Jablonka & Lamb (J&L) have produced an admirable synthesis in Evolution in Four Dimensions (Jablonka & Lamb Reference Jablonka and Lamb2005), showing how processes with vastly different underlying mechanisms constitute important, interrelated facets of evolution. Ironically, although their intent is to highlight Lamarckian aspects of evolution, their framework discourages it. If genetic and cultural evolution were viewed not as components of one big, four-dimensional evolutionary process but as two intertwined evolutionary processes, one primarily Darwinian and the other primarily Lamarckian, there would be no need to rely heavily on genetic assimilation as the means by which behavioral and symbolic systems exert a lasting evolutionary effect. (Behavioral and symbolic systems affect cultural evolution regardless of whether they affect genes.) The focus on genetic assimilation leads to a gradualist scenario for the transition to symbolic thought that is unsupported, as is the contention that symbolic thought followed naturally from possessing a larger brain (p. 304). Leakey (Reference Leakey1984) writes of human populations in the Middle East that had brains that were modern in shape and size, but virtually nothing in the way of symbolic culture, and concludes, “The link between anatomy and behavior therefore seems to break” (Leakey Reference Leakey1984, p. 95). This suggests that encephalization was followed by an enhanced capacity to make use of a larger brain. To my mind, the most reasonable explanation for the transition to symbolic thought is that genetic mutation facilitated the capacity to subconsciously shift between focused and defocused attention, thereby shifting between analytic thought, which is conducive to logic and symbol manipulation, and associative thought, which is conducive to analogy and “breaking out of a rut” (Gabora Reference Gabora, Alterman and Hirsch2003). Onset of this capacity would confer upon the mind both hierarchical structure and associative richness conducive to language and other complex tasks. Another hypothesis is that once culturally generated artifacts created sufficient change in the environment, cultural evolution simply snowballed, without any underlying genetic change at all (e.g., Donald Reference Donald1991; Reference Donald1993). Explanations such as these that do not rely on genetic assimilation cannot be ruled out.
The authors' reason for treating behavioral and symbolic transmission as distinct dimensions is that behavior must be displayed, whereas symbols can transmit latent information that skips generations (Jablonka & Lamb Reference Jablonka and Lamb2005, p. 202). This distinction breaks down when one considers real transmission among creative individuals operating in different contexts with different abilities. Consider the following simple scenario. Ann pats the cat. Bob, who is sitting in a chair holding a baby, sees this and nuzzles the cat with his foot. Cindy, who sees Bob but not Ann, pats the cat. Thus, the patting skipped a generation. The other rationale given for treating symbols as distinct – that symbols must be taught, whereas behavior need not be – is also not strictly true. In my view, both behavior and symbol use reflect the primarily non-Darwinian cultural evolution of a world-view – the individual's means of internally construing the world and his or her place in it. At any rate, a stronger argument should be made for treating symbols and behavior separately.
Throughout the book, J&L assume that epigenetic, behavioral, and symbolic change proceed through natural selection (a move Darwin himself never made). They speak of “selection of epigenetic variants” (p. 359) and “a change in the parents' behavior that generates a new behavioral variant” (p. 166), and refer to their theory as a “version of Darwinism” (p. 356). However, for a process to evolve through natural selection, inheritance of acquired characteristics must be negligible compared to change resulting from differential replication of individuals with heritable variation competing for scarce resources. What necessitated the theory of natural selection, a theory of population-level change, is that acquired traits are not inherited from parent to offspring at the individual level. In a world in which if a cat bites off a rat's tail, the rat's offspring are not born tail-less, how does one explain how change accumulates? That was the paradox Darwin faced – the paradox for which natural selection provided a solution. There is no such paradox for early life or culture, because they do not replicate using a template, a self-assembly code that is both actively transcribed to produce a new individual and passively copied to ensure that the new individual can itself reproduce. The individual may change, but the passively copied code does not. The mathematical framework of natural selection is not transferable to evolutionary processes that are not code-driven (Gabora Reference Gabora2006). Such processes are correctly described in terms of “actualizing potential” rather than “selecting amongst variants.”
I suspect many will find the arguments concerning the key role played by epigenetic processes ultimately unconvincing, because of the paucity of heritable epigenetic change. (How much of what we or Jaynusians [inhabitants of the imaginary planet Janus that J&L refer to at length in their book to illustrate key points] learn or acquire in a lifetime is transmissible through the germ line?) The authors' position could be strengthened by considering recent work which indicates that epigenetic inheritance not only began in simple unicellular organisms (as they rightly point out), but was the means by which early life evolved (Gabora Reference Gabora2006; Vetsigian et al. Reference Vetsigian, Woese and Goldenfeld2006). Given the book's breadth, it is understandable that the origin of life is considered “outside the scope of this book” (p. 320). However, to me this felt like going on a treasure hunt, peeking down the alley that holds the treasure, and passing it by. When one realizes that there existed a time in which self-organized structure replicated (albeit sloppily) through autocatalysis prior to the onset of template-mediated replication, one appreciates that epigenetic processes are what provided the means by which this primitive structure evolved the genetic code itself.
J&L's contention that epigenetic processes constitute a distinct and important dimension of evolution is indeed strengthened by the realization that they cannot be described by natural selection, which is intimately tied to the genetic code. This also gives us a clear rationale for treating cultural evolution, a non-Darwinian process with behavioral and symbolic components, as distinct from genetic evolution (and the epigenetic processes it grew out of). Indeed, it has been suggested that cultural evolution operates through a mechanism very similar to the one by which early life evolved (Gabora Reference Gabora2004). The evolving entity, the individual's conceptual network, or (from a subjective perspective) internal model of the world, or worldview, is – like a primitive life form – integrated, self-organizing, and self-mending.