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Contingency, selection, and the long-term evolution experiment

I'm a big fan of Richard Lenski's long-term Evolution experiment (LTEE) and of Zachary Blount's work in particular. [Strolling around slopes and valleys in the adaptive landscape] [On the unpredictability of evolution and potentiation in Lenski's long-term evolution experiment] [Lenski's long-term evolution experiment: the evolution of bacteria that can use citrate as a carbon source]

The results of the LTEE raise some interesting questions about evolution. The Lenski experiment began with 12 (almost) identical cultures and these have now "evolved" for 31 years and more than 65,000 generations. All of the cultures have diverged to some extent and one of them (and only one) has developed the ability to use citrate as a carbon source. Many of the cultures exhibit identical, or very similar, mutations that have reached significant frequencies, or even fixation, in the cultures.

Several other laboratory evolution experiments have been completed or are underway in various labs around the world. The overall results are relevant to a discussion about the role of contingency and accident in the history of life [see Evolution by Accident]. Is it true that if you replay the tape of life the results will be quite different? [Replaying life's tape].

Blount and Lenski have discussed this issue several times in the past (Yedid et al., 2008; Blount et al., 2008; Blount, 2016; Lenski, 2017). Last Fall they teamed up with Jonathan Losos to review the latest results. The paper was published in Science.
Blount, Z.D., Lenski, R.E., and Losos, J.B. (2018) Contingency and determinism in evolution: replaying life’s tape. Science, 362:655, eaam5979 1-10. [doi: 10.1126/science.aam597]

Abstract: Historical processes display some degree of “contingency,” meaning their outcomes are sensitive to seemingly inconsequential events that can fundamentally change the future. Contingency is what makes historical outcomes unpredictable. Unlike many other natural phenomena, evolution is a historical process. Evolutionary change is often driven by the deterministic force of natural selection, but natural selection works upon variation that arises unpredictably through time by random mutation, and even beneficial mutations can be lost by chance through genetic drift. Moreover, evolution has taken place within a planetary environment with a particular history of its own. This tension between determinism and contingency makes evolutionary biology a kind of hybrid between science and history. While philosophers of science examine the nuances of contingency, biologists have performed many empirical studies of evolutionary repeatability and contingency. Here, we review the experimental and comparative evidence from these studies. Replicate populations in evolutionary “replay” experiments often show parallel changes, especially in overall performance, although idiosyncratic outcomes show that the particulars of a lineage’s history can affect which of several evolutionary paths is taken. Comparative biologists have found many notable examples of convergent adaptation to similar conditions, but quantification of how frequently such convergence occurs is difficult. On balance, the evidence indicates that evolution tends to be surprisingly repeatable among closely related lineages, but disparate outcomes become more likely as the footprint of history grows deeper. Ongoing research on the structure of adaptive landscapes is providing additional insight into the interplay of fate and chance in the evolutionary process.
The conclusion is consistent with earlier results: similar isolated populations/species tend to find similar solutions when put under pressure to adapt but over the long term the populations diverge considerably due to stochastic effects.

It's not the paper's conclusion that I want to highlight. I want to call attention to the style of the paper and the quality of the writing. The authors define a serious problem (contingency vs determinism); they present the historical background and put it in a modern context; they review the data; and they discuss various problems and issues of interpretation. Throughout the paper they take the time to present both sides of the issue and cover all the objections that make this such a controversial issue.

In an ideal world this paper would not merit particular attention because this is the way all literature reviews should be written. In an ideal world all scientific papers would be excellent examples of critical thinking. However, this is not an ideal world and that's why this paper is unusual. Read this paper if you want to see a model for how all papers should be written.

There are a couple of points in the paper that deserve special mention ....

The meaning of "contingency"

When discussing the history of life, the word contingency usually means that the path of evolution is shaped by all of the events that occurred earlier. Stephen Jay Gould made the word popular in his book Wonderful Life, which was all about contingency in that sense. Here's what he said on page 283 ...
I am not speaking of randomness ... but of the central principle of all history—contingency. A historical explanation does not rest on direct deductions from laws of nature, but on an unpredictable sequence of antecedent states, where any major change in any step of the sequence would have altered the final result. This final result is therefore dependent, or contingent, upon everything that came before—the unerasable and determining signature of history.
Unfortunately, Gould did not stick to this definition. He often used the word contingency as a synonym for an unpredictable event. Blount et al. deal with this confusion in their paper by saying ...
Gould also introduced confusion about the concept of contingency itself. Despite its centrality to his thinking, Gould never formally defined "contingency." He gave various informal descriptions, but these tended to be unfulfilling and circular. Moreover, he often conflated the two common meanings of the word "contingency": "dependence on something else" and "an accidental or chance event."

The role of mutation

Here's how Blount et al. explain the relationship between mutation and contingency.
... the stochastic processes of mutation and genetic drift virtually guarantee that different histories will occur even when populations start from the same state and evolve under identical conditions. Such differences, in turn, constitute the sort of unpredictable antecedent events that might preclude populations from evolving the same solutions when confronting the same selective circumstances or, at least, change the relative likelihoods of different outcomes. These effects arise from how mutations and the order in which they occur affect later evolution. Indeed, the particular mutations that occur, their effects, and their fates can alter the rates of occurrence, phenotypic and developmental effects, and fates of later mutations, thereby shifting the probabilities of alternative evolutionary paths.

Convergence

Many biologists have emphasized convergence, where two different species have converged on the same adaptations to a particular environment. We are often so impressed with these examples that we have been lured into thinking that convergence is an important part of the history of life. Indeed, some biologists have explicitly made that point. Simon Conway Morris wrote a book that attempts to refute Gould's thought experiment on replaying the tape of life. Here's what he says on page 202 in The Crucible of Creation ...
Convergence demonstrates that the possible types of organisms are not only limited, but may in fact be severely constrained. The underlying reason for convergence seems to be that all organisms are under constant scrutiny of natural selection and are also subject to the constraints of the physical and chemical factors that severely limit the action of all inhabitants of the biosphere. Put simply, convergence shows that in a real world not all things are possible.
Conway Morris doubled down on this point in subsequent books. For example, in Life's Solution he argues that the numerous examples of convergence imply that contingency has been widely exaggerated and that the history of life is broadly deterministic. Here's how he puts it on page 106 ...
... rewind the tape of life, as S.J. Gould repeatedly claimed, and let it replay: assuredly next time round the world will be a very different place, with a vanishingly small prospect of anything like a human emerging. I have already argued forcibly against such a position, and the purpose of much of the rest of this book is to develop in more detail why the trajectories of evolution are much more severely constrained than is sometimes supposed.1
Blount et al. deal with this argument in an interesting way. They point out that cherry-picking examples of convergence ignores the many other examples where convergence does not occur.
Another difficulty is that convergence is identified after the fact. The saber-toothed condition evolved at least three times in the Carnivora, as well as once each in creodonts and South American marsupials, presumably as an adaptation to a particular predatory strategy. But how many other taxa, faced with the same selective conditions, failed to evolve this adaptation? Knowing the denominator is key to determining how repeatable a convergent trend is, but rarely does one know how many other lineages experienced similar circumstances, yet failed to evolve the trait in question. Moreover, although recent compilations of convergence are impressive, one could just as easily compile lists of adaptive types lacking a convergent doppelgänger: the two-leaved Welwitschia mirabilis, the platypus, chameleons, kiwis, elephants, octopuses, and hominins—all adaptive types that have evolved just once—to name a few.
They also come up with an excellent example of a real-life experiment to test convergence.
Some convergence proponents go so far as to say that if life has evolved on Earth-like exoplanets, it will look much like what we see here. But we need not look to the stars to test that hypothesis: All we need to do is go to New Zealand, an island lacking any native terrestrial mammals. In their absence, New Zealand’s flora and fauna evolved to bear little resemblance to any other ecosystem in the world. In addition to kiwis, there are both carnivorous and flightless parrots, adzebills, moas, giant eagles, and flightless wrens, as well as a semi-terrestrial bat ..., giant snails and orthopterans, and divaricating shrubs with leaves that grow in the interior of the bush. And going back in time, one would be hard-pressed to find many similarities between the Mesozoic world of the dinosaurs and today’s faunas.

In short, lineages adapting to similar environmental conditions in nature can be thought of as evolutionary replays, even if these “natural experiments” are not as precise as carefully designed and controlled laboratory experiments. Because the lineages will have different genetic constitutions and will have experienced different histories, these cases are analogous to the historical difference experiments in laboratory studies. Unfortunately, however, the evidence boils down to one list of cases in which convergence occurred and another where it did not, rendering quantitative conclusions unsatisfactory. Nonetheless, the many impressive cases of convergence show that repeated outcomes can arise from similar environmental challenges. Conversely, the many cases in which convergence did not occur suggest that contingent effects can play a strong role in shaping divergent adaptive responses.
This is the kind of scientific reasoning I admire. It's a shame that there aren't more examples in papers on junk DNA, alternative splicing, and a host of other examples where only one side of the argument is presented.


1. Simon Conway Morris is mostly upset about one of the main implications of evolution by accident; namely, that under different circumstances humans might never have arisen. He believes that God set up evolution so that sentient beings like humans were inevitable.

Blount, Z.D., Borland, C.Z., and Lenski, R.E. (2008) Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proceedings of the National Academy of Sciences, 105(23), 7899-7906. [doi: 10.1073/pnas.0803151105]

Blount, Z. D. (2016) A case study in evolutionary contingency. Studies in History and Philosophy of Science Part C: Studies in History and Philosophy of Biological and Biomedical Sciences. [doi: 10.1016/j.shpsc.2015.12.007]

Lenski, R.E. (2017) Convergence and divergence in a long-term experiment with bacteria. The American Naturalist, 190:S57-S68. [doi: 10.1086/691209]

Yedid, G., Ofria, C., and Lenski, R.E. (2008) Historical and contingent factors affect re‐evolution of a complex feature lost during mass extinction in communities of digital organisms. Journal of evolutionary biology, 21:1335-1357. [doi: 10.1111/j.1420-9101.2008.01564.x]


This post first appeared on Sandwalk, please read the originial post: here

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Contingency, selection, and the long-term evolution experiment

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