Constructive neutral evolution

Constructive neutral evolution (CNE) is a theory that seeks to explain how complex systems can evolve through neutral transitions and spread through a population by chance fixation (genetic drift).[1] Constructive neutral evolution is a competitor for both adaptationist explanations for the emergence of complex traits and hypotheses positing that a complex trait emerged as a response to a deleterious development in an organism.[2] Constructive neutral evolution often leads to irreversible or "irremediable" complexity[3] and produces systems which, instead of being finely adapted for performing a task, represent an excess complexity that has been described with terms such as "runaway bureaucracy" or even a "Rube Goldberg machine".[4]

The groundworks for the concept of CNE were laid by two papers in the 1990s, although first explicitly proposed by Arlin Stoltzfus in 1999.[1][2][5] The first proposals for the role CNE was in the evolutionary origins of complex macromolecular machines such as the spliceosome, RNA editing machinery, supernumerary ribosomal proteins, chaperones, and more.[4][6][7] Since then and as an emerging trend of studies in molecular evolution,[8] CNE has been applied to broader features of biology and evolutionary history including some models of eukaryogenesis, the emergence of complex interdependence in microbial communities, and de novo formation of functional elements from non-functional transcripts of junk DNA.[9][10] Several approaches propose a combination of neutral and adaptive contributions in the evolutionary origins of various traits.[11]

Many evolutionary biologists posit that CNE must be the null hypothesis when explaining the emergence of complex systems to avoid assuming that a trait arose for an adaptive benefit. A trait may have arisen neutrally, even if later co-opted for another function. This approach stresses the need for rigorous demonstrations of adaptive explanations when describing the emergence of traits. This avoids the "adaptationist fallacy" which assumes that all traits emerge because they are adaptively favoured by natural selection.[9][12]

  1. ^ a b Stoltzfus, Arlin (1999). "On the Possibility of Constructive Neutral Evolution". Journal of Molecular Evolution. 49 (2): 169–181. Bibcode:1999JMolE..49..169S. doi:10.1007/PL00006540. ISSN 0022-2844. PMID 10441669. S2CID 1743092.
  2. ^ a b Muñoz-Gómez, Sergio A.; Bilolikar, Gaurav; Wideman, Jeremy G.; Geiler-Samerotte, Kerry (2021-04-01). "Constructive Neutral Evolution 20 Years Later". Journal of Molecular Evolution. 89 (3): 172–182. Bibcode:2021JMolE..89..172M. doi:10.1007/s00239-021-09996-y. ISSN 1432-1432. PMC 7982386. PMID 33604782.
  3. ^ Gray, Michael W.; Lukeš, Julius; Archibald, John M.; Keeling, Patrick J.; Doolittle, W. Ford (2010-11-12). "Irremediable Complexity?". Science. 330 (6006): 920–921. Bibcode:2010Sci...330..920G. doi:10.1126/science.1198594. ISSN 0036-8075. PMID 21071654. S2CID 206530279.
  4. ^ a b Lukeš, Julius; Archibald, John M.; Keeling, Patrick J.; Doolittle, W. Ford; Gray, Michael W. (2011). "How a neutral evolutionary ratchet can build cellular complexity". IUBMB Life. 63 (7): 528–537. doi:10.1002/iub.489. PMID 21698757. S2CID 7306575.
  5. ^ Covello, PatrickS.; Gray, MichaelW. (1993). "On the evolution of RNA editing". Trends in Genetics. 9 (8): 265–268. doi:10.1016/0168-9525(93)90011-6. PMID 8379005.
  6. ^ Gray, Michael W.; Lukeš, Julius; Archibald, John M.; Keeling, Patrick J.; Doolittle, W. Ford (2010-11-12). "Irremediable Complexity?". Science. 330 (6006): 920–921. Bibcode:2010Sci...330..920G. doi:10.1126/science.1198594. ISSN 0036-8075. PMID 21071654. S2CID 206530279.
  7. ^ Lamech, Lilian T.; Mallam, Anna L.; Lambowitz, Alan M. (2014-12-23). Herschlag, Daniel (ed.). "Evolution of RNA-Protein Interactions: Non-Specific Binding Led to RNA Splicing Activity of Fungal Mitochondrial Tyrosyl-tRNA Synthetases". PLOS Biology. 12 (12): e1002028. doi:10.1371/journal.pbio.1002028. ISSN 1545-7885. PMC 4275181. PMID 25536042.
  8. ^ Liberles, David A.; Chang, Belinda; Geiler-Samerotte, Kerry; Goldman, Aaron; Hey, Jody; Kaçar, Betül; Meyer, Michelle; Murphy, William; Posada, David; Storfer, Andrew (2020). "Emerging Frontiers in the Study of Molecular Evolution". Journal of Molecular Evolution. 88 (3): 211–226. Bibcode:2020JMolE..88..211L. doi:10.1007/s00239-020-09932-6. ISSN 0022-2844. PMC 7386396. PMID 32060574.
  9. ^ a b Cite error: The named reference :3 was invoked but never defined (see the help page).
  10. ^ Palazzo, Alexander F.; Koonin, Eugene V. (2020-11-25). "Functional Long Non-coding RNAs Evolve from Junk Transcripts". Cell. 183 (5): 1151–1161. doi:10.1016/j.cell.2020.09.047. PMID 33068526. S2CID 222815635.
  11. ^ Vosseberg, Julian; Snel, Berend (2017-12-01). "Domestication of self-splicing introns during eukaryogenesis: the rise of the complex spliceosomal machinery". Biology Direct. 12 (1): 30. doi:10.1186/s13062-017-0201-6. ISSN 1745-6150. PMC 5709842. PMID 29191215.
  12. ^ Cite error: The named reference :2 was invoked but never defined (see the help page).