Charles Darwin was never entirely satisfied with the evolutionary role he originally gave to natural selection in On the Origin of Species. He later expressed reservations about attributing too much of evolution to the action of natural selection and survival of the fittest because he became convinced that nonfunctional structures evolving without natural selection could later prove to be useful and therefore come within the range of natural selection. Darwin thought his failure to sufficiently consider the existence of structures that are neither beneficial nor injurious was one of the greatest oversights in his work. He realized that he was not able to eliminate entirely the influence of his former belief that each species had been purposely created and each structure was of some special service. He felt that anyone with this assumption in mind would naturally extend the action of natural selection too far.
Darwin’s observation on the link between natural selection and a belief in the purposeful creation of species remains applicable to much of evolutionary biology today. Evolutionary approaches in anthropology and archeology are largely reduced to imagining the evolutionary advantage conferred by an adaptation, and this presumed advantage is supposed to explain why the adaptation came into existence. In a recent compendium on the evolution of great ape intelligence, for example, authors repeatedly imagined selection pressures that were supposed to have increased the intellectual ability of great apes compared with other primates. Because a larger and more complex brain was more costly, it had to be an advantage so that it could be selected to provide the advantages by which it would exist in the first place. Never, in any of these arguments, is there any empirical demonstration that such adaptations owed their origin to the past action of natural selection or that the advantages incurred had anything to do with their origin.
The appeal to imagined selection pressures is superficially very attractive because it requires no deeper understanding of biological structure beyond the constraints of imagination. As Darwin correctly identified, the mode of reasoning is scientifically problematic because it involves an explanation of the origin of a structure in terms of its purpose in servicing the organisms’ future survival and reproductive success. Many modern practitioners of evolution appear to be unaware of Darwin’s concerns, and with natural selection shown to have an ecological reality, it would seem to be a simple extrapolation to assume its role in evolution as well.
The use of teleological reasoning—the explanation of origin in terms of future purpose—is perhaps one of the greatest ironies of evolutionary biology. Evolution was supposed to end this kind of reasoning and yet it continues as the most popular and pervasive form of biological reasoning. Teleology makes nonsense of biology because it reverses the actual relationship between morphology and genetics by treating morphology as a response to a need that in turn determines the genetic basis for a feature’s existence. This developmental relationship is the wrong way around because it is the pathways of molecular communication that produce morphology in the first place, and it is the organism’s morphology that constrains what the organism can or cannot do. In what Jeffery Schwartz recently called the “vacuum theory of evolution and adaptation,” the biological structure or adaptation of an organism is sucked into a function, and the genetic foundations of this form are sucked along the way.
Darwin not only questioned the applicability of natural selection to evolution, he also attributed the origin of nonbeneficial structures to “laws of growth” acting independently of natural selection. The nature of these laws was characterized as being largely unknown, although he suggested general possibilities such as “correlation,” “compensation,” and structural “pressure.” His views reflected a concept of biological organization that determined the kind of changes that could take place in the evolution and adaptation of an organism. With the widespread skepticism about natural selection among most evolutionary biologists through the late 19th and early 20th centuries, there was considerable interest in alternative models that looked to a biologically mediated process of evolution. One of the most prominent non-Darwinian models was “orthogenesis,” proposed in 1893 by William Haacke. Like many other evolutionists, Haacke noted a sequential pattern of changes in the biological structure, particularly in the fossil record. These changes suggested to Haacke that there was a biological link historically connecting the sequence of evolutionary changes. He cited the well-known example of the single-toed modern horse that did not evolve directly from a five-toed ancestor, but involved interim toe combinations. Terms such as Berg’s nomogenesis and Rosa’s hologenesis also represented similar concepts. These alternatives to natural selection encompassed the principle of organisms evolving as a consequence of their biological properties. Organisms were not passive blobs of organic jelly that sat around doing nothing until pushed by an external force such as natural selection. Rather, there were two active elements in evolution—the organism and the environment.
The combination of Mendelian and population genetics in the 1930s was seen by architects of the Darwinian synthesis to substantiate the primary role of natural selection in evolution. As selection became more popular, orthogenetic models waned under the burden of having no comparable explanatory mechanism and the problematic application of orthogenesis to teleological models by some evolutionists. Prominent Darwinian scholars such as George Gaylord Simpson, Ernst Mayr, and Stephen Jay Gould dismissed orthogenesis as an imaginary, if not a mystical, dead end, often equating the concept to the idea of “straight-line” evolution (instead of branching), even though this representation was historically incorrect. Ironically, Darwinians such as Gould and Eldredge ended up dabbling with orthogenetic ideas when they acknowledged that the origin of variation could not be entirely random because it was apparent that there were structural constraints in the type of organization of an organism at any given time. However, unlike Darwin’s laws of growth, structural constraints were not a mechanism generating change, just a limit on the mutational possibilities that were still random and spread through the action of natural selection.
Concurrent with the Darwinian evolutionary synthesis was a distinctly non-Darwinian panbiogeographic synthesis proposed by the French-Italian biologist Leon Croizat. Whereas most evolutionary theorists focused on the origin of species in terms of their biological differentiation and adaptation, Croizat developed a theory focused on their geographic differentiation, because all species evolve in both space and time. It was geographic distribution that provided Darwin with evidence for evolution. Darwin attempted to synthesize the great problem of spatial separation between related species by proposing an original, localized birthplace or center of origin from which the species dispersed either before or after the formation of geographic barriers. This idea of geographically localized origin allowed for natural selection to affect the evolution of individual populations, and therefore speciation.
Croizat’s unique insight was to test Darwin’s theory of evolution as no one had done before, by graphically comparing distributional patterns of related taxa with each other and their dispersal ability. He found that there was no correspondence between dispersal ability and the geographic range or pattern of a group. A group of poor dispersers could be distributed as widely as a group of good dispersers. The lack of concordance between dispersal ability and distribution suggested that the location of related species in different localities was the result of their having each originated in their different localities. This vicariant origin required a different evolutionary model to that of Darwin’s centers of origin theory. Croizat suggested that vicariant species (or any other taxonomic entities) occur in different localities because the ancestor was formerly wide-spread and each descendant species differentiated over part of the ancestral range, giving the appearance that they had each resulted from dispersal, particularly when they may now be geographically isolated by topographical or ecological barriers. In a spatial context, the center of origin for any one vicariant species would be the entire ancestral range established during earlier geologically mediated periods of mobility.
The biogeographic process of geographically widespread differentiation involving multiple species led Croizat to propose a biological mechanism for speciation and evolution. His model was for different evolutionary trends to take place over different parts of the ancestral range as a consequence of the geographically heterogeneous distribution of ancestral characters. An ancestor with characters (a + b + c + d. . .) would vicariously evolve into descendants with characters (a + b), (a + c), (b + c), and so on, according to the geographic clustering of those characters. He also looked to biological structure and, as Gould and Eldredge noticed many years later (although Gould had read Croizat’s 1958 book during graduate school), Croizat recognized that organisms represented particular types of organization that constrained and oriented the range and direction of evolution without requiring natural selection. Croizat identified the process as orthogenetic and compatible with Darwin’s concept of laws of growth.
Croizat was the first evolutionist to attempt a comprehensive synthesis of orthogenesis and natural selection by viewing orthogenesis as the primary constraint upon the evolution of novelty, whereas natural selection provided fine-tuning between the structure of an organism and its environment. He also drew attention to the developmental relationship between different morphologies, such as the interchangeable positions of legs, wings, and antennae on flies, as the result of a common developmental process. These observations led to a general model of biological development that he called morphogenesis, whereby a single developmental process could be altered slightly to generate many different individual morphologies. In genetic terms, Croizat described this as the recombination of ancestral characters resulting in descendants as specialized versions of the generalized ancestor.
Despite objections by Darwinian theorists to orthogenetic models, molecular and developmental studies also point to a complex, interconnected biological foundation for the origin and evolution of variation. The geneticist Gabriel Dover (University of Leicester) and the primate systematist Jeffrey Schwartz (University of Pittsburgh) have both proposed radical departures from the general Darwinian assumption of evolution being primarily the result of natural selection acting on minute incremental changes in variation. In contrast, they emphasize the role of regulatory genes affecting the presence or absence of entire structures or organ systems, so evolution may not require incremental missing links between different biological forms or structures (for example, the evolution of the eye may not require intermediate and incomplete ancestral eyes). Although selection may change the pattern of variation for a given structure, selection acting upon that structural variation will not make it disappear altogether.
Developmental genetics suggests that the origin of biological structure involves a web of interactions between regulatory and structural genes in which one gene can turn a variety of other genes on or off. This is not a simple relationship between particular regulatory and structural genes and a specific structure, because both master and target genes may participate in many different functions involving unrelated developmental, metabolic, and behavioral processes. With genes each contributing to a function or structure through molecular interactions with other genes and their proteins, any given gene can be involved with multiple partner genes, and it is the combination of partners in any given cell at any time during development that gives rise to a particular part of the individual organisms. No individual gene, or even complex of genes, exists uniquely for a given biological function. A given species-specific structure emerges at the right time and place when a group of multifunctional genes is active or inactive in the appropriate combination at a given location and point in time. This coincidence of gene interactions at a particular stage of development is, itself, contingent upon earlier combinations of genes that can also involve some of the same genes.
This complex and contingent relationship between regulatory and structural genes does not support the popular selection-based narratives that assume that biological structures and adaptations are the result of incremental changes in variation. Morphogenesis involves a complex relationship between regulatory and structural genes that lies outside the popular model of incremental variation and natural selection. Dover focused on the nonindependent evolution of repetitive DNA sequences called concerted evolution, which suggests that there are nonreciprocal transfers of sequence information, such as biased gene conversion, that spread mutations through an entire gene family and a sexually reproducing population. This spreading mechanism, called molecular drive, can result in a long-term change in the genetic composition of a population, and where the gene involves multiple copies, it cannot be spread through natural selection because the mutation must convert multiple sites. As these mutations become established, a phenotypic transformation of a population may permit the organism to exploit previously inaccessible components of the environment. Schwartz looked to a Mendelian mechanism of genetic turnover involving the accumulation of recessive mutants within a population giving rise to relatively rapid evolutionary events when they reached a critical level of representation to produce a high number of homozygote individuals who could preferentially mate and produce a new lineage or allow the exploitation of different ecological relationships.
The molecular and developmental evolutionary models are non-Darwinian in the sense that they do not assume natural selection as the predominant mechanism for the spread of evolutionary novelty and adaptation. By providing an alternative biological context for evolution, the models are Darwinian in the sense that they develop Darwin’s laws of growth in the context of molecular genetics and development. These models demonstrate a genetic and developmental foundation for earlier non-Darwinian orthogenetic models of evolution, and they call into question the widespread assumption that there is a functional purpose for adaptations that is the reason for their existence, or that imaginary selection pressures or advantages necessarily have anything to do with evolutionary novelty. Once selection is no longer necessary for the spread of novel mutations, the evolutionary questions shift to the origin of the mutation itself. Is the origin of any given mutation contingent in some way with preceding mutations? It is this consequence of the structural constraints inherent in each type of organization that is implicit in orthogenetic models and that remains to be explored by evolutionary biologists.
A biologically based model for the evolutionary spread of novelty reverses current models for interpreting the evolution of humans and human ancestors. For example, the evolution of bipedalism may be the result of a shifting relationship between regulatory and structural genes producing a skeletal and musculature structure that resulted in the evolution of obligate bipedalism, whether or not the ancestor was arboreal or terrestrial and whether or not these ancestors liked it. As an ecological consequence, the bipedal mode of locomotion may have decreased exposure to radiation that allowed, in turn, for ancestral hominids to survive in open habitats. Hair loss may be necessary for effective survival of a biped in open situations through greater cooling, but it is the loss of hair that made this possible in the first place rather than the need to lose hair. Increased intelligence may have afforded hominids greater opportunities for survival, again as a consequence of changes in brain evolution, not as a cause of that evolution. The benefit is the result, not the origin, of evolution.
Even with molecular and developmental evidence suggesting a biological foundation for evolution without natural selection, it is highly unlikely that these models will gain much popularity among historical evolutionists in anthropology and paleontology. The temptation to continue to construct imaginary narratives assigning purpose to the meaning of life through untestable notions of historical selection pressures and advantages will be a temptation too hard to resist.
- Croizat, L. (1958). Panbiogeography. Caracas, Venezuela: Author.
- Croizat, L. (1964). Space, time, form: The biological synthesis. Caracas, Venezuela: Author.
- Dover, G. A. (2000). Dear Mr. Darwin. Berkeley: University of California Press.
- Schwartz, J. H. (1999). Sudden origins. New York: Wiley.