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No Positive Selection, No Darwin: A New Non-Darwinian Mechanism for the Origin of Adaptive Phenotypes

Galapagos finch

A new study (Hughes 2011) in the Nature Publishing Group journal Heredity proposes a new non-Darwinian mechanism for the origin of adaptive phenotypes. Its author, Austin L. Hughes of the University of South Carolina, pioneered statistical methods for detecting positive selection at the molecular level with geneticist Masatoshi Nei (Hughes & Nei 1988). He later had the hubris in 2007 to question the majority of inferences to positive selection based on those methods (Hughes 2007). Now he’s proposing a mechanism for adaptive evolution that renders Darwin unnecessary.
If positive selection may be thought of as the promulgator of novelties, purifying selection is the damage control. The latter is an easy affair; selection has only to “nip in the bud” any mutations that render an organism disadvantaged. However, only the former is Darwinian, and it is much more ambitious; positive selection may only act effectively on a mutation that increases the fitness of an organism’s phenotype so as to overwhelm random noise. It must then, through repeated generations of differential survival, succeed in replacing all inferior genotypes with the newcomer. The difficulty of completing this process in a sufficient amount of time, an issue raised by Haldane, was a leading impetus for Kimura’s neutral theory (Kimura 1969, 1983).
It is in the spirit of that question that Hughes now proposes a model he refers to as the plasticity-relaxation-mutation (PRM) model. PRM suggests that adaptive phenotypes arise as follows: (1) there exists a phenotypically plastic trait (i.e., one that changes with the environment, such as sweating in the summer heat); (2) the environment becomes constant, such that the trait assumes only one of its states for a lengthened period of time; and (3) during that time, deleterious mutations accumulate in the unused state of the trait, such that its genetic basis is subsequently lost.
Hughes argues that PRM is a mechanism for whose generality there is “substantial, though generally neglected, evidence.” Moreover, he writes that the number of well-established cases of positive selection has not substantially increased since the 1970s, something that may come as a surprise given the prominence accorded to Darwinian evolution in the biological community. Even oft-cited examples such as Darwin’s finches and antibiotic resistance appear to typically involve no more than phenotypic plasticity and the selection of irreducibly complex traits already in existence. A recent study (D’Costa et al. 2011) demonstrating that resistance to modern antibiotics is present in ancient metagenomic samples should give Darwinists pause.
The PRM suggests that most adaptive traits originate through the loss rather than gain of function. Sound familiar? If true, the hypothesis fits precisely with Michael J. Behe’s first rule of adaptive evolution published last December in Quarterly Review of Biology (Behe 2010): “The results of decades of experimental laboratory evolution studies strongly suggest that, at the molecular level, loss-of-[functional coded elements] and diminishing modification-of-function adaptive mutations predominate.” And though Hughes does not question the importance of Darwinian evolution in some cases (neither did Kimura), he does suggest that the PRM explains the data in a way more consistent with the evidence.
But if most adaptations result from the loss of genetic specifications, how did the traits initially arise? One letter (Chevin & Beckerman 2011) of response to Hughes noted that the PRM “does not explain why the ancestral state should be phenotypically plastic, or why this plasticity should be adaptive in the first place.”
References Cited
Behe MJ (2010) Experimental evolution, loss-of-function mutations, and “the first rule of adaptive evolution.” The Quarterly Review of Biology 85:419-445.
Chevin L-M, Beckerman AP (2011) From adaptation to molecular evolution. Heredity, advance online publication. doi:10.1038/hdy.2011.96
D’Costa VM, et al. (2011) Antibiotic resistance is ancient. Nature 477:457-461.
Hughes AL (2007) Looking for Darwin in all the wrong places: the misguided quest for positive selection at the nucleotide sequence level. Heredity 99:364-373.
Hughes AL (2011) Evolution of adaptive phenotypic traits without positive Darwinian selection. Heredity, advance online publication. doi:10.1038/hdy.2011.97
Hughes AL, Nei M (1988) Pattern of nucleotide substitution at MHC class I loci reveals overdominant selection. Nature 335:167-170.
Kimura M (1968) Evolutionary rate at the molecular level. Nature 217:624-626.
Kimura M (1983) The Neutral Theory of Molecular Evolution. Cambridge University Press.