Preprint Article Version 1 This version is not peer-reviewed

Stress-Induced Evolutionary Innovation: A Mechanism for the Origin of Cell Types

Version 1 : Received: 8 September 2018 / Approved: 11 September 2018 / Online: 11 September 2018 (11:41:34 CEST)

How to cite: Wagner, G.P.; Erkenbrack, E.M.; Love, A.C. Stress-Induced Evolutionary Innovation: A Mechanism for the Origin of Cell Types. Preprints 2018, 2018090193 (doi: 10.20944/preprints201809.0193.v1). Wagner, G.P.; Erkenbrack, E.M.; Love, A.C. Stress-Induced Evolutionary Innovation: A Mechanism for the Origin of Cell Types. Preprints 2018, 2018090193 (doi: 10.20944/preprints201809.0193.v1).

Abstract

Understanding the evolutionary role of environmentally-induced phenotypic variation (i.e., environmental plasticity) is an important issue in developmental evolution. One of the major physiological responses to environmental changes is cellular stress, which is counteracted by a generic stress reaction that detoxifies the cell, refolds proteins, and repairs DNA damage. In this paper, we elaborate on a previous finding suggesting that the cell differentiation cascade of human decidual stromal cells, a cell type critical for embryo implantation and the maintenance of pregnancy, evolved from a cellular stress reaction. We hypothesize that the stress reaction in these cells was elicited ancestrally through the inflammation caused by embryo attachment and invasion. We describe a model, Stress-Induced Evolutionary Innovation (SIEI), whereby ancestral stress reactions and their corresponding pathways can be transformed into novel structural components of body plans, such as new cell types. After reviewing similarities and differences between SIEI and the “plasticity first hypothesis” (PFH) of evolution, we argue that SIEI is a distinct form of plasticity-based evolutionary change because it leads to the origin of novel structures rather than the adaptive transformation of a pre-existing character.

Subject Areas

evolutionary innovation, cell type evolution, cellular stress response, evolution of gene regulation, gene regulatory network evolution, decidual cell, evolution of pregnancy

Comments (3)

Comment 1
Received: 4 November 2018
Commenter: Todd Oakley
The commenter has declared there is no conflict of interests.
Comment: I find the idea of SIEI very interesting, and I am glad to see the idea laid out here in a general and fairly detailed way.

I too have thought about the idea of SIEI, inspired by my research on evolutionary origins of eyes. While definitely not the prime focus, I proposed (with co-author Dan Speiser) that eye evolution involved SIEI. This idea came out of a synthesis on the evolutionary origins of genes involved in eyes and vision, published here:

https://www.annualreviews.org/doi/full/10.1146/annurev-ecolsys-110512-135907
Note, for example, the last 2 lines of the abstract:

"Multiple genes used in eyes today had ancestral roles in stress responses. We hypothesize that photo-oxidative stress had a role in eye origins by increasing the chance that those genes were expressed together in places on animals where light was abundant."

Also, in the main text, we wrote:
"Because light causes photo-oxidative stress and DNA damage, protective responses are mounted in cells exposed to much light. We speculate that during evolutionary history multiple genes that now interact for visual function originated in stress responses to light."

We review how genes like melanin and crystallins are deployed under photo-oxidative stress.

Dan and I discussed (although space limitations prevented much from getting into the final paper much beyond what I quote above) ideas very similar to SIEI acting during eye evolution. It seems quite logical that plasticity due to localized responses to photo-stress could pre-date genetic assimilation of genes like melanin and crystallins that are critical for eye function.

Of course other light-interacting structures might also have evolved similarly, like feathers or photophores:
http://evolutionarynovelty.blogspot.com/2009/06/eyes-abound.html
Perhaps SIEI is quite general indeed!
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Response 1 to Comment 1
Received: 5 November 2018
Commenter: Gunter Wagner
Commenter's Conflict of Interests: I am an author of the posted preprint
Comment: Dear Todd,

I am very glad that you made the connection between our findings on stromal cells publishe in PLoS Biology this year, and your ideas about photoreceptors and lense cells. I am very excited that these connections are emerging.

Best,
Gunter Wagner
Comment 2
Received: 9 April 2019
Commenter: Todd Oakley
The commenter has declared there is no conflict of interests.
Comment: We now summarized some of the literature on the connections between light-induced stress and eye evolution; in part inspired by this SIEI manuscript.

https://www.preprints.org/manuscript/201904.0107/v1
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