Most biological students think that adaptive radiations and Darwinism go together, and that the mechanisms of genetic mutation and natural selection explain all the data. However, in most cases, this explanation is assumed and not supported by evidence. It is assumed because of the dominance of neodarwinism in evolutionary biology and because students are very impressed with the "mountains of evidence" claimed to support the consensus. Happily, there are some biologists prepared to step outside the paradigm, and one of them is Austin Hughes from the University of South Carolina. In preparing the ground for his iconoclastic analysis, he writes:
"I will refer to this mechanism as the Neo-Darwinian mechanism; and, following general usage, I will refer to an allele that has been fixed by this process as one that has been fixed by positive Darwinian selection. The Neo-Darwinian mechanism is often assumed by biologists to be the only source of adaptive traits of organisms, to the point where 'adaptive evolution' and 'positive (Darwinian) selection' are treated as interchangeable terms in the literature."
Also, by way of preparation, he refers to the significant theoretical and evidential base for neutral evolution (Kimura, 1976). There is a phenomenon known as genetic drift involving neutral or nearly neutral mutations. There are mechanisms for fixing these genetic changes - all invisible to natural selection. These are considered to be more important than we realise, evidenced by the continuing scarcity of advantageous mutations. This was recognised in 1976 and it continues to this day.
"In the ensuing decades, a vast amount of molecular sequence data, including complete genome sequences of many organisms, has become available to test for the evidence of positive selection at the molecular level. However, the number of well-established cases has not increased greatly in comparison with those known in the mid-1970s. It is true that a very large number of papers have been published in recent years purporting to show evidence of positive selection on the basis of various statistical methods. However, the vast majority of these cases cannot be considered well established. [. . .] Moreover, in almost all of the putative cases of positive selection identified by statistical analysis of sequence data alone, the biological basis of the supposed selection and even the phenotypic effects, if any, of the supposedly selected nucleotide substitutions have not been addressed."
Hughes has previously pointed out difficulties in identifying evidence for positive selection, yet there appears to be plenty of evidence for purifying selection (the elimination of deleterious variants).
"The predominance of purifying selection was predicted by Kimura and Ohta (1974), and the fact that their prediction has been proved to be correct is the cornerstone of many routine methods of modern bioinformatics, whereby evolutionary conservation of a sequence element (the consequence of purifying selection) is taken as evidence of that element's functional importance."
So, in view of the meagre evidential support for "the Neo-Darwinian mechanism", Hughes turns his attention to the thought that adaptive phenotypes might arise by alternative routes. This has been considered by a few other authors, but the field is wide open. Consequently, Hughes proposes one such mechanism: the plasticity - relaxation - mutation (PRM) mechanism. He argues that the evidential base for this concept is already in existence in the biological literature.
"I examine some predictions of this theory and summarize evidence relating to those predictions. The present hypothesis does not deny that the Neo-Darwinian mechanism operates in certain cases. Rather, based on what we can learn from the known cases of positive selection, I conclude that the phenomenon of positive selection may be of relatively minor importance in phenotypic evolution. Instead, phenotypic plasticity and changes in the direction and nature of purifying selection, combined with the chance fixation of neutral or nearly neutral mutations, are proposed to be the major factors in the evolution of adaptive phenotypes."
Much of the paper provides clarification of the PRM mechanism and justifies the claim that the concept has a track record in the literature. The emerging scenario is that organisms typically have an ability to adapt to environmental inputs in ways that change and fix the phenotype. This is a variability that does not depend on mutations for new genetic information, although mutations may be involved in the fixing of the phenotype. The genomic architecture is already present that supports adaptation in a variety of directions. Influences may come from neutral mutations and genetic drift, and they may involve epigenetic mechanisms. After reviewing a variety of evidences, Hughes concludes:
"The PRM mechanism provides unification to the biological sciences by uniting observations at the genomic level (where purifying selection and genetic drift predominate) with those at the phenotypic level (where adaptive characters are well known). As mentioned above, some known examples are suggestive of the action of the PRM mechanism, but it is not yet known how widespread this mechanism is. However, I would predict that the PRM mechanism is likely to be a major mechanism for the origin of evolved adaptations, and perhaps more common than the Neo-Darwinian mechanism."
Let's look at some of the applications of the PRM concept.
First, a comment on the general picture. Adaptive radiations in the fossil record appear to have been rapid, followed by stasis. This pattern is quite unlike the branching illustration found in On the Origin of Species.
"In some cases, the time frame seems rather short for a Darwinian process to have occurred, and in other cases, the effective population sizes of the species in question are small, suggesting that there is unlikely to have been extensive genetic variation in the population prior to selection. However, none of these factors are problematic if these cases of apparent rapid evolution in fact represent cases of phenotypic plasticity, perhaps in some cases rendered heritable through germline DNA methylation. Thus, rather than the paradoxical observation of Darwinian evolution over ecological time, we may be merely seeing incipient evolution by the PRM mechanism, which is expected to operate over ecological time."
Second, the specific case of cichlid fishes is of interest, because these radiations do not have the luxury of extensive time.
"The PRM mechanism provides a simple explanation of such comparatively recent adaptive radiations as that of the cichlids of the East African Great Lakes. The oldest of these lakes, Lake Victoria, is no more than 200,000 years old, and others are still more recent. The diversity of species in these lakes is problematic for Neo-Darwinism, but is easily explained by the PRM mechanism if prior to the divergence of ecotypes the ancestral species showed a phenotypic plasticity similar to that described in sticklebacks."
Third, consider that classic example of adaptive radiation: the Galapagos finches.
"Perhaps ironically, the PRM mechanism can likewise account readily for the radiation of Darwin's finches in the Galapagos Islands. The natural history of Darwin's finches provides many examples where it is plausible that phenotypic plasticity preceded morphological change; a striking example involves the sharper bill shape of a population of the ground finch Geospiza diffilis that feeds on the blood of boobies."
Fourth, the topic of artificial selection is of interest - not least because Darwin (and modern textbooks) portrayed artificial selection as directly relevant to natural selection, whereas Wallace thought it was irrelevant. There is no doubt that artificial selection produces rapid phenotypic change, but we already know that most of this does not involve mutations.
"The same process [incipient evolution by the PRM mechanism] might also be involved in rapid responses to artificial selection, for instance in accelerated domestication."
The significance of this research for the study of biological variation surely deserves our attention. We are not here considering a theory that claims to explain the concept of common descent from a single cell, but it has the more modest aim of explaining adaptive radiations from ancestral populations. However, the main critique that has been advanced is that the PRM hypothesis "does not explain why the ancestral state should be phenotypically plastic, or why this plasticity should be adaptive in the first place." The critique is not a fair one, because the new theory is proposed to explain observations of biological variation, rather than to explain the origin of all species.
The perspective provided by Hughes is one that is based on both theory and empirical data, and it stands up to testing very well. This model of variation provides an understanding that differs markedly from the Darwinism and the Neo-Darwinism of most textbooks. It is time for evolutionists to cease claiming all examples of variation and adaptation as evidence for Darwinian mechanisms of evolution. This is bad science and it is the perpetuation of a consensus by repetition rather than by hypothesis testing and validation. Hughes concludes thus:
"The hypothesis proposed here has the advantage of explaining the available data regarding adaptive evolution on the levels of genomics, ecology and paleontology, without invoking any mechanisms other than the commonly observed phenomena of phenotypic plasticity, purifying selection, mutation and genetic drift. Although it may represent a new perspective to biologists schooled in Neo-Darwinism, this view of life in its own way is not without 'a certain grandeur.'"
Evolution of adaptive phenotypic traits without positive Darwinian selection
A L Hughes
Heredity, advance online publication 2 November 2011 | doi: 10.1038/hdy.2011.97
Recent evidence suggests the frequent occurrence of a simple non-Darwinian (but non-Lamarckian) model for the evolution of adaptive phenotypic traits, here entitled the plasticity-relaxation-mutation (PRM) mechanism. This mechanism involves ancestral phenotypic plasticity followed by specialization in one alternative environment and thus the permanent expression of one alternative phenotype. Once this specialization occurs, purifying selection on the molecular basis of other phenotypes is relaxed. Finally, mutations that permanently eliminate the pathways leading to alternative phenotypes can be fixed by genetic drift. Although the generality of the PRM mechanism is at present unknown, I discuss evidence for its widespread occurrence, including the prevalence of exaptations in evolution, evidence that phenotypic plasticity has preceded adaptation in a number of taxa and evidence that adaptive traits have resulted from loss of alternative developmental pathways. The PRM mechanism can easily explain cases of explosive adaptive radiation, as well as recently reported cases of apparent adaptive evolution over ecological time.
Levi, P.J. No Positive Selection, No Darwin: A New Non-Darwinian Mechanism for the Origin of Adaptive Phenotypes, Evolution News & Views (November 14, 2011)
Tyler, D. Rodents evolve - but does the evidence suggest phenotypic plasticity? ARN Literature Blog (18 November 2011)
Tyler, D. A call for an end to Pseudo-Darwinian hype, ARN Literature Blog (11 September 2008)
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