Many evolutionary biologists are engaged in research that focuses on large organisms that are (presumably) adapting to a local environment. These "field biologists" are mostly concerned with rapid evolutionary changes. Those kind of changes are almost always due to natural selection. Many of these biologists are not interested in molecular evolution and not interested in any process other than natural selection.Unfortunately, this promotes an adaptationist mentality where all of evolution is viewed through the filter of natural selection. This is the view criticized by Stephen Jay Gould and Richard Lewontin back in 1978 when they presented the Spandrels paper at a Royal Society meeting in London (UK).
Gould, S. J. and Lewontin, R.C. (1979) The Spandrels of San Marco and the Panglossian Paradigm: A Critique of the Adaptationist Programme. Proc. R. Soc. Lond. B 205:581-598. [doi: 10.1098/rspb.1979.0086I believe there was a substantive change in our view of evolution back in the late 1960s and early 1970s. That's when the results of evolution at the molecular level were first being published. It lead to the development of Neutral Theory, Nearly-Neutral Theory and a growing appreciation of the importance of random genetic drift. Modern population genetics was able to cope easily with this new view of evolution.
It seems to me that most evolutionary biologists missed the revolution. That's why they're stuck with a 1950s view of evolution—one that only recognizes natural selection as a mechanism that changes allele frequencies in a population. That was the dominant perspective at the most recent Royal Society meeting in London a few weeks ago. Ironically, the participants were advocating the overthrow of the Modern Synthesis (1950s version) but they did not want to overthrow the view that adapationism is the only perspective. In fact, most of the changes they proposed were hyper-adaptationist.
Nothing in biology makes sense except in the light of population genetics.
It's been almost half-a-century since this new perspective on evolutionary theory was proposed. Many evolutionary biologists now know that deleterious alleles can be fixed in a population by random genetic drift. They know that natural selection isn't all-powerful; in fact, most beneficial alleles are lost before they ever become fixed. They know
The overwhelming emphasis on natural selection in the media, and even in the scientific literature, has stalled the revolution and led to a situation where the vast majority of scientists have a flawed view of evolution. We see this in the universities where our students are often taught evolution by the very scientists I described in the opening paragraph. I'm particularly sensitive to this because I'm getting ready for my course on molecular evolution next semester and I know my most important task will be to correct the misconceptions of my students.
Michael Lynch has been trying to educate his fellow scientists, and the rest of the world, for the past few decades. His latest attempt is a paper in last month's edition of Nature Reviews: Genetics where he promotes the Drift-Barrier Hypothesis. He does this in the context of understanding mutation rates but the idea is generally applicable to all examples of evolution.
Lynch, M., Ackerman, M. S., Gout, J.-F., Long, H., Sung, W., Thomas, W. K., and Foster, P. L. (2016) Genetic drift, selection and the evolution of the mutation rate. Nature Reviews Genetics, 17:704-714. doi: 10.1038/nrg.2016.104Let's look at Michael Lynch's view of evolution. This won't be new to most readers of Sandwalk but maybe it will stimulate some of you to reconsider your old-fashioned, adaptationist, view of evolution.
As one of the few cellular traits that can be quantified across the tree of life, DNA-replication fidelity provides an excellent platform for understanding fundamental evolutionary processes. Furthermore, because mutation is the ultimate source of all genetic variation, clarifying why mutation rates vary is crucial for understanding all areas of biology. A potentially revealing hypothesis for mutation-rate evolution is that natural selection primarily operates to improve replication fidelity, with the ultimate limits to what can be achieved set by the power of random genetic drift. This drift-barrier hypothesis is consistent with comparative measures of mutation rates, provides a simple explanation for the existence of error-prone polymerases and yields a formal counter-argument to the view that selection fine-tunes gene-specific mutation rates.
The question we're considering is: Why doesn't natural selection reduce the mutation rate to zero?. It seems reasonable to imagine that since some mutations are harmful, evolution should select for populations with the lowest possible mutation rate. The standard answer to the question is to imagine there are physical constraints on the accuracy of DNA replication preventing the evolution of a perfect DNA polymerase. This explanation doesn't hold up to close scrutiny as I pointed out in my earlier blog post.
Furthermore, the overall mutation rate—expressed as the number of mutations per generation—depends not only on the accuracy of DNA replication (and repair) but also on additional features such as the number of cell divisions required for formation of the germ cells. In humans, for example, the mutation rate could be substantially reduced by reducing the number of sperm cells made in males. Why hasn't that happened?
The answer depends on understanding the relationship between natural selection and random genetic drift. The two processes compete with each other and the winner is influenced by the size of the population. In small populations, a beneficial mutation can easily be lost by drift before it becomes established in a population. In larger populations, on the other hand, it's harder to lose the beneficial mutation by accident so eventually selection will win out and the beneficial allele becomes fixed by natural selection.
This is the essence of the drift-barrier hypothesis described in Lynch's latest paper by using a very nice figure.
The figure shows the probability of achieving adaptation (trait performance) as a function of the size of the population. Improvements by natural selection are impeded by downward pressure due to the stochastic effects of random genetic drift (blue arrows). This is very effective in small populations. Selection is represented by upward pressure (red arrows) and this is increasingly effective in large populations. However, "perfection" can never be achieved in any reasonable population as the selection coefficient becomes smaller and smaller. This is the drift barrier to adaptation.
The "drift-barrier hypothesis is described in Sung et al. (2012) (see also, Lynch, 2011),
... the drift-barrier hypothesis predicts that the level of refinement of molecular attributes, including DNA replication fidelity and repair, that can be accomplished by natural selection will be negatively correlated with the effective population size (Ne) of a species. Under this hypothesis, as natural selection pushes a trait toward perfection, further improvements are expected to have diminishing fitness advantages. Once the point is reached beyond which the effects of subsequent beneficial mutations are unlikely to be large enough to overcome the power of random genetic drift, adaptive progress is expected to come to a standstill. Because selection is generally expected to favor lower mutation rates as a result of the associated load of deleterious mutations, and because the power of drift is inversely proportional to Ne, lower mutation rates are expected in species with larger Ne.
The consequences are modeled in simulations of mutation rate evolution (below). When the initial mutation rate is high (red, black) there will be a decrease in the mutation rate until a point is reached where improvements are impeded by the drift barrier. When the initial mutation rate is low (blue) the rate will increase because the deleterious effects of increasing the number of mutations are below the threshold imposed by the pressure of drift. The result is a steady-state mutation rate that is far from perfection.
The important point here is not the evolution of mutation rates. It's the idea that drift and selection are both operating in natural populations and you can't understand one without taking into account the other. This is a point that needs to be publicized. We need to get out the message that's there's more to evolution that just natural selection. We need to convince science writers that modern population genetics provides a much better explanation of biological phenomena than just blind allegiance to the old-fashioned Modern Synthesis of Ernst Mayr and his colleagues.
Here's what you need to know in order to understand modern evolutionary theory. The first quotation is from the preface to The Origins of Genome Architecture (pages xiii-xiv). The second quotations are from the last chapter (page 366 and pages 368-369).
Contrary to popular belief, evolution is not driven by natural selection alone. Many aspects of evolutionary change are indeed facilitated by natural selection, but all populations are influenced by nonadaptive forces of mutation, recombination, and random genetic drift. These additional forces are not simple embellishments around a primary axis of selection, but are quite the opposite—they dictate what natural selection can and cannot do. Although this basic principle has been known for a long time, it is quite remarkable that most biologists continue to interpret nearly aspect of biodiversity as an outcome of adaptive processes. This blind acceptance of natural selection as the only force relevant to evolution has led to a lot of sloppy thinking, and is probably the primary reason why evolution is viewed as a soft science by much of society.
A central point to be explained in this book is that most aspects of evolution at the genome level cannot be fully explained in adaptive terms, and moreover, that many features could not have emerged without a near-complete disengagement of the power of natural selection. This contention is supported by a wide array of comparative data, as well as by well-established principles of population genetics. However, even if such support did not exist, there is an important reason for pursuing nonadaptive (neutral) models of evolution. If one wants to confidently invoke a specific adaptive scenario to explain an observed pattern of comparative data, then an ability to reject a hypothesis based entirely on the nonadaptive forces of evolution is critical.
The blind worship of natural selection is not evolutionary biology. It is arguably not even science.
Despite the tremendous theoretical and physical resources now available, the field of evolutionary biology continues to be widely perceived as a soft science. Here I am referring not to the problems associated with those pushing the view that life was created by an intelligent designer, but to a more significant internal issue: a subset of academics who consider themselves strong advocates of evolution but who see no compelling reason to probe the substantial knowledge base of the field. Although this is a heavy charge, it is easy to document. For example, in his 2001 presidential address to the Society for the Study of Evolution, Nick Barton presented a survey that demonstrated that about half of the recent literature devoted to evolutionary issues is far removed from mainstream evolutionary biology.
With the possible exception of behavior, evolutionary biology is treated unlike any other science. Philosophers, sociologists, and ethicists expound on the central role of evolutionary theory in understanding our place in the world. Physicists excited about biocomplexity and computer scientists enamored with genetic algorithms promise a bold new understanding of evolution, and similar claims are made in the emerging field of evolutionary psychology (and its derivatives in political science, economics, and even the humanities). Numerous popularizers of evolution, some with careers focused on defending the teaching of evolution in public schools, are entirely satisfied that a blind adherence to the Darwinian concept of natural selection is a license for such activities. A commonality among all these groups is the near-absence of an appreciation of the most fundamental principles of evolution. Unfortunately, this list extends deep within the life sciences.
... the uncritical acceptance of natural selection as an explanatory force for all aspects of biodiversity (without any direct evidence) is not much different than invoking an intelligent designer (without any direct evidence). True, we have actually seen natural selection in action in a number of well-documented cases of phenotypic evolution (Endler 1986; Kingsolver et al. 2001), but it is a leap to assume that selection accounts for all evolutionary change, particularly at the molecular and cellular levels. The blind worship of natural selection is not evolutionary biology. It is arguably not even science. Natural selection is just one of several evolutionary mechanisms, and the failure to realize this is probably the most significant impediment to a fruitful integration of evolutionary theory with molecular, cellular, and developmental biology.
Natural selection is just one of several evolutionary mechanisms, and the failure to realize this is probably the most significant impediment to a fruitful integration of evolutionary theory with molecular, cellular, and developmental biology.It should be emphasized here that the sins of panselectionism are by no means restricted to developmental biology, but simply follow the tradition embraced by many areas of evolutionary biology itself, including paleontology and evolutionary ecology (as cogently articulated by Gould and Lewontin in 1979). The vast majority of evolutionary biologists studying morphological, physiological, and or behavioral traits almost always interpret the results in terms of adaptive mechanisms, and they are so convinced of the validity of this approach that virtually no attention is given to the null hypothesis of neutral evolution, despite the availability of methods to do so (Lande 1976; Lynch and Hill 1986; Lynch 1994). For example, in a substantial series of books addressed to the general public, Dawkins (e,g., 1976, 1986, 1996, 2004) has deftly explained a bewildering array of observations in terms of hypothetical selection scenarios. Dawkins's effort to spread the gospel of the awesome power of natural selection has been quite successful, but it has come at the expense of reference to any other mechanisms, and because more people have probably read Dawkins than Darwin, his words have in some ways been profoundly misleading. To his credit, Gould, who is also widely read by the general public, frequently railed against adaptive storytelling, but it can be difficult to understand what alternative mechanisms of evolution Gould had in mind.
Lynch, M. (2011) The lower bound to the evolution of mutation rates. Genome Biology and Evolution, 3:1107. [doi: 10.1093/gbe/evr066]
Sung, W., Ackerman, M.S., Miller, S.F., Doak, T.G., and Lynch, M. (2012) Drift-barrier hypothesis and mutation-rate evolution. Proc. Natl. Acad. Sci. (USA) 109:18488-18492. [doi: 10.1073/pnas.1216223109]