Cold genome hypothesis
The cold genome hypothesis is an evolutionary theory that correlates the rate of genomic mutations caused by transposable elements with the process of speciation. The hypothesis states that in taxa presenting an ongoing evolutionary radiation, their higher frequency of speciation depends in part on the fast mutation rate caused by active transposable elements. The term cold genome was coined by the biologist Marco Ricci in 2014[1]. In this context, “cold” genomes are genomes with few or no active transposable elements and should correspond to taxa with low speciation rates. On the other hand, “hot” genomes feature high TE activity associated with accelerated diversification [2][3]. Therefore, this hypothesis provides a framework that bridges the activity of these genetic elements to patterns of speciation as described by the punctuated equilibria evolutionary theory. The first study that introduced the hypothesis and statistically validated it was done on mammals [3] then later studies found similar results also in cichlid fish,[4],[5] and birds [6].
Content of hypothesis
The evolutionary radiation, once it occurs in a certain taxon, is characterised by an increased diversity of species over time because of an increased rate of speciation.[7] The cold genome hypothesis provides a new framework to detect patterns of increased rates of speciation and to test whether these rates correspond to an increased level of transposable element activity. The “relative rate of speciation” (RRS) is the innovative strategy designed to distinguish between actual and apparent differences in the speciation rates. “The RRS is a conditional parameter that compares a pair of taxa at the same hierarchical level (e.g., two families within the same order). If one taxon of a given pair at the same time shows (1) a higher number of species and (2) a lower age compared to its paired taxon, then its RRS is positive (+) and putatively experienced a (relatively) recent speciation burst. Consequently, the other taxon has a negative RRS (−) and is experiencing a more static phase. If only one of the two conditions is met, there is no evidence of adaptive radiation/stasis for neither of the two taxa (RRS = 0). The RRS can be applied at any taxonomical level on any monophyletic clade.” [3]. The RRS attribution is represented by the logical formulae: RRS1(+), RRS2(−) ∶ NS1 > NS2ΛCA1 < CA2, NS = number of species of the taxon CA = crown age of the taxon According to the cold genome hypothesis, the genome of species belonging to the taxon with RRS (+) is expected to show a higher density of recently inserted transposable elements (hot genome) than the counterpart with RRS (-) (cold genome). The density of recently inserted transposable elements is a measure of the impact of insertional mutagenesis occurring in a genome. Ricci and colleagues showed that the species labelled as RRS (+) have genomes with higher density of recently inserted transposable elements [3]. A genome is cold when its transposable elements are mainly inactive and consequently its structure should remain more stable over time with respect to genomes which transposable elements are active (hot genomes).

The debated idea of stasis proposed by Stephen Jay Gould and Niles Eldredge in the punctuated equilibria evolutionary theory finds a molecular ally since a cold genome has lower mutation of the genotype and should reflect at least in part a slower change in the phenotype. Already Barbara McClintock in the 50’s intuited the possible role of transposable elements in the evolution of genomes. Indeed, since their discovery, transposable elements were found to be involved in the origin of key evolutionary features like the vertebrate acquired immune system [8] and the industrial melanism observed in the peppered moths Biston betularia [9] (the animal that provided the real time evidence of Darwinian natural selection). Because of these and numerous other evidence, scientists hypothesized an involvement of transposable elements in the origin of species and proposed various models all compatible with the cold genome hypothesis: carrier subpopulation [10], TE thrust [11] and epi-transposons [12] hypotheses. The different models and mechanisms proposed by these authors do not conflict with each other, but all can contribute to explain the speciation processes.
References
- ↑ Ricci, Marco (2014). "Transposable elements dynamics in taxa with different reproductive strategies or speciation rate". doi:10.6092/unibo/amsdottorato/6537.
- ↑ Naciri, Yamama; Linder, H. Peter (2020). "The genetics of evolutionary radiations". Biological Reviews. 95 (4): 1055–1072. doi:10.1111/brv.12598. PMID 32233014 Check
|pmid=value (help). Unknown parameter|s2cid=ignored (help) - ↑ 3.0 3.1 Ricci, Marco; Peona, Valentina; Guichard, Etienne; Taccioli, Cristian; Boattini, Alessio (2018). "Transposable Elements Activity is Positively Related to Rate of Speciation in Mammals". Journal of Molecular Evolution. 86 (5): 303–310. Bibcode:2018JMolE..86..303R. doi:10.1007/s00239-018-9847-7. PMC 6028844. PMID 29855654.
- ↑ Carleton, Karen L.; Conte, Matthew A.; Malinsky, Milan; Nandamuri, Sri Pratima; Sandkam, Benjamin A.; Meier, Joana I.; Mwaiko, Salome; Seehausen, Ole; Kocher, Thomas D. (2020). "Movement of transposable elements contributes to cichlid diversity". Molecular Ecology. 29 (24): 4956–4969. doi:10.1111/mec.15685. PMID 33049090 Check
|pmid=value (help). Unknown parameter|s2cid=ignored (help) - ↑ Ahmad, Syed Farhan; Singchat, Worapong; Panthum, Thitipong; Thitipong, Kornsorn (2021). "Impact of repetitive DNA elements on snake genome biology and evolution". Cells. 10 (7): 1707. doi:10.3390/cells10071707. PMC 8303610 Check
|pmc=value (help). PMID 34359877 Check|pmid=value (help). - ↑ Galbraith, James; Kortschak, Robert Daniel; Suh, Alexander (2021). "Genome Stability Is in the Eye of the Beholder: CR1 Retrotransposon Activity Varies Significantly across Avian Diversity". Genome Biology and Evolution. 13 (12): 1–14. doi:10.1093/gbe/evab259. PMC 8665684 Check
|pmc=value (help). PMID 34894225 Check|pmid=value (help). - ↑ Simões, M.; Breitkreuz, L.; Alvarado, M.; Baca, S.; Cooper, J.C.; Heins, L.; Herzog, K.; Lieberman, B.S. (January 2016). "The Evolving Theory of Evolutionary Radiations". Trends in Ecology & Evolution. 31 (1): 27–34. doi:10.1016/j.tree.2015.10.007. PMID 26632984.
- ↑ Kapitonov, Vladimir V; Jurka, Jerzy (24 May 2005). "RAG1 Core and V(D)J Recombination Signal Sequences Were Derived from Transib Transposons". PLOS Biology. 3 (6): e181. doi:10.1371/journal.pbio.0030181. PMC 1131882. PMID 15898832.
- ↑ Hof, Arjen E. van’t; Campagne, Pascal; Rigden, Daniel J.; Yung, Carl J.; Lingley, Jessica; Quail, Michael A.; Hall, Neil; Darby, Alistair C.; Saccheri, Ilik J. (June 2016). "The industrial melanism mutation in British peppered moths is a transposable element". Nature. 534 (7605): 102–105. Bibcode:2016Natur.534..102H. doi:10.1038/nature17951.
- ↑ Jurka, Jerzy; Bao, Weidong; Kojima, Kenji K (2011). "Families of transposable elements, population structure and the origin of species". Biology Direct. 6 (1): 44. doi:10.1186/1759-8753-2-8. PMC 3183009. PMID 21929767.
- ↑ Oliver, Keith R; Greene, Wayne K (2011). "Mobile DNA and the TE-Thrust hypothesis: supporting evidence from the primates". Mobile DNA. 2 (1): 8. doi:10.1186/1759-8753-2-8. PMC 3123540. PMID 21627776.
- ↑ Zeh, David W.; Zeh, Jeanne A.; Ishida, Yoichi (July 2009). "Transposable elements and an epigenetic basis for punctuated equilibria". BioEssays. 31 (7): 715–726. doi:10.1002/bies.200900026. PMID 19472370. Unknown parameter
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