Contingency and chance erase necessity in the experimental evolution of ancestral proteins
- University of Chicago, United States
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).
-
BCL2-Chance and ContingencyDryad Digital Repository, 10.5061/dryad.866t1g1ns.
Article and author information
Author details
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
-
- 6,770
- views
-
- 951
- downloads
-
- 32
- 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)
Contingency and chance erase necessity in the experimental evolution of ancestral proteins
eLife 10:e67336.
https://doi.org/10.7554/eLife.67336
Further reading
-
- Evolutionary Biology
Haldane’s rule occupies a special place in biology as one of the few ‘rules’ of speciation, with empirical support from hundreds of species. And yet, its classic purview is restricted taxonomically to the subset of organisms with heteromorphic sex chromosomes. I propose explicit acknowledgement of generalized hypotheses about Haldane’s rule that frame sex bias in hybrid dysfunction broadly and irrespective of the sexual system. The consensus view of classic Haldane’s rule holds that sex-biased hybrid dysfunction across taxa is a composite phenomenon that requires explanations from multiple causes. Testing of the multiple alternative hypotheses for Haldane’s rule is, in many cases, applicable to taxa with homomorphic sex chromosomes, environmental sex determination, haplodiploidy, and hermaphroditism. Integration of a variety of biological phenomena about hybrids across diverse sexual systems, beyond classic Haldane’s rule, will help to derive a more general understanding of the contributing forces and mechanisms that lead to predictable sex biases in evolutionary divergence and speciation.
-
- Evolutionary Biology
Living organisms control the formation of mineral skeletons and other structures through biomineralization. Major phylogenetic groups usually consistently follow a single biomineralization pathway. Foraminifera, which are very efficient marine calcifiers, making a substantial contribution to global carbonate production and global carbon sequestration, are regarded as an exception. This phylum has been commonly thought to follow two contrasting models of either in situ ‘mineralization of extracellular matrix’ attributed to hyaline rotaliid shells, or ‘mineralization within intracellular vesicles’ attributed to porcelaneous miliolid shells. Our previous results on rotaliids along with those on miliolids in this paper question such a wide divergence of biomineralization pathways within the same phylum of Foraminifera. We have found under a high-resolution scanning electron microscopy (SEM) that precipitation of high-Mg calcitic mesocrystals in porcelaneous shells takes place in situ and form a dense, chaotic meshwork of needle-like crystallites. We have not observed calcified needles that already precipitated in the transported vesicles, what challenges the previous model of miliolid mineralization. Hence, Foraminifera probably utilize less divergent calcification pathways, following the recently discovered biomineralization principles. Mesocrystalline chamber walls in both models are therefore most likely created by intravesicular accumulation of pre-formed liquid amorphous mineral phase deposited and crystallized within the extracellular organic matrix enclosed in a biologically controlled privileged space by active pseudopodial structures. Both calcification pathways evolved independently in the Paleozoic and are well conserved in two clades that represent different chamber formation modes.
