Contingency and determinism in evolution: Replaying life’s tape
The evolutionary biologist Stephen Jay Gould once dreamed about replaying the tape of life in order to identify whether evolution is more subject to deterministic or contingent forces. Greater influence of determinism would mean that outcomes are more repeatable and less subject to variations of his...
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| Published in | Science (American Association for the Advancement of Science) Vol. 362; no. 6415 |
|---|---|
| Main Authors | , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
09.11.2018
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| Subjects | |
| Online Access | Get full text |
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| Abstract | The evolutionary biologist Stephen Jay Gould once dreamed about replaying the tape of life in order to identify whether evolution is more subject to deterministic or contingent forces. Greater influence of determinism would mean that outcomes are more repeatable and less subject to variations of history. Contingency, on the other hand, suggests that outcomes are contingent on specific events, making them less repeatable. Blount
et al.
review the numerous studies that have been done since Gould put forward this question, both experimental and observational, and find that many patterns of adaptation are convergent. Nevertheless, there is still much variation with regard to the mechanisms and forms that converge.
Science
, this issue p.
eaam5979
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. |
|---|---|
| AbstractList | The evolutionary biologist Stephen Jay Gould once dreamed about replaying the tape of life in order to identify whether evolution is more subject to deterministic or contingent forces. Greater influence of determinism would mean that outcomes are more repeatable and less subject to variations of history. Contingency, on the other hand, suggests that outcomes are contingent on specific events, making them less repeatable. Blount
et al.
review the numerous studies that have been done since Gould put forward this question, both experimental and observational, and find that many patterns of adaptation are convergent. Nevertheless, there is still much variation with regard to the mechanisms and forms that converge.
Science
, this issue p.
eaam5979
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. 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. 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.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. Replaying the tape of lifeThe evolutionary biologist Stephen Jay Gould once dreamed about replaying the tape of life in order to identify whether evolution is more subject to deterministic or contingent forces. Greater influence of determinism would mean that outcomes are more repeatable and less subject to variations of history. Contingency, on the other hand, suggests that outcomes are contingent on specific events, making them less repeatable. Blount et al. review the numerous studies that have been done since Gould put forward this question, both experimental and observational, and find that many patterns of adaptation are convergent. Nevertheless, there is still much variation with regard to the mechanisms and forms that converge.Science, this issue p. eaam5979BACKGROUNDEvolution is a strongly historical process, and evolutionary biology is a field that combines history and science. How the historical nature of evolution affects the predictability of evolutionary outcomes has long been a major question in the field. The power of natural selection to find the limited set of high-fitness solutions to the challenges imposed by environments could, in principle, make those outcomes deterministic. However, the outcomes also may depend on idiosyncratic events that an evolving lineage experiences—such as the order of appearance of random mutations or rare environmental perturbations—making evolutionary outcomes unrepeatable. This sensitivity of outcomes to the details of history is called “historical contingency,” which Stephen Jay Gould argued was an essential feature of evolution. Gould illustrated this view by proposing the thought experiment of replaying life’s tape to see if the living world that we know would re-evolve. But, Gould wrote, “The bad news is that we can’t possibly perform the experiment.”Gould’s pessimistic assessment notwithstanding, experimental evolutionary biologists have now performed many replay experiments, albeit on a small scale, while comparative biologists are analyzing evolutionary outcomes in nature as though they were natural replay experiments. These studies provide new examples and insights into the interplay of historical contingency and natural selection that sits at the heart of evolution.ADVANCESBiologists have devised a variety of approaches to study the effects of history on the repeatability of evolutionary outcomes. On the experimental side, several designs have been employed, mostly using microbes, including “parallel replay experiments,” in which initially identical populations are followed as they evolve in identical environments, and “historical difference experiments,” in which previously diverged populations evolve under identical conditions (see the figure). Our review of many such experiments indicates that responses across replicate populations are often repeatable to some degree, although divergence increases as analyses move from overall fitness to underlying phenotypes and genetic changes. It is common for replicates with similar fitness under the conditions in which they evolved to vary more in their performance in other environments. Idiosyncratic outcomes also occur. For example, aerobic growth on citrate has evolved only once among 12 populations in an experiment with Escherichia coli, even after more than 65,000 generations. In that case, additional replays showed that the trait’s evolution was dependent on the prior occurrence of particular mutations.Meanwhile, comparative biologists have cataloged many notable examples of convergent evolution among species living in similar environments, illustrating the power of natural selection to produce similar phenotypic outcomes despite different evolutionary histories. Nonetheless, convergence is not inevitable—in many cases, lineages adapt phenotypically in different ways to the same environmental conditions. For example, the aye-aye (a lemur) and woodpeckers have evolved different morphological adaptations to similar ecological niches (see the figure). An emerging theme from comparative studies, tentatively supported by replay experiments, is that repeatability is common when the founding populations are closely related, perhaps resulting from shared genetics and developmental pathways, whereas different outcomes become more likely as historical divergences become greater.OUTLOOKGould would be pleased that his thought experiment of replaying life’s tape has been transformed into an empirical research program that explores the roles of historical contingency and natural selection at multiple levels. However, his view of historical influences as the central feature of evolution remains debatable. Laboratory replay experiments show that repeatable outcomes are common, at least when defined broadly (e.g., at the level of genes, not mutations). Moreover, convergence in nature is more common than many biologists would have wagered not long ago. On the other hand, as evolving lineages accumulate more differences, both experimental and comparative approaches suggest that the power of selection to drive convergence is reduced, and the contingent effects of history are amplified. Recognizing the joint contributions of contingency and natural selection raises interesting questions for further study, such as how the extent of prior genetic divergence affects the propensity for later convergence. Theory and experiments indicate that the “adaptive landscape”—that is, how specific phenotypes, and ultimately fitness, map onto the high dimensionality of genotypic space—plays a key role in these outcomes. Thus, a better understanding of these mappings will be important for a deeper appreciation of how fate and chance intertwine in the evolutionary pageant.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. |
| Author | Lenski, Richard E. Losos, Jonathan B. Blount, Zachary D. |
| Author_xml | – sequence: 1 givenname: Zachary D. orcidid: 0000-0001-5153-0034 surname: Blount fullname: Blount, Zachary D. organization: Department of Microbiology and Molecular Genetics and BEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, MI 48824, USA., Department of Biology, Kenyon College, Gambier, OH 43022, USA – sequence: 2 givenname: Richard E. orcidid: 0000-0002-1064-8375 surname: Lenski fullname: Lenski, Richard E. organization: Department of Microbiology and Molecular Genetics and BEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, MI 48824, USA – sequence: 3 givenname: Jonathan B. orcidid: 0000-0003-4712-8258 surname: Losos fullname: Losos, Jonathan B. organization: Department of Biology, Washington University, St. Louis, MO 63130, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30409860$$D View this record in MEDLINE/PubMed |
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| Snippet | The evolutionary biologist Stephen Jay Gould once dreamed about replaying the tape of life in order to identify whether evolution is more subject to... Historical processes display some degree of "contingency," meaning their outcomes are sensitive to seemingly inconsequential events that can fundamentally... Replaying the tape of lifeThe evolutionary biologist Stephen Jay Gould once dreamed about replaying the tape of life in order to identify whether evolution is... |
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| Title | Contingency and determinism in evolution: Replaying life’s tape |
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