1984, 1989; Axelrod and Hamilton 1981, inter alia.), which is why game theory formulations are largely indifferent to the degree of relatedness, if any, between the co-operators. Moreover, game theory provides a window into a vastly larger galaxy of co-operative phenomena that, I submit, reduces the group selection controversy to a sideshow. This alternative formulation was originally developed in The Synergism Hypothesis: A Theory of Progressive Evolution (1983) and is summarized in Corning (1995, 1996a). It was also developed independently by Maynard Smith and Szathmáry (1995), and it is supported by an accumulating body of research findings across many different specialized disciplines, from molecular biology and microbiology to behavioral ecology and sociobiology -- not to mention the social sciences. (See also Dugatkin and Reeve, 1994, and Dugatkin and Mesterton-Gibbons, 1996, on indirect "by-product mutualism" in evolution and Wilson and Dugatkin, 1997, on the role of "assortative interactions," or behavioral selection, a mechanism of group selection.) This alternative paradigm might be characterized as "Holistic Darwinism." ON THE CONCEPT OF SYNERGY Holistic Darwinism is not an oxymoron. The term was coined as a way of highlighting the paradox that selfish genes are, without exception, "selected" in the context of their functional consequences (if any) for various wholes.4 Holistic Darwinism is strictly Darwinian in its underlying assumptions about natural selection and the evolutionary process. It has no fundamental quarrel with the theoretical premise of "gene selfishness." Rather, it involves a different perspective on the causal dynamics of evolution. In his preface to the second edition of The Selfish Gene, Dawkins uses the metaphor of a Necker cube -- a two-dimensional drawing of a three-dimensional object that can be perceived in different ways -- to characterize the intent behind his inspired metaphor: "My point was that there are two ways of looking at natural selection, the gene's angle and that of the individual...It is a different way of seeing, not a different theory" (1989/1976:x-xi). Actually, there are more than two ways of looking at natural selection, and Holistic Darwinism focusses not on genes, or individuals, or even groups as units of selection but on the functional relationships among the "units" at various levels of biological organization, from genomes to ecosystems, and on their consequences for differential survival and reproduction. It involves refocussing the Necker cube on the "interactions" between genes, between cells, between organisms, and between organisms and their environment(s). Perforce, Holistic Darwinism is also about the role of synergy -- the combined effects produced by phenomena that "co-operate" (operate together) -- as a major cause of evolutionary continuity and change. It should be stressed at the outset that the term co-operation will be used here in a strictly functional sense; it refers to functional interactions. In this conceptualization, co-operation may or may not also be considered selfish or altruistic, mutualistic or parasitic, positive or negative. Such attributes involve additional, post-hoc judgments about the consequences of a co-operative relationship with respect to some separately specified goal or value. (Of course, in Darwinian theory the "operative value" is survival and reproductive success.) By the same token, a co-operative relationship may or may not be voluntary. Slavery, in nature and in human societies alike, involves a form of involuntary co-operation, and so (presumably) does the host's role in a parasitic relationship. Accordingly, a key point about co-operation as a functional concept is that it is found at every level of living systems. Beginning with the very origins of life, it is a common denominator in all of the various formal hypotheses about the earliest steps in the evolutionary process (reviewed in Corning 1996a). All share the common assumption that co-operative interactions among various component parts played a central role in catalyzing living systems. Similarly, at the level of the genome, it goes without saying that genes do not act alone, even when major single-gene effects are involved. Indeed, the human genome sequencing project has so far established, among other things, that there are in fact 1,195 distinctive genes associated with the human heart, 2,164 with white blood cells and 3,195 with the human brain (see Little 1995). The functional (morphogenetic) implications behind those numbers are awesome to contemplate.5 As Richard Dawkins himself so eloquently put it in a more recent book, The Blind Watchmaker (1987/1986): In a sense, the whole process of embryonic development can be looked upon as a cooperative venture, jointly run by thousands of genes together. Embryos are put together by all the working genes in the developing organism, in collaboration with one another....We have a picture of teams of genes all evolving toward cooperative solutions to problems...It is the ‘team' that evolves (pp.,170,171). The origin of chromosomes, likewise, may have involved a co-operative/symbiotic process (see Maynard Smith and Szathmáry 1993). Sexual reproduction, one of the major outstanding puzzles in evolutionary theory, is also a co-operative phenomenon, as the term is used here. Although there is still great uncertainty about the precise nature of the benefits, it is assumed that sexual reproduction is, by and large, a mutually beneficial joint venture. As we move up "the great chain of being" (to borrow that still-useful anachronism), we find further variations on the theme of functional co-operation. Once upon a time bacteria were considered to be mostly loners, but no longer. It is now recognized that large-scale, sophisticated co-operative efforts -- complete with a division of labor -- are commonplace among bacteria and can be traced back at least to the origin of the so-called stromatolites (rocky mineral deposits) that were constructed by bacterial colonies some 3.5 billion years ago (Shapiro 1988; Shapiro and Dworkin 1997; Margulis 1993; Bloom 1997). Shapiro suggests that bacterial colonies can be likened to multicellular organisms. Eukaryotic cells can also be characterized as co-operative ventures -- obligate federations which may have originated as symbiotic unions (parasitic, predatory or perhaps mutualistic) between ancient prokaryote hosts and what have now become cytoplasmic organelles, particularly the mitochondria, the chloroplasts and, possibly, eukaryotic undulipodia (cilia) and certain internal structures that may have evolved from structurally-similar spirochete ancestors (Margulis 1993). The phenomenon of symbiosis, by definition a category of co-operative relationships in nature, provides yet another example. Not only has the darker side of symbiosis -- parasitism -- gained new prominence over the past decade or so but more benign commensalistic and mutualistic forms of symbiosis are also more widely appreciated (see below). Sociobiology is also, by definition, concerned with co-operative relationships among conspecifics, interactions which can provide a variety of adaptive consequences for the participants. As shown by the many field studies and laboratory experiments that were inspired by inclusive fitness theory and game theory, the social interactions that occur in nature among members of the same species may be perturbed by free-riders, "defectors", exploiters, conspecific parasites, etc., yet the fact remains that within-species co-operative behaviors are fairly common and encompass a broad array of survival-related functions, including: (1) hunting and foraging collaboratively, which may serve to increase capture efficiency, the size of the prey that can be pursued, or the likelihood of finding food patches; (2) joint detection, avoidance of and defense against predators, the forms of which range from mobbing and other kinds of coordinated attacks to flocking, herding, communal nesting and synchronized reproduction; (3) shared protection of jointly acquired food caches, notably among many insects and some birds; (5) co-operative movement and migration, including the use of formations that increase aerodynamic or hydrodynamic efficiency and reduce individual energy costs and/or facilitate navigation; (6) co-operation in reproduction, which can include joint nest-building, joint feeding and joint protection of the young; and (7) shared environmental conditioning. Neo-Darwinian theory -- as purified by the selfish gene perspective -- attributes evolutionary change to competition among the "replicators" -- the ultimate units of information transfer in evolution. In the classical neo-Darwinian model, co-operation plays a decidedly subsidiary role. But if we shift our perspective and view evolution as an ecological and economic process -- a "survival enterprise" in which living systems and their replicators are embedded -- then differential reproductive success may be viewed as the result of a complex interplay of competitive and co-operative interactions (along with a variety of other factors), both within and among functionally interdependent units of ecological interaction. Our focus shifts to the activities of the "vehicles" (in Dawkins's terminology) or the "interactors" (in the terminology of David Hull, 1980) -- and, more important, to the bioeconomic consequences of their functional interactions. It has been a cardinal assumption of neo-Darwinism that co-operation in nature is a phenomenon that is at odds with the basic principle of gene competition, and that extraordinary conditions are required to overcome the inherent selective bias against the evolution of co-operation. This assumption is what accounts for the importance attached to inclusive fitness theory (or kin selection, in Maynard Smith's term) and to game theory. However, a functional/ bioeconomic perspective on the evolutionary process challenges that point of view. Not only is co-operation (broadly defined) fairly common in nature but synergistic effects (the functional consequences of co-operation), it is argued, have played an important causal role in evolution, especially in relation to the evolution of complexity. To put it baldly, functional synergy explains the evolution of co-operation in nature, not the other way around. In other words, functional groups (in the sense of functionally integrated "teams" of co-operators of various kinds) have been important units of evolutionary change at all levels of biological organization; "functional group selection" is thus a ubiquitous aspect of the evolutionary process.6 This is obviously a highly contentious assertion. Let me briefly summarize the evidence. CONSIDER THE EVIDENCE If co-operation in nature is not largely dependent on inclusive fitness, we would expect to find a significant degree of decoupling in the natural world between genetic relatedness and co-operation, and, in fact, there are at least four sources of evidence for this proposition. First, there is the entire domain of symbioses. Here we can observe a wide range of co-operative relationships that can only be accounted for in bioeconomic, cost-benefit terms. Kinship is largely irrelevant. Indeed, many types of symbioses, such as the estimated 20,000 species of lichen partnerships involving approximately 300 different genera of fungi, or the Rhizobium-like bacteria that form root nodules with some 17,500 species in 600 genera of plants, reflect a plethora of independent inventions. In other words, many different species may discover and utilize the same functionally-advantageous co-operative relationships. (As Maynard Smith, 1989, has noted, extreme non-specificity is the rule among mutualists, whereas parasitism is highly specific.) The case for "symbiogenesis" as a significant factor in evolution was documented by participants at a 1989 conference on the subject and in a subsequent volume edited by Margulis and Fester (1991). Among the extensive evidence that was presented:
A second body of supporting evidence can be found in the various game theoretic models of co-operation between unrelated individuals, along with the substantial research literature that these models have inspired. (These will be discussed further below.) Third, there is the entire category of outbreeding reproduction, a class of co-operative behaviors which, by definition, falls outside of the inclusive fitness model. Finally, over the past decade or so there have been many field and laboratory studies of co-operation among conspecifics that are inconsistent with inclusive fitness theory and/or suggest that the particular behaviors in question are more satisfactorily explained in bioeconomic terms, although co-operation remains more likely to occur in closely-related, or at least familiar, animals. A detailed summary of this discordant evidence (including 28 recent field and laboratory studies and seven reviews of the older literature) can be found in Corning (1996a) (see also the careful analysis by Goodnight and Stevens 1997). One particularly well-documented illustration is the food-sharing behavior among vampire bats (Desmodus rotundus), which clearly demonstrates the power of functional/bioeconomic factors to transcend the influence of genetic relatedness in shaping co-operative behaviors (Wilkinson 1984,1988,1990). If gene competition were of overriding importance, the sharing of blood among vampire bats (their exclusive food-source) would be confined to close relatives. The reason is that blood sharing in this species has very high fitness value; an individual bat that fails to feed for two nights in a row will die. In field studies as well as controlled observations in captive groups over a ten-year period, Wilkinson found that blood-sharing both between relatives (matrilines) and non-relatives was extensive. Both relatedness and prior association proved to be important facilitators. Moreover, quantitative cost-benefit analyses showed that the cost to donors was relatively low (in effect, they were sharing their surpluses), while the fitness benefits to recipients was relatively high. When this was combined with the fact that the donors' generosity was usually reciprocated later (i.e., "reciprocal altruism" sensu Trivers, 1971,1985), there was a significant increase in the mutualists' joint fitness. Wilkinson concludes: "Reciprocity is likely to be more beneficial than kin selection -- provided that cheaters can be detected and excluded from the system" (1990:82). Two themes stand out in the many other examples that are described in Corning (1996a): (1) the importance of bioeconomic cost-benefit considerations in co-operative relationships and (2) the presence of synergy -- combined functional effects (payoffs) which are jointly produced and provide benefits to the co-operators that are greater than would otherwise be possible. As Maynard Smith and Szathmáry put it in The Major Transitions in Evolution (1995), if an individual can produce two offspring on its own but by co-operating in a group consisting of "n" individuals can produce "3n" offspring, it pays to co-operate. (An application of this perspective to avian species can be found in Emlen 1996.) GAME THEORY REVISITED Game theory, viewed in the proper light, is also consistent with Holistic Darwinism. Game theory suggests that the evolution of co-operative behaviors depends on an appropriate set of strategic circumstances. Although the focus has always been on the behavioral context and the strategies of the "players," if one looks closely at the various game theory formalizations they tacitly depend on an interaction between the behavior of the players and the structure of the payoff matrix. And if one looks closely at the payoff matrices in some of the "classic" formulations, like Tit-For-Tat, the co-operative strategies in turn depend on synergy. In Axelrod and Hamilton's (1981) model, mutual defection yielded one point each; asymmetrical co-operation (parasitism?) yielded 5 points for the "defector" and none for the co-operator; and mutual co-operation yielded a total of six points, evenly divided. Furthermore, defectors would be penalized in subsequent "rounds" (it was conceived as an iterated game) so that mutual co-operation becomes an increasingly rewarding option over time. In effect, this amounts to a quantification of synergy; the implicit economics of the game are critically important. But what about "cheating" or "defection" (the Prisoner's Dilemma)? Maynard Smith and Szathmáry (1995) have proposed a response in terms of game theory, as illustrated in the two diagrams below. (I have taken the liberty of revising the payoff values that were utilized by Maynard Smith and Szathmáry to accord with a more explicit assumption about the object of the game, namely, that the oarsmen are both seeking to cross a river.) The first diagram involves a "sculling" model in which two oarsmen each have a pair of oars and row in tandem. In this situation, it is easy for one oarsman to slack off and let the other one do the heavy work. This corresponds to the Prisoner's Dilemma game. However, in a two-person "rowing" model, each oarsman has only one opposing oar. Now their relationship to the performance of the boat is interdependent. If one oarsman slacks off, the boat will go in circles. In this case, mutual co-operation becomes an evolutionarily stable strategy and defection is totally unrewarding; in the absence of teamwork, the boat will not reach its goal.
Figure I: Sculling Versus Rowing Games Maynard Smith and Szathmáry conclude that the rowing model is a better representation of how co-operation evolves in nature: "The intellectual fascination of the Prisoner's Dilemma game may have led us to overestimate its evolutionary importance" (1995:261). Indeed, as Peck (1993:195) observed: "The position of [stable] equilibria (and hence the frequency of co-operators) depends on the size of the various payoffs that define the Prisoner's Dilemma game." (See also Dugatkin et al., 1992; Brembs 1996.) AN EVOLUTIONARY THEORY OF GOVERNMENT If many forms of co-operation are functionally interdependent and thus self-policing, many more are not. The problems of cheating, defection, and "free-riders" -- phenomena that the selfish gene metaphor has helped to illuminate -- are real. But, in retrospect the problem may have loomed much larger in theory than it does in fact; our models may have been too pessimistic about the constraints on errant behavior in co-operative relationships. In effect, the games may have been unintentionally "rigged." Consider some of the common assumptions in Prisoner's Dilemma games: The games are always voluntary and democratic; each player is free to choose his/her own preferred strategy, and the opposing player has no means available for coercing choices, or compliance. Also, the players are not allowed to communicate with one another in an effort to reduce the uncertainties in the interactions. Furthermore, defectors are usually rewarded handsomely for cheating while the co-operators are denied the power to prevent defectors from enjoying the rewards, much less punishing them for defection. Such "grade inflation" for defection biases the game in favor of cheating. Worse yet, in iterative games the players are forced to continue playing; they cannot exclude or ostracize a defector. They can only retaliate by themselves defecting and hoping thereby to penalize the other player. A tacit rebuttal to this formulation was incorporated into a new kind of Prisoner's Dilemma model developed by Nowak and Sigmund (1993) called "Pavlov," which the authors suggest can outperform Tit-For-Tat. They call their strategy "win-stay, lose-shift," and the significance of this innovation is that, in contrast with an iterated game in which the players must continue playing regardless of the outcome, in Pavlov they have the choice of leaving the game if they don't like the results. In other words, a player may also have the power to exercise some control over the behavior of a defector by denying to that player future access to the game and its potential benefits. Punishments as well as rewards may be utilized as a means of keeping the game honest and, more important, as a means of restricting the game over time to mutual co-operators. In addition to such suggestive formalizations, there is increasing evidence that a policing function does in fact exist in nature (see especially Boyd and Richerson 1992; Clutton-Brock and Parker 1995; also Frank 1995,1996; and the analysis in Michod 1996). As Clutton-Brock and Parker point out in the summary of their review article on the subject: "In social animals, retaliatory aggression is common. Individuals often punish other group members that infringe their interests, and punishments can cause subordinates to desist from behaviour likely to reduce the fitness of dominant animals. Punishing strategies are used to establish and maintain dominance relationships, to discourage parasites and cheats, to discipline offspring or prospective sexual partners and to maintain co-operative behaviour" (1995:209). Evidence of a policing function has also been documented in social insects (Ratnieks and Visscher 1989), naked mole-rats (Sherman et al., 1991), primates (de Waal 1996) and, needless to say, Homo sapiens. From a functional (synergy) perspective, if co-operation offers sufficient benefits it may be in the interest of some individuals to invest in coercing the co-operation of others. Inclusive fitness provides one possible explanation for punishment as a successful strategy in social groups. Another might be the sort of individual fitness tradeoffs referred to above. But group selection may also provide a mechanism. The enforcement of co-operation in the "public interest" might have significant fitness-enhancing value for groups that are in competition with other groups, or other species. (In effect, we are resurrecting Darwin's tripartite explanation of social evolution.) Maynard Smith's (1982, 1983, 1989) "synergistic selection" model is relevant here. The model suggests that, if co-operative interactions among two or more individuals -- related or unrelated -- produces selectively advantageous synergistic effects for all parties (on average), the co-operating "players" may become a unit of selection. A synergistic functional group might be favored in competition with other groups, or with ecological competitors from other species, or with the statistical probability of their survival and reproduction in the absence of co-operation. (More broadly, synergistic selection can be defined in terms of gene combinations that enable/induce synergistic functional effects at various levels of biological organization. For a model related to the multicellular level, see Michod 1996.) SYNERGISTIC SELECTION The concept of functional group selection, or synergistic selection, can be illustrated by returning to Maynard Smith and Szathmáry's sculling and rowing models, as described above. What if the object of the game were changed? Rather than merely crossing a river (say), now the two oarsmen in each boat share the objective of winning a race against the other boat. Now it has become a functional group selection game (see Figure II). In this situation, if either oarsman were to defect, their "team" might lose the race; only all-out co-operation would provide rewards for either player. (Note that the two payoff matrices are now identical.) Now the sculling and the rowing games are functionally equivalent in the sense that the performance of either boat depends upon both oarsmen; they have both become "functional groups"; there is "synergistic selection." Furthermore, whether the oarsmen are related or not is irrelevant.
Figure II: A Group Selection Game
Below are a few specific examples of synergistic selection:
DOWNWARD CAUSATION Closely related to the notion of functional group selection, or synergistic selection, as an evolutionary phenomenon is the concept of "downward causation." The term was actually coined by psychobiologist Roger Sperry (1969, 1991, inter alia) in connection with the functional organization and operation of the human brain -- i.e., cybernetic control processes. (It may be that psychologist Donald Campbell, 1974, developed the concept independently.) Sperry was fond of using as an illustration the metaphor of a wheel rolling down hill; its rim, all of its spokes, indeed all of its atoms, are compelled to go along for the ride. We will use the term here in a slightly different sense. Downward causation in this context refers to the selective influences that have shaped the evolution of co-operative phenomena generally and complexity in particular. Why do selfish genes co-operate in ways that produce teamwork which, in turn, leads to interdependency? What compels them to subordinate their interests to the interests of the "whole"? To be specific, how did morphological castes and a division of labor evolve in army ants? How do reproductive controls evolve in mutualistic symbioses where, as Margulis (1993) points out, there must of necessity be reproductive synchronization if the relationship is to remain stable? (See also the discussion of "sociogenesis" in E.O. Wilson 1985; also Buss 1987; Smith 1992; and the examples cited in Leigh 1991.) Equally important, how can the potential for cheating among selfish genes (or selfish individuals) be constrained? Downward causation in an evolutionary context refers to the fact that the functional (synergistic) properties of the whole become a selective "screen" -- a significant influence on the differential survival/reproduction of the parts. Sometimes the parts might be disadvantaged (e.g., non-reproductive workers), and kin selection may help us to understand how such sacrifices for the common good may occur. But, as the evidence cited above indicates, kinship is not a sine qua non. The whole may also be sustained by fitness tradeoffs; that is, the costs may be offset by commensurate benefits. For instance, an animal that is at risk from predators might suffer a reduction in its relative reproductive fitness in a social group setting, but it may also enjoy greatly enhanced odds of survival and absolute fitness. (This may help to explain why defeated contenders for breeding privileges sometimes stay on in the group and may even serve as helpers.) To quote Dawkins again: "In natural selection, genes are always selected for their capacity to flourish in the environment in which they find themselves...But from each gene's point of view, perhaps the most important part of its environment is all the other genes that it encounters [his emphasis]...Doing well in such environments will turn out to be equivalent to ‘collaborating' with these other genes" (1987/1986: 170,171). In some cases, the whole may represent an unalloyed benefit for the parts with little or no costs. Many cases of mutualistic symbioses seem to fit into this category. For instance, Margulis (1993) is adamant about the co-operativeness, promiscuity (and evolutionary significance) of bacterial colonies. (See also the parallel argument of Shapiro, 1988.) Thus, an isolated bacterium would be cut off from access both to the extensive gene swapping and the collective environmental "intelligence" (information) that commonly exists in bacterial colonies, not to mention the advantages of a division of labor and various collaborative efforts. Among mammals, some Cataceans may also fit the mutualistic category, although not enough is as yet known for certain about their breeding patterns (see Würsig 1988, 1989). Conversely, the power of a social group to isolate or ostracize a free-rider can be a significant deterrent and an agency of negative (downward) selection. In any case, the synergies that result from co-operation may selectively "reinforce" co-operative behavior (to use the terminology of behaviorist psychology), and this may in turn differentially favor the evolution of relevant morphological/psychological characters over time. Thus, army ant sub-majors have acquired anatomical specializations that facilitate their role as "porters," and humans have evolved psychological predispositions that help us to orchestrate (and even enjoy) our participation in group activities. In sum, the relevant "parameters" for explaining co-operative phenomena in nature (and in human societies) may include genetic relatedness, but kinship is neither necessary nor sufficient. The key lies in functional synergy and its bioeconomic consequences for differential survival and reproduction in a specific context; functional synergy is the frequently unappreciated common denominator in various models of co-operative behavior in sociobiology. SUPERORGANISMS Holistic Darwinism, and a multilevelled view of the evolutionary process, may also provide some additional insight into the venerable concept of a "superorganism". A well-known metaphor for social wholes that many theorists have found distasteful (e.g., George Williams and Richard Dawkins), the term superorganism was coined, in its modern incarnation, by Herbert Spencer (1897/1874-82]). Spencer used it to connote the fact that societies exhibit a degree of functional interdependence that is analogous to the division of labor found in complex organisms.7 Subsequent generations of theorists, both in biology and in the social sciences, have freely borrowed Spencer's term (often without attribution) and have generally used it either more loosely or more narrowly than Spencer intended. Sometimes the superorganism concept has even been endowed with mystical properties or an autonomous self-interest, making it a sort of metaphorical antipode of Dawkins's selfish gene. At the other extreme, Moritz and Southwick (1992), while arguing for a revival of the concept after a generation of being out of favor among biologists, nonetheless chose to use a very restrictive definition. Among other things, they require a segregation of sterile and reproductive castes, which pretty much confines their usage to eusocial insects. Not even a human society is a superorganism by that standard. We prefer to define a superorganism, in the spirit of Spencer (and Plato before him), as: a behavioral system (social system) in which there are functional interdependencies and coordinated, joint actions with respect to one or more collective, goal-related activities. Thus, it can be said that the term superorganism refers only to a limited (and variable) aspect of any given social organization. Moreover, a particular group's superorganismic properties may change over the course of time. For example, while some of the coalitions and alliances that occur in various primate species are stable and long-lasting, many others are ephemeral, short-lived and situation-specific (de Waal 1982, 1996). Yet, regardless of the duration, each of these groupings can be characterized by an implicit collective goal and the coordination of individual behavior toward the realization of that goal, whether it be group defense, group hunting, dominance competition, rivalry over mating privileges, or the like.8
As Spencer suggested, the concept of a superorganism is also closely linked to what economists have traditionally called a "division of labor" -- though in many cases it could be termed, perhaps more felicitously, a combination of labor.9 Not only have various divisions/combinations of labor played a central role in the evolution of human societies, but they have also been prodigious generators of functional synergy in the overall evolutionary process. To cite a few, perhaps less familiar examples:
THE "SELFISH GENOME" All of this holism begs a question, however. Do wholes have goals that transcend the goals of the parts? Can wholes come to exercise a degree of autonomous control as wholes? In other words, can we postulate a "selfish genome?" The neo-Darwinian response, it appears, is a somewhat equivocal "no". Richard Dawkins (1989/1976) became famous for the assertion that organisms are merely "robot vehicles" that have been blindly programmed to serve the interests of the genes, yet (as noted earlier) he also allowed that genes can be selected for their ability to serve the interests of the gene team. And George Williams (1966), while acknowledging the wholeness and unity of organisms, characterized many of the claims regarding superorganisms as figments of a "romantic imagination" (p.220). In truth, some of these superorganismic claims were inflated, but Williams's view of this issue was perhaps a bit too-jaundiced: "A wolf can live on elk only when it attacks its prey in the company of other wolves with similar dietary tendencies. I am not aware, however, of any evidence of functional organization of wolf packs" (pp. 217-218). In contrast, Holistic Darwinism postulates that wholes at various levels of biological organization may evolve mechanisms that permit partially-autonomous control over the parts and their actions. Some insight into how superordinate controls can evolve in nature is provided in Egbert Leigh's various discussions of how groups might act to contain or override individual advantages for the good of the group -- what he calls the "parliament of the genes" (Leigh 1971, 1977, 1983, 1991; see also Michod 1996). Leigh's argument, in essence, is that, if the potential payoffs (synergies) for each of the participants in a co-operative relationship are high enough, this could also provide an incentive for the imposition of "government" in the "public interest." Leigh even draws on Adam Smith's reasoning, not from The Wealth of Nations (1964/1776) but from the less well-known The Theory of Moral Sentiments (1976/1759). Although it is not widely appreciated, Smith argued for the necessity of a system of laws and appropriate means of enforcement in human societies to resist the dangers of unfettered self-interest. (pp., 86, 88-89, 340-341). A key to understanding the evolution of "government" at various levels of biological organization may lie in what could be called the "paradox of dependency." Although co-operative interactions may produce individual fitness-enhancing synergies, a tradeoff may be that the more valuable the benefits the more likely it is that the parts will become dependent upon the whole. As the benefits of co-operation increase, so may the costs of not doing so. Wholes may then become obligatory survival units, one consequence of which may be that a decrement in the performance of the whole might result in the demise of the parts. An example can be found in a long-term study by Jeon (1972, 1983). A strain of Amoeba proteus were initially infected with bacterial parasites that were resistant to the hosts' digestive enzymes. After 200 generations, or 18 months, a mutualistic relationship had become established, and after 10 years the symbionts had developed complete interdependence. (Jeon, 1992, has also illuminated some of the biochemistry of these changes.) It should also be noted that Margulis (1993) makes a similar argument with respect to the integration of symbiotic organelles in the ancestral eukaryotic cells. An obvious implication is that the incentives (both proximate and ultimate) for imposing government over the parts are likely to increase in relation to the degree of interdependency among the parts, and the advantages of operating as a superorganism.10 In fact, in what may appear to be an utter contradiction of classical neo-Darwinism, it may often be the case that it is in the interest of a gene, or an individual, to promote the well-being of an interdependent "other", simply because functional interdependence means just that; it's "one for all, and all for one," to borrow a legendary slogan. Consider this hypothetical example. If one of the two oarsmen in the rowing game (above) should suffer from thirst and dehydration in the summer heat (he forgot his water bottle), his partner might decide to share his/her water supply, in the interest of reaching their joint goal. Or, to cite a concrete example from nature, consider the exquisitely complex energy-production services that the mitochondria provide for eukaryotic cells, in their own direct self-interest. Or, for that matter, consider the innumerable situations in human societies where our well-being depends, unequivocally, upon the performance of others -- airline pilots, railroad engineers, surgeons, and the other motorists that we encounter on the highways, to name a few. How do we explain these co-operative relationships? They have nothing to do with altruism, kin selection, reciprocal altruism or even (strictly speaking) tit-for-tat mutualism. They are sustained by "pure" self-interest. One compelling example of a superorganism in nature involves the naked mole-rat (Heterocephalus glaber), a unique African rodent species that lives in large underground colonies (usually numbering 75-80 but sometimes over 200). Naked mole-rats represent a particularly significant illustration of an economic division of labor, because these odd-looking animals -- affectionately dubbed "sabre-toothed sausages" -- have morphologically-specialized castes and a pattern of breeding restrictions that is both unique among mammals and suggestive of eusocial insects. Typically (but not always), the breeding is done by a single "queen", with other reproductively suppressed females waiting in the wings. The smallest of the non-breeders, both males and females, engage co-operatively in tunnel-digging, tunnel-cleaning and nest-making, as well as in carrying pups, foraging and the transportation of food (succulent tubers) within the colony's often extensive tunnel systems. (One investigator, Robert A. Brett, found a tunnel system in Kenya that was more that 3 kilometers long, altogether, and occupied an area equivalent to 20 football fields.) Sherman et al., (1992:75), who have studied these animals extensively, provide the following description of the mole-rats' co-operative tunnel-building efforts: The animals line up head-to-tail behind an individual who is gnawing [with it's outsized, powerful front teeth] on the earth at the end of a developing tunnel. Once a pile of soil has accumulated behind the digger, the next mole-rat in line begins transporting it through the tunnel system, often by sweeping it backward with its hind feet. Colony mates stand on tiptoe and allow the earthmover to pass underneath them; then, in turn, they each take their place at the head of the line. When the earthmover finally arrives at a surface opening, it sweeps its load to a large colony mate that has stationed itself there. This "volcanoer" [so-called because its actions appear to an observer outside to resemble miniature volcano eruptions] ejects the dirt in a fine spray with powerful kicks of its hind feet, while the smaller worker rejoins the living conveyor belt. The vital and dangerous role of defense in a mole-rat colony is also allocated to the largest colony members, who respond to intruders, such as predatory snakes, by trying to kill or bury them and by sealing off the tunnel system to protect the colony. The mole-rats' "militia" will also mobilize for defense against intruders from other colonies. Why do mole-rats utilize this highly co-operative survival strategy? Eusociality is relatively rare in nature, and the traditional view has been that a haplodiploid reproductive pattern provides a genetic facilitator. But this is obviously not the case with mole-rats, which are diploid. (Indeed, it seems that haplodiploidy is neither necessary nor sufficient; all species of Hymenoptera are haplodiploid, but most are not eusocial; on the other hand, all termites are eusocial and diploid.) Sherman et al., (1992) provide a bioeconomic (synergy) explanation for the mole-rat strategy: "We hypothesize that naked mole-rats live in groups because of several ecological factors. The harsh environment, patchy food distribution and the difficulty of burrowing when the soil is dry and hard, as well as intense predation, make dispersal and independent breeding almost impossible. By co-operating to build, maintain and defend a food-rich subterranean fortress, each mole-rat enhances its own survival" (p.78). (See also Sherman et al., 1991.) (Although it is not stressed in the mole-rat research literature, another critically important facilitator is a co-operative relationship -- and synergy -- between the mole-rats and an endosymbiotic bacterium which is able to break down the cellulose in succulent tubers.) If the bioeconomics -- the functional synergies -- provide an important part of the explanation for the naked mole-rat survival strategy, the "political" aspects are equally important, and are also well-documented. As is the case with many other socially-organized species, naked mole-rats exhibit a combination of self-organized co-operation (pre-programmed individual "volunteerism") and orchestrated social controls that are policed by various coercive means. The control role of the breeding queen is of central importance. The queen is usually the largest animal in the colony (size usually determines the dominance hierarchy), and she aggressively patrols, prods, shoves and vocally harangues the other animals to perform their appointed tasks. Indeed, it has been observed that her level of aggressiveness varies with the relative urgency of the tasks at hand. In addition, the queen acts to suppress breeding and reproduction on the part of non-queen females, who are always ready to take over that role. (Occasionally other females are allowed to share the breeding function with the queen; why this is so is not known.) The queen also intervenes frequently in the low-level competition that goes on among colony members over such things as nesting sites and the exploitation of food sources. And when the reigning queen dies, there is a sometimes bloody contest among the remaining females to determine her successor. All of this control activity is facilitated by an elaborate communication system that includes 17 distinct categories of vocalizations -- alarms, recruitment calls, defensive alerts, aggressive threats, breeding signals, etc. In fact, the mole-rats' communication system rivals that of some primate species in its level of sophistication. Thus, a naked mole-rat colony may be characterized as a superorganism with a superordinate system of cybernetic control ("government"), along with clear evidence of downward causation in the mole-rats' morphological specializations and breeding restrictions. One final point related to "downward causation," "government" and the "selfish genome." At the most basic level of biological organization (the genome itself), there is mounting evidence that the genes do not inhabit a "bean bag" (in Ernst Mayr's felicitous caricature), and that morphogenesis is not a "mindless" process. Rather, it is an organized, cybernatic process which entails the extensive use of superordinate feedback controls (the very essence of a "teleonomic" system). In other words, selfish genes are only citizens on good behavior in the selfish genome, and the outlaws, tax evaders and parasites among them do not have a license to pursue their anti-social interests ad libitum. EVOLUTION AS A MULTILEVEL PROCESS
There is one other aspect of Holistic Darwinism that should be mentioned briefly. It relates to the traditional distinctions between parts and wholes, individuals and groups, even "self-interest" and the "public interest." During the past decade or so, there has been a growing appreciation of the fact that evolution is a multilevelled, hierarchical (some prefer "holarchical") process, just as survival and reproduction is a multifaceted problem (see especially Koestler 1967; Corning 1983; Brandon and Burian 1984; Eldredge and Salthe 1984; Salthe 1985; Eldredge 1985, 1995; Buss 1987; Grene 1987; Gould 1994; Wilson and Sober 1994; Maynard Smith and Szathmáry 1995; Michod 1996). In essence, there is a recognition that natural section operates at various levels of biological organization -- from genes to ecosystems -- often simultaneously. One implication of this more complex view of evolution is that both competition and co-operation may coexist at different levels of organization, or in relation to different aspects of the survival enterprise. There may be a delicately balanced interplay between these supposedly polar relationships. To illustrate: EMERGENT EVOLUTION Closely associated with this multi-levelled paradigm is the venerable concept of "emergent evolution." The concept traces back at least to the 1920s, when C. Lloyd Morgan (1923), Jan Smuts (1926), William Morton Wheeler (1927) and others mounted a theoretical counterattack against the reductionist evolutionary theories of August Weismann (1891, 1902), Hugo de Vries (1901) and others of the so-called "mutationist" school, which many people at that time viewed as an alternative to Darwin's theory. The underlying theme of emergent evolutionism is familiar to us. The central idea is that evolved "wholes" (organisms, groups and species) are significant units of evolutionary change and are not reducible to the sum of their parts. Some of these early holists, like Smuts, asserted that whole organisms were the "only" unit of evolutionary change. Citing Charles Darwin's flirtation with Lamarckism as a precedent for his own views, Smuts also suggested that "holistic selection," or the actions and choices of organisms, often precede and precipitate evolutionary changes. ("Organic selectionism," as it was more commonly called, has had a checkered history, which goes back to the end of the 19th century -- see Corning 1983, 1995, 1996a and below.) Although the term "emergent evolution" fell into disuse in the middle years of the century, it reemerged (so to speak) in, of all places, E.O. Wilson's Sociobiology: The New Synthesis (1975). In the very opening line of his second, foundation-building chapter, entitled "Elementary Concepts of Sociobiology," Wilson wrote: "The higher properties of life are emergent" (p.7). Wholes cannot be comprehended as a mere sum of their parts, he said. He also asserted that the "new holism," as he called it, is rigorous and testable, not a vague, mystical abstraction. What is the key? (Here I am augmenting Wilson's words.) The difference is that the "new holism" is based on the testable premise that natural selection also acts directly on wholes -- combinations of parts with synergistic functional properties which may be differentially selected, along with their genes, as emergent wholes (i.e., synergistic selection). So far as I know, Wilson's bold challenge to the monolithic reductionism of some of his colleagues was totally overlooked in the ensuing bitter controversy over sociobiology. Ironically, Wilson was portrayed as a genetic determinist (reductionist) and was accused of having "genitis" (the genetic disease), in Sherwood Washburn's pejorative term. The concept of emergent evolution has had a vigorous revival in the 1980s and 1990s, particularly in paleontology where it is often treated under the heading of "species selection." Although the theoretical roots of the contemporary debate trace back to the early days of population genetics and especially the work of Sewall Wright (1968-78) on what he called "interdemic selection," the term "species selection" was actually coined by Steven Stanley (1975, 1979), who was particularly concerned about how to explain the widely varying patterns of phenotype distributions among species. Needless to say, species selection was quickly challenged (e.g., Bock 1979, Vrba 1980, 1983). Bock characterized it an illusion; the so-called emergent properties of a species can be reduced to the interactions between individual organisms and their environments; any aggregate consequences are epiphenomenal. In a similar vein, Elizabeth Vrba advanced what she called "the effect hypothesis" -- the idea that speciation events could be the incidental consequences of a variety of non-adaptive factors and random accidents. Likewise, Gould (1982), Vrba and Eldredge (1984) and others proposed that the term species selection be narrowed in scope so as to apply, not to statistical patterns or the "aggregate properties" of populations but only to "emergent" higher-level functional properties that have a direct causal influence at the population/species level -- what Kawata (1995) calls "effective properties." An unambiguous case in point would be a bacterial colony, where the individual members reproduce independently and yet each bacterium benefits from various collaborative efforts -- from the food quest to environmental conditioning. I would argue that the distinction between "aggregate" properties and "emergent" properties is not so clear cut as it may appear. The key criterion for "higher-level" selection is that there are functional interdependencies among the "units". As Michael Ghiselin (1997) puts it, the aggregate must have some of the properties of an "individual". That is, if the differential survival and reproduction of a given "unit", or all of the units in combination, is materially affected by their relationships with one another (there is a "shared fate"), then it can properly be called emergent selection (synergistic selection). Obvious examples include the many cases in nature where the fitness of any given individual is density- or frequency-dependent -- some function of the size and spatial distribution of a population. Thus, if you are a member of a very small school of dwarf herring, your odds of getting eaten by a predatory barracuda may be considerably greater than if you are in a very large school; your fitness is a function of the "aggregate" size of your group. Likewise, the literature in ecology includes many instances of population "crashes"; for various reasons, a population may fall below some minimum threshold for successfully reproducing itself and may go extinct (as some of our commercial fishermen have been learning to their regret). A more subtle example of how "aggregate properties" may be irreducible involves the "gene pool" in a sexually reproducing population. One way to illustrate this point is by means of a thought experiment based on H.B.D. Kettlewell's (1955, 1973) classic studies of "industrial melanism." Kettlewell documented that the relative frequencies of two strains of moths found in the English countryside near its industrial cities had changed dramatically over the years. A mottled, "cryptic" strain (Biston betularia), originally the dominant form, had gradually been replaced by a darker, melanic form (Biston carbonaria). The reason, it was determined, was that the relative visibility of the two strains had markedly changed over time as industrial soot progressively blackened the trees that were the moths' favored resting places. Originally, the cryptic form had been less visible to avian predators, but now they stood out and the darker form blended in much better against the soot-blackened tree-trunks. Now consider a hypothetical variation on that real-world example of natural selection. Suppose there are two distinct, non-interbreeding species of moths. One species is totally cryptic in coloration (monomorphic), while the other has (initially) a 50-50 mixture of the melanic and cryptic forms (it is polymorphic). Selection from airborne predators commences suddenly (not an unusual occurence in nature) and operates equally in both species. In the monomorphic species, the population soon goes extinct and all of its genes are history. However, in the polymorphic species, the melanic and cryptic forms continue to interbreed and to maintain the population as a whole, including most of the genes of the melanic form as well. Over time, the frequency of the gene or genes associated with cryptic coloration declines and may disappear from that species' "gene pool" (as the textbook selection equations predict), but all of the other genes that were not subject to negative selection survive and prosper. There has been a form of "group selection," or "interdemic selection," or "species selection" (take your choice) between the two species, involving a species-level genetic "resource". (For a more extensive analysis of this paradigm, to which I am indebted, see Smillie 1995. Also, see Stidd and Wade 1995). TESTING HOLISTIC DARWINISM Can Holistic Darwinism be tested? Specifically, can we demonstrate the causal role of synergistic phenomena and functional group selection (synergistic selection) in evolution? There are at least three different ways of doing so. Game theory provides one possible means for formulating testable hypotheses of synergistic selection. Another method involves either experiments or "thought experiments" (like the one above) in which a major part is removed from the whole and the consequences are then observed (an idea originally suggested by Aristotle in The Metaphysics, 1041b11-31, to my astonishment). Thus, for example, it is not hard to imagine what would happen if a major gene were to be removed from the homeobox gene complex, or if the mitochondria were removed from a eukaryotic cell, or the gut bacteria from a termite, or the sub-majors from an army ant colony, or the water supply from a human settlement. A third means of testing for synergistic selection involves comparative analyses of various kinds. Lichens provide a ready-made example. Many of these symbiotic partnerships are facultative, and their constituent alga and fungi can exist independently. However, they do not go it alone in the barren environments which they are legendary for pioneering; their ability to survive in these more rigorous settings is dependent upon their joint capabilities. In short, if synergistic effects are real and measurable, an absence of synergy should also provide measurable comparisons. Human evolution may provide a singular illustration of the synergistic, functional group selection hypothesis. In effect, the principles which were elucidated above can also be observed in the evolution of the human species, and in cultural evolution as well. For various reasons, the evolution of humankind has often been portrayed as a process that is sui generis. Of course, this overlooks the fact that all of evolution can be said to be sui generis, given its historical and situation-specific causal dynamics. As Darwin himself put it in The Descent of Man (1874/1871), any evolutionary innovation depends upon many "concurrent favorable developments" that are always "tentative" (p. 150). Nevertheless, the evolution of humankind is undeniably one of the more remarkable episodes in evolutionary history. A number of suggestive and thoughtfully argued theories of human evolution have been advanced over the years. These theories were reviewed and critiqued in depth in Corning (1983), and a "synthetic" explanation was offered there that, in effect, combined Darwin's "tripartite" selection theory of human evolution -- family (kin) selection, mutualism (including reciprocity) and group selection -- with the concept of functional synergism. As Darwin pointed out, and this is a crucial point, the three modes of selection need not be opposed to one another; they can be complementary and mutually reinforcing. In addition, the synergism hypothesis asserts, in essence, that it was the bioeconomic payoffs (the synergies) associated with various forms of social co-operation that produced -- in combination -- the ultimate directional trend over a period of several million years, from the earliest bipedal hominids to modern Homo sapiens. That is, the synergies produced by various collaborative behavioral innovations provided "proximate" rewards or reinforcements (as the behaviorists would say) that were substantial enough to create a behavioral "pacemaker" (sensu Ernst Mayr, 1960) for the "progressive" evolution over time of our distinctive wardrobe of biological characteristics. In other words, we invented ourselves in response to various ecological pressures and opportunities -- a paradigm that may be more widely applicable to evolutionary change than is generally appreciated (see Corning 1996a). Here I can only summarize the argument.11 THE SYNERGISM HYPOTHESIS The traditional approach to explaining human evolution has been to propose a "prime mover" theory, which is typically portrayed as the "engine" that has powered the course of human evolution. Darwin, in The Descent of Man (1874[1871]), singled out the role of tool-making. E.O. Wilson (1975) stressed our primate "preadaptations" and speculated about the possible role of an unspecified "autocatalysis". Bipedalism, which we now know preceded the development of the "big brain," is currently viewed by many theorists as the "breakthrough" development (e.g., Johanson, Leakey, White, etc.). Major climate changes during the Miocene and Pliocene have also been suggested as important precipitating factors (e.g., Coppens, Vrba). Then there are the various competing "group theories": group hunting (Dart, Washburn, Ardrey, Thompson and others), group scavenging (Potts, Blumenshine, Shipman, etc.), female gathering (Zihlman and Tanner), the nuclear family and male provisioning (Lovejoy), collective defense against predation (Kruuk, Kortlandt, Alexander, etc.) and the ever-popular group conflict hypothesis, which traces back to Darwin and Spencer and which has been championed in this century by Dart, Keith, Ardrey, Lorenz, Bigelow, Otterbein, and Alexander, among others. In the latter stages of human evolution, climate change, population growth, food surpluses, the adoption of fire, language development, increased intelligence and warfare have also been singled out as prime movers by various theorists at various times. Holistic Darwinism suggests the contrarian view that all of these factors were important but that none was sufficient -- the engine is nothing without the car -- and that the answer lies in the unique combination of factors that produced, over time, many compatible and mutually supportive co-operative effects (functional synergies). Indeed, objections can be mounted against every one of the factors cited above, taken individually. For example, bipedalism is not unique to humans; birds are bipedal, after all, and kangaroo forelimbs have atrophied rather than becoming instruments for the skilled manipulation of tools. In fact, hominid bipedalism existed for some millions of years before the "big brain" emerged. Tool-making is also an insufficient explanation; we now know that many species make and use tools, especially our closest relatives the chimpanzees. And, again, crude stone tools were used by our hominid ancestors for perhaps a million years before the more refined and standardized Acheulean tool-kit appeared (Leakey 1994; Tattersall 1995). Group hunting and scavenging are also inadequate explanations, for the same reasons; our ancestors were hardly unique in this regard. The primeval gathering scenario and the nuclear family scenario are appealing, though difficult to support empirically, yet they are in any case insufficient because they overlook other factors -- namely, the often serious threat from potential predators and the premium associated with meat-getting (via scavenging, hunting or both) in the more open savanna-like environment in which some of the later hominid developments most likely occurred. Even the conflict hypothesis -- which Alexander (1979) asserts is both necessary and sufficient -- begs the question: why are there no nation-states composed of chimpanzees, which we now know can be quite warlike? The very absurdity of that idea highlights the fact that there had to be many other factors that "worked together" to propel the process. Indeed, the extensive hominid migrations out of Africa over time suggest that conflict avoidance might well have been a common adaptive strategy.
In a major critique of cultural evolution theories many years ago, anthropologist Elman Service came to this emphatic conclusion: "down with prime movers!" (1971:25) The same can be said, equally emphatically, of the larger process of human evolution. Prime mover arguments invariably take for granted some, or all, of the other requisites for survival and reproduction. Very often they reflect a kind of ecological naivete; they discount the many life-and-death challenges associated with living (and evolving) in a demanding and changeable environment over a period of several million years. But if no one factor alone can provide a sufficient explanation for the evolution of humankind, then what is sufficient? The answer is that all of the important human traits were necessary and none were sufficient. In effect, there was a mutually-reinforcing synergy among the key innovations -- combined effects that would not otherwise have been possible. Consider a few of the relevant points (here in outline form): "MAN MAKES HIMSELF" In sum, the dominant theme of human evolution may have been the expansion of various modes of social co-operation (including co-operative modes of competition), which have been rewarded with commensurate bioeconomic benefits. To reiterate, competition and co-operation are not mutually exclusive explanations for human evolution; both played an important role in shaping our evolution. Nevertheless, the thesis here is that increasingly potent (and selectively advantageous) forms of social co-operation may have given our ancestors the competitive edge. As Edward O. Wilson (1975; 1985) has noted, a multifaceted group-living ecological strategy is a relatively rare occurrence in nature. We rightly admire the complex social organization of honeybees, naked mole-rats, army ants and a small number of other highly social species, including some of our close primate relatives. The synergies that have made such collective survival strategies rewarding for various social species are increasingly well documented. We are among that select company, and it has been the key to our evolutionary success. A human society can be characterized as a "collective survival enterprise." We meet our basic survival needs through elaborate networks of social co-operation. We do not know, and likely never will know, the full story of our evolution as a species, although we are gradually adding more details to the outline and making better-informed guesses. However, there is reason to believe that behavioral changes in the direction of greater social co-operation for specific functional purposes were the "pacemakers" that precipitated supportive morphological changes. In a very real sense, as anthropologist V. Gordon Childe (1951[1936]) put it in the title of his famous book on the rise of civilization, the human species may have "invented" itself. The real key to human evolution, accordingly, was not any single prime mover but the entire suite of co-operative behavioral, cultural and morphological inventions -- a synergy of synergies.12 An oft-used (and important) illustration of this dynamic is the adoption by evolving hominids of the controlled use of fire (or, more broadly, various exogenous forms of energy). This is a uniquely human cultural invention and is still a major factor in our ongoing evolution -- a point that various energy-oriented theorists have thoroughly documented (e.g., White 1943, 1949; Cottrell 1953; Odum 1971; Adams 1975, 1988). The earliest strong evidence for the use of fire by our hominid ancestors is identified with the Middle Pleistocene, perhaps 200-400,000 years B.P. However, some theorists argue on plausibility grounds, albeit with more fragmentary evidence, for a much earlier date (see especially the cautious review by James 1989 and the offsetting commentary by Lewis). The controlled use of fire by hominids (in effect, a co-operative animal-tool symbiosis) had enormous long-term benefits. Over the course of time, fire was most likely used as an effective means of defense against predators; it was a source of warmth that facilitated migration into colder climates; it might well have served as an insect repellant and as a means for obtaining honey from bee hives (as a bee suppressant); it probably became a weapon for driving and capturing prey animals; it was a means for shaping and hardening tools; it could be used for conditioning the environment (as in slash and burn horticulture); and, not least, it enabled our ancestors to add to their diets many foods that would otherwise have been toxic, indigestible, or possibly even infectious if eaten raw (Leopold and Ardrey 1972; Stahl 1984 and commentaries). Fire represented the functional equivalent of a major morphological development. With the acquisition of fire, our ancestors were able to expand their niche over time, which in turn changed the selective forces to which our ancestors were subject. Furthermore, fire most likely became another focal point of social co-operation. Fire-keeping was a "collective good" that required a division of labor -- for gathering fire wood, fire tending, fire transport and, eventually, fire-making. In other words, this primordial hominid technology, like most human technologies, was at once a source of bioeconomic benefits and a generator of social co-operation and social organization. How can this synergistic theory of human evolution be tested? Let us try out a few thought experiments: Take away fire (along with other energy sources in modern societies); we are utterly dependent upon exogenous forms of energy. Or, take away language; or bipedalism; or tools and technology. In short, there is no major adaptive modality that we could do without; they are all necessary parts of an interdependent, synergistic system. CONCLUSION: A POST-NEO-DARWINIAN PARADIGM? I believe that Holistic Darwinism can plausibly be viewed as a candidate for a post-neo-Darwinian synthesis. It involves a paradigm that refocuses evolutionary theory on the "vessels" (to borrow a metaphor from our rowing examples) and their functional properties as the vanguard of evolutionary change. In fact, that is where natural selection as a causal dynamic actually occurs; to use an older turn of phrase, it is the vessels that are "tested" in the environment. Holistic Darwinism shifts our focus from the anthropomorphic purposes of selfish genes in theoretical isolation to the evolved, emergent purposiveness of the living systems as wholes, and to the functional interactions and relationships (adaptations in specific environments) that result in differential survival and reproduction. Equally important, Holistic Darwinism de-emphasizes (without denying) the role of genetic mutations, recombinations, transpositions, etc., as sources of creativity in evolution and emphasizes purposeful innovations which may occur at the behavioral, cognitive, even social levels (inclusive of symbiogenesis). In this model, proximate "teleonomic selections" by wholes (i.e., adapting organisms and, in some cases, adapting groups) assume a much more important role in evolutionary change than is acknowledged in neo-Darwinism. Finally, and perhaps most contentious of all, I maintain that Holistic Darwinism also encompasses human evolution and, indeed, the ongoing bio-cultural evolution of our species. It is a seamless theoretical framework that does not require any additional causal principle or "mechanism" to account for humankind.13 We must recognize human culture, human economies, even human political systems for what they truly are -- an augmentation of adaptive modalities that can be found in rudimentary form in many other species. (In this paradigm, the activities of humankind virtually everywhere on earth are viewed as an integral part of the evolutionary process, not something that is separate from it.) But, having recognized that, we must also acknowledge our uniqueness as a species. Complex human societies are as different from those of honeybees or naked mole-rats or even chimpanzees as complex multicellular organisms are from single-celled protists. The cumulative, synergistic effects of many differences in degree have produced a difference in kind -- and a dynamic of rapid change at the behavioral/cultural level that is obviously unique. This is an evolutionary development that Holistic Darwinism can fully comprehend. It is not even conceivable in a theoretical world that barely recognizes the existence of wholes. I believe that it is time to refocus the Necker cube on the problem of explaining the evolution of complex wholes in a way that is fully consistent with Darwin's vision. In the long run, I believe that the Darwinian, functional explanation of complexity will prevail over various orthogenetic theories of "self-organization" (in reality a teleological "black box" that begs the question), or theories that postulate a random "drunkard's walk" (Gould 1996) -- a formulation which tacitly ignores the functional costs and benefits related to the evolution of biological complexity; complexity is not a free lunch but a cumulation of adaptive changes over the eons. (This is a surprising argument, coming from such a sophisticated and articulate student of evolution.)14 I can only second the conclusion of George Williams in the peroration of his famous book (1966:273): "It may not, in any absolute or permanent sense, represent the truth, but I am convinced that it is the light and the way."
REFERENCES / BIBLIOGRAPHY
Adams, R. (1975). Energy and Structure. Austin: University of Texas Press. ACKNOWLEDGEMENTS The author wishes to thank the following for encouragement and helpful suggestions on an earlier version of this paper: Howard Bloom, Michael Ghiselin, Lynn Margulis, Peter Meyer, John Maynard Smith, Ernst Mayr, Anatol Rapoport, John Paul Scott, David Smillie, Eörs Szathmáry, and David Sloan Wilson. I also benefitted from an on-line discussion of some of these issues among the members of Howard Bloom's International Paleopsychology Project group. Particularly helpful were the comments of David Smillie, Timothy Perper and Peter Frost. The diligent and resourceful research efforts of Patrick Tower are also greatly appreciated, along with the indispensable bibliographic assistance of Kitty Chiu. |
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