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Mutational hazard hypothesis

The mutational hazard hypothesis is a non-adaptive theory for increased complexity in genomes.[1] The basis of mutational hazard hypothesis is that each mutation for non-coding DNA imposes a fitness cost.[2] Variation in complexity can be described by 2Neu, where Ne is effective population size and u is mutation rate.[3]

In this hypothesis, selection against non-coding DNA can be reduced in three ways: random genetic drift, recombination rate, and mutation rate.[4] As complexity increases from prokaryotes to multicellular eukaryotes, effective population size decreases, subsequently increasing the strength of random genetic drift[1]. This, along with low recombination rate[4] and high mutation rate[4], allows non-coding DNA to proliferate without being removed by purifying selection.[1]

Accumulation of non-coding DNA in larger genomes can be seen when comparing genome size and genome content across eukaryotic taxa. There is a positive correlation between genome size and noncoding DNA genome content with each group staying within some variation.[1][2] When comparing variation in complexity in organelles, effective population size is replaced with genetic effective population size (Ng).[3] In plant and animal mitochondria, differences in mutation rate account for the opposite directions in complexity, with plant mitochondria being more complex and animal mitochondria more streamlined.[5]

The mutational hazard hypothesis has been used to explain expanded mitochondrial, nuclear, and plastid genomes in Volvox cateri by comparing differences in silent-site nucleotide diversity.[6] However a later study found that Volvox cateri and Volvox africanus have a higher intergenic mutation rate in their plastid genomes, opposite of what the hypothesis predicts.[7] The hypothesis was also used as a possible explanation for intron loss and compact genome size in Arabiopsis thaliana. When compared to Arabidopsis lyrata, researchers found a higher mutation rate overall and in lost introns (an itron that is no longer transcribed or spliced) compared to conserved introns.[8]

Mitochondrial genomes in Seline noctiflora and Seline conica only partially lined up with the mutational hazard hypothesis. Even though they have lower intron lengths and more non-coding DNA elements, their higher mutation rate and genome expansion is opposite of what the hypothesis predicts.[9] If the difference in size between Curcurbita pepo and Citrullus lanatus could be explained by the hypothesis, then the former would have a lower mitochondrial mutation rate than the latter because it is larger. However this didn't prove true because the mutation rate in Curcurbita pepo is four times higher than that of Citrullus lanatus.[10] There was also an attempt to use the hypothesis to explain large nuclear genomes of salamander, but researchers found opposite results than expected, including lower long-term strength of genetic drift.[11]

  1. ^ a b c d Lynch, Michael; Conery, John S. (2003-11-21). "The Origins of Genome Complexity". Science. 302 (5649): 1401–1404. doi:10.1126/science.1089370. ISSN 0036-8075.
  2. ^ a b Lynch, Michael; Bobay, Louis-Marie; Catania, Francesco; Gout, Jean-François; Rho, Mina (2011-09-22). "The Repatterning of Eukaryotic Genomes by Random Genetic Drift". Annual Review of Genomics and Human Genetics. 12 (1): 347–366. doi:10.1146/annurev-genom-082410-101412. ISSN 1527-8204. PMC 4519033. PMID 21756106.{{cite journal}}: CS1 maint: PMC format (link)
  3. ^ a b Lynch, M. (2006-03-24). "Mutation Pressure and the Evolution of Organelle Genomic Architecture". Science. 311 (5768): 1727–1730. doi:10.1126/science.1118884. ISSN 0036-8075.
  4. ^ a b c Lynch, Michael (2006-02-01). "The Origins of Eukaryotic Gene Structure". Molecular Biology and Evolution. 23 (2): 450–468. doi:10.1093/molbev/msj050. ISSN 0737-4038.
  5. ^ Lynch, Michael (2006-10-13). "Streamlining and Simplification of Microbial Genome Architecture". Annual Review of Microbiology. 60 (1): 327–349. doi:10.1146/annurev.micro.60.080805.142300. ISSN 0066-4227.
  6. ^ Smith, D. R.; Lee, R. W. (2010-10-01). "Low Nucleotide Diversity for the Expanded Organelle and Nuclear Genomes of Volvox carteri Supports the Mutational-Hazard Hypothesis". Molecular Biology and Evolution. 27 (10): 2244–2256. doi:10.1093/molbev/msq110. ISSN 0737-4038.
  7. ^ Gaouda, Hager; Hamaji, Takashi; Yamamoto, Kayoko; Kawai-Toyooka, Hiroko; Suzuki, Masahiro; Noguchi, Hideki; Minakuchi, Yohei; Toyoda, Atsushi; Fujiyama, Asao; Nozaki, Hisayoshi; Smith, David Roy (2018-09-01). Chaw, Shu-Miaw (ed.). "Exploring the Limits and Causes of Plastid Genome Expansion in Volvocine Green Algae". Genome Biology and Evolution. 10 (9): 2248–2254. doi:10.1093/gbe/evy175. ISSN 1759-6653. PMC 6128376. PMID 30102347.{{cite journal}}: CS1 maint: PMC format (link)
  8. ^ Yang, Yu-Fei; Zhu, Tao; Niu, Deng-Ke (2013-04-XX). "Association of Intron Loss with High Mutation Rate in Arabidopsis: Implications for Genome Size Evolution". Genome Biology and Evolution. 5 (4): 723–733. doi:10.1093/gbe/evt043. ISSN 1759-6653. PMC 4104619. PMID 23516254. {{cite journal}}: Check date values in: |date= (help)CS1 maint: PMC format (link)
  9. ^ Sloan, Daniel B.; Alverson, Andrew J.; Chuckalovcak, John P.; Wu, Martin; McCauley, David E.; Palmer, Jeffrey D.; Taylor, Douglas R. (2012-01-17). Gray, Michael William (ed.). "Rapid Evolution of Enormous, Multichromosomal Genomes in Flowering Plant Mitochondria with Exceptionally High Mutation Rates". PLoS Biology. 10 (1): e1001241. doi:10.1371/journal.pbio.1001241. ISSN 1545-7885. PMC 3260318. PMID 22272183.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  10. ^ Alverson, Andrew J.; Wei, XioXin; Rice, Danny W.; Stern, David B.; Barry, Kerrie; Palmer, Jeffrey D. (January 29, 2010). "Insights into the Evolution of Mitochondrial Genome Size from Complete Sequences of Citrus lanatus and Curcurbita pepo (Curcurbitaceae)". Molecular Biology and Evoltuion. 27: 1436–1448.
  11. ^ Mohlhenrich, Erik Roger; Lockridge Mueller, Rachel (September 27, 2016). "Genetic drift and mutational hazard in the evolution of salamander genomic gigantism". Evolution. 70: 2865–2878 – via JSTOR.
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