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PNAS Paper Admits Understanding the Origin of Cellular Features Is a "Glaring Gap" in Evolutionary Biology

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In 2001, biochemist Franklin Harold wrote in an Oxford University Press monograph that "there are presently no detailed Darwinian accounts of the evolution of any biochemical or cellular system, only a variety of wishful speculations." Last month, a new paper in Proceedings of the National Academy of Sciences, "Evolutionary cell biology: Two origins, one objective," admitted much the same thing. The article states (emphasis added):

All aspects of biological diversification ultimately trace to evolutionary modifications at the cellular level. This central role of cells frames the basic questions as to how cells work and how cells come to be the way they are. Although these two lines of inquiry lie respectively within the traditional provenance of cell biology and evolutionary biology, a comprehensive synthesis of evolutionary and cell-biological thinking is lacking. ... Because all evolutionary change ultimately requires modifications at the cellular level, questioning and understanding how cellular features arise and diversify should be a central research venue in evolutionary biology. However, if there is one glaring gap in this field, it is the absence of widespread cell-biological thinking. Despite the surge of interest at the molecular, genomic, and developmental levels, much of today's study of evolution is only moderately concerned with cellular features, perhaps due to lack of appreciation for their wide variation among taxa. However, a full mechanistic understanding of evolutionary processes will never be achieved without an elucidation of how cellular features become established and modified.
Co-authored by some leading evolutionary biologists who are also critics of the standard neo-Darwinian paradigm, the article suggests that evolutionary and cellular biologists need to focus on "bridging the gap" between their two fields. However, though the authors aren't necessarily neo-Darwinians, they retain the evolutionary materialist view that biological processes produce clumsy features, evidence of an absence of design. They want to understand how "historical contingency" and the "opportunistic process of 'descent with modification'" have produced living systems. Thus, they take an efficient molecular machine like the ATP synthase and consider the possibility that it's a poor solution to the problem of generating ATP:
One remarkable example of how history continues to influence today's cell biology is the near universal use of ATP synthase as a mechanism for energy generation. Embedded in the surface membranes of bacteria and organellar membranes of eukaryotes, this complex molecular machine uses the potential energy of a proton gradient to generate a rotational force that converts ADP to ATP, much like a turbine converts the potential energy of a water gradient into electricity. However, the proton gradient does not come for free: cells first use energy derived from metabolism to pump protons out of membrane-bound compartments, creating the gradient necessary for reentry through ATP synthase. Even assuming that ATP production is an essential requirement for the origin of life, it is by no means clear that the path chosen for ADP-to-ATP conversion is the only possibility.
However, they acknowledge that selection can't explain everything:
A commonly held but incorrect stance is that essentially all of evolution is a simple consequence of natural selection. Leaving no room for doubt on the process, this narrow view leaves the impression that the only unknowns in evolutionary biology are the identities of the selective agents operating on specific traits. However, population-genetic models make clear that the power of natural selection to promote beneficial mutations and to remove deleterious mutations is strongly influenced by other factors. Most notable among these factors is random genetic drift, which imposes noise in the evolutionary process owing to the finite numbers of individuals and chromosome architecture.
Where selection fails, they propose forces like neutral drift. Yet as I explained here, under random genetic drift, features arise entirely due to random factors. At least natural selection offers some explanation as to how beneficial features are preserved. If selection has trouble building complex features, random drift would seem even more inadequate. Thus, incredibly, the paper argues that complex molecular machines evolved despite the fact that they may not have yielded a benefit:
Certainly, today's cells cannot survive without such molecular machines. However, the existence of complex cellular features need not imply that each of the myriad of changes that sculpted such structures over evolutionary time was adaptive at the time of establishment.
It seems doubtful that we can explain the origin of some of life's most complex, fundamental, and efficient machine-like features by appealing to random factors like random genetic drift, random recombination, and random mutation. This is hardly different from saying that molecular machines arose for no reason at all.

Be that as it may, their admission that explaining the origin of cellular features is a "glaring gap" shows that this remains a major problem for evolutionary thinking, whether under an adaptationist or a neutralist model. Though they don't put it quite as bluntly as Franklin Harold, this paper's message is no less potent: modern evolutionary biology lacks explanations for the origin of molecular machines.

Photo source: gmacfadyen/Flickr.