1. Evolutionary Biology

Contingency and chance erase necessity in the experimental evolution of ancestral proteins

  1. Victoria Cochran Xie
  2. Jinyue Pu  Is a corresponding author
  3. Brian PH Metzger
  4. Joseph W Thornton  Is a corresponding author
  5. Bryan C Dickinson  Is a corresponding author
  1. University of Chicago, United States
https://doi.org/10.7554/eLife.67336
Share this article
Cite this article
  1. Victoria Cochran Xie
  2. Jinyue Pu
  3. Brian PH Metzger
  4. Joseph W Thornton
  5. Bryan C Dickinson
(2021)
Contingency and chance erase necessity in the experimental evolution of ancestral proteins
eLife 10:e67336.
https://doi.org/10.7554/eLife.67336
  2. Download BibTeX
  3. Download .RIS

Abstract

The roles of chance, contingency, and necessity in evolution is unresolved, because they have never been assessed in a single system or on timescales relevant to historical evolution. We combined ancestral protein reconstruction and a new continuous evolution technology to mutate and select B-cell-lymphoma-2-family proteins to acquire protein-protein-interaction specificities that occurred during animal evolution. By replicating evolutionary trajectories from multiple ancestral proteins, we found that contingency generated over long historical timescales steadily erased necessity and overwhelmed chance as the primary cause of acquired sequence variation; trajectories launched from phylogenetically distant proteins yielded virtually no common mutations, even under strong and identical selection pressures. Chance arose because many sets of mutations could alter specificity at any timepoint; contingency arose because historical substitutions changed these sets. Our results suggest that patterns of variation in BCL-2 sequences – and likely other proteins, too – are idiosyncratic products of a particular, unpredictable course of historical events.

Data availability

The high throughput sequencing data of evolved BCL-2 family protein variants were deposited in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) databases. They can be accessed via BioProject: PRJNA647218. The processed sequencing data are available on Dryad (https://doi.org/10.5061/dryad.866t1g1ns). The coding scripts and reference sequences for processing the data are available on Github (https://github.com/JoeThorntonLab/BCL2.ChanceAndContingency).

The following data sets were generated

Article and author information

Author details

  1. Victoria Cochran Xie

    Department of Chemistry, University of Chicago, Chicago, United States
    Competing interests
    No competing interests declared.

  2. Jinyue Pu

    Department of Chemistry, University of Chicago, Chicago, United States
    For correspondence
    pujy@uchicago.edu
    Competing interests
    Jinyue Pu, Has a patent on the proximity-dependent split RNAP technology used in this work (US Patent App. 16/305,298, 2020)..

  3. Brian PH Metzger

    Department of Ecology and Evolutionary Biology, University of Chicago, Chicago, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4878-2913

  4. Joseph W Thornton

    Department of Ecology and Evolution, University of Chicago, Chicago, United States
    For correspondence
    joet1@uchicago.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9589-6994

  5. Bryan C Dickinson

    Department of Chemistry, University of Chicago, Chicago, United States
    For correspondence
    Dickinson@uchicago.edu
    Competing interests
    Bryan C Dickinson, Has a patent on the proximity-dependent split RNAP technology used in this work (US Patent App. 16/305,298, 2020)..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9616-1911

Funding

National Institutes of Health (R01GM131128)

  • Joseph W Thornton

National Institutes of Health (R01GM121931)

  • Joseph W Thornton

National Institutes of Health (R01GM139007)

  • Joseph W Thornton

National Institutes of Health (F32GM122251)

  • Brian PH Metzger

National Science Foundation (DGE-1746045)

  • Victoria Cochran Xie

National Science Foundation (1749364)

  • Bryan C Dickinson

The content is solely the responsibility of the authors and the funders had no input on the study design, analysis, or conclusions.

Copyright

© 2021, Xie et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 7,135
    views
  • 993
    downloads
  • 38
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Victoria Cochran Xie
  2. Jinyue Pu
  3. Brian PH Metzger
  4. Joseph W Thornton
  5. Bryan C Dickinson
(2021)
Contingency and chance erase necessity in the experimental evolution of ancestral proteins
eLife 10:e67336.
https://doi.org/10.7554/eLife.67336

Share this article

https://doi.org/10.7554/eLife.67336

Categories and tags

Research organism

Further reading

    1. Evolutionary Biology

    The population genetics of convergent adaptation in maize and teosinte is not locally restricted

    Silas Tittes, Anne Lorant ... Jeffrey Ross-Ibarra
    Research Article

    What is the genetic architecture of local adaptation and what is the geographic scale over which it operates? We investigated patterns of local and convergent adaptation in five sympatric population pairs of traditionally cultivated maize and its wild relative teosinte (Zea mays subsp. parviglumis). We found that signatures of local adaptation based on the inference of adaptive fixations and selective sweeps are frequently exclusive to individual populations, more so in teosinte compared to maize. However, for both maize and teosinte, selective sweeps are also frequently shared by several populations, and often between subspecies. We were further able to infer that selective sweeps were shared among populations most often via migration, though sharing via standing variation was also common. Our analyses suggest that teosinte has been a continued source of beneficial alleles for maize, even after domestication, and that maize populations have facilitated adaptation in teosinte by moving beneficial alleles across the landscape. Taken together, our results suggest local adaptation in maize and teosinte has an intermediate geographic scale, one that is larger than individual populations but smaller than the species range.

    1. Evolutionary Biology
    2. Neuroscience

    Vision: The inner workings of a miniature eye

    Gregor Belušič
    Insight

    The first complete 3D reconstruction of the compound eye of a minute wasp species sheds light on the nuts and bolts of size reduction.

    1. Developmental Biology
    2. Evolutionary Biology

    Single-cell sequencing provides clues about the developmental genetic basis of evolutionary adaptations in syngnathid fishes

    Hope M Healey, Hayden B Penn ... William A Cresko
    Research Article

    Seahorses, pipefishes, and seadragons are fishes from the family Syngnathidae that have evolved extraordinary traits including male pregnancy, elongated snouts, loss of teeth, and dermal bony armor. The developmental genetic and cellular changes that led to the evolution of these traits are largely unknown. Recent syngnathid genome assemblies revealed suggestive gene content differences and provided the opportunity for detailed genetic analyses. We created a single-cell RNA sequencing atlas of Gulf pipefish embryos to understand the developmental basis of four traits: derived head shape, toothlessness, dermal armor, and male pregnancy. We completed marker gene analyses, built genetic networks, and examined the spatial expression of select genes. We identified osteochondrogenic mesenchymal cells in the elongating face that express regulatory genes bmp4, sfrp1a, and prdm16. We found no evidence for tooth primordia cells, and we observed re-deployment of osteoblast genetic networks in developing dermal armor. Finally, we found that epidermal cells expressed nutrient processing and environmental sensing genes, potentially relevant for the brooding environment. The examined pipefish evolutionary innovations are composed of recognizable cell types, suggesting that derived features originate from changes within existing gene networks. Future work addressing syngnathid gene networks across multiple stages and species is essential for understanding how the novelties of these fish evolved.