Restricted access
Research articles
Research articles
Genomic estimates of mutation and substitution rates contradict the evolutionary speed hypothesis of the latitudinal diversity gradient
Published:25 October 2023https://doi.org/10.1098/rspb.2023.1787
Abstract
The latitudinal diversity gradient (LDG) refers to a decrease in biodiversity from the equator to the poles. The evolutionary speed hypothesis, backed by the metabolic theory of ecology, asserts that nucleotide mutation and substitution rates per site per year are higher and thereby speciation rates are higher at higher temperatures, generating the LDG. However, prior empirical investigations of the relationship between the temperature and mutation or substitution rate were based on a few genes and the results were mixed. We here revisit this relationship using genomic data. No significant correlation between the temperature and mutation rate is found in 13 prokaryotes or in 107 eukaryotes. An analysis of 234 diverse trios of bacterial taxa indicates that the synonymous substitution rate is not significantly associated with the growth temperature. The same data, however, reveal a significant negative association between the nonsynonymous substitution rate and temperature, which is explainable by a larger fraction of detrimental nonsynonymous mutations at higher temperatures due to a stronger demand for protein stability. We conclude that the evolutionary speed hypothesis of the LDG is unsupported by genomic data and advise that future mechanistic studies of the LDG should focus on other hypotheses.
Footnotes
References
- 1.
Hillebrand H . 2004 On the generality of the latitudinal diversity gradient. Am. Nat. 163, 192-211. (doi:10.1086/381004) Crossref, PubMed, Web of Science, Google Scholar - 2.
Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL, Brown JH . 2008 A latitudinal diversity gradient in planktonic marine bacteria. Proc. Natl Acad. Sci. USA 105, 7774-7778. (doi:10.1073/pnas.0803070105) Crossref, PubMed, Web of Science, Google Scholar - 3.
Dowle EJ, Morgan-Richards M, Trewick SA . 2013 Molecular evolution and the latitudinal biodiversity gradient. Heredity (Edinb) 110, 501-510. (doi:10.1038/hdy.2013.4) Crossref, PubMed, Web of Science, Google Scholar - 4.
Mittelbach GG 2007 Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol. Lett. 10, 315-331. (doi:10.1111/j.1461-0248.2007.01020.x) Crossref, PubMed, Web of Science, Google Scholar - 5.
Rohde K . 1992 Latitudinal gradients in species diversity: the search for the primary cause. Oikos 65, 514-527. (doi:10.2307/3545569) Crossref, Web of Science, Google Scholar - 6.
Martin AP, Palumbi SR . 1993 Body size, metabolic rate, generation time, and the molecular clock. Proc. Natl Acad. Sci. USA 90, 4087-4091. (doi:10.1073/pnas.90.9.4087) Crossref, PubMed, Web of Science, Google Scholar - 7.
Gillooly JF, Allen AP, West GB, Brown JH . 2005 The rate of DNA evolution: effects of body size and temperature on the molecular clock. Proc. Natl Acad. Sci. USA 102, 140-145. (doi:10.1073/pnas.0407735101) Crossref, PubMed, Google Scholar - 8.
Kimura M . 1983 The neutral theory of molecular evolution. Cambridge, UK: Cambridge University Press. Crossref, Google Scholar - 9.
Allen AP, Gillooly JF, Savage VM, Brown JH . 2006 Kinetic effects of temperature on rates of genetic divergence and speciation. Proc. Natl Acad. Sci. USA 103, 9130-9135. (doi:10.1073/pnas.0603587103) Crossref, PubMed, Web of Science, Google Scholar - 10.
Chu XL, Zhang BW, Zhang QG, Zhu BR, Lin K, Zhang DY . 2018 Temperature responses of mutation rate and mutational spectrum in an Escherichia coli strain and the correlation with metabolic rate. BMC Evol. Biol. 18, 126. (doi:10.1186/s12862-018-1252-8) Crossref, PubMed, Web of Science, Google Scholar - 11.
Waldvogel AM, Pfenninger M . 2021 Temperature dependence of spontaneous mutation rates. Genome Res. 31, 1582-1589. (doi:10.1101/gr.275168.120) Crossref, PubMed, Web of Science, Google Scholar - 12.
Ogur M, Ogur S, St John R . 1960 Temperature dependence of the spontaneous mutation rate to respiration deficiency in Saccharomyces. Genetics 45, 189-194. (doi:10.1093/genetics/45.2.189) Crossref, PubMed, Web of Science, Google Scholar - 13.
Liu H, Zhang J . 2021 The rate and molecular spectrum of mutation are selectively maintained in yeast. Nat. Commun. 12, 4044. (doi:10.1038/s41467-021-24364-6) Crossref, PubMed, Web of Science, Google Scholar - 14.
Kimura M . 1967 On the evolutionary adjustment of spontaneous mutation rates. Genet. Res. 9, 23-34. (doi:10.1017/S0016672300010284) Crossref, Web of Science, Google Scholar - 15.
Ho WC, Zhang J . 2018 Evolutionary adaptations to new environments generally reverse plastic phenotypic changes. Nat. Commun. 9, 350. (doi:10.1038/s41467-017-02724-5) Crossref, PubMed, Web of Science, Google Scholar - 16.
Liu H, Zhang J . 2019 Yeast spontaneous mutation rate and spectrum vary with environment. Curr. Biol. 29, 1584-1591. (doi:10.1016/j.cub.2019.03.054) Crossref, PubMed, Web of Science, Google Scholar - 17.
Drake JW . 2009 Avoiding dangerous missense: thermophiles display especially low mutation rates. PLoS Genet. 5, e1000520. (doi:10.1371/journal.pgen.1000520) Crossref, PubMed, Web of Science, Google Scholar - 18.
Vieille C, Zeikus GJ . 2001 Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol. Mol. Biol. Rev. 65, 1-43. (doi:10.1128/MMBR.65.1.1-43.2001) Crossref, PubMed, Web of Science, Google Scholar - 19.
Stark C, Bautista-Leung T, Siegfried J, Herschlag D . 2022 Systematic investigation of the link between enzyme catalysis and cold adaptation. eLife 11, e72884. (doi:10.7554/eLife.72884) Crossref, PubMed, Web of Science, Google Scholar - 20.
Joyner-Matos J, Bean LC, Richardson HL, Sammeli T, Baer CF . 2011 No evidence of elevated germline mutation accumulation under oxidative stress in Caenorhabditis elegans. Genetics 189, 1439-1447. (doi:10.1534/genetics.111.133660) Crossref, PubMed, Web of Science, Google Scholar - 21.
Rajaei M, Saxena AS, Johnson LM, Snyder MC, Crombie TA, Tanny RE, Andersen EC, Joyner-Matos J, Baer CF . 2021 Mutability of mononucleotide repeats, not oxidative stress, explains the discrepancy between laboratory-accumulated mutations and the natural allele-frequency spectrum in C. elegans. Genome Res. 31, 1602-1613. (doi:10.1101/gr.275372.121) Crossref, PubMed, Web of Science, Google Scholar - 22.
Wright S, Keeling J, Gillman L . 2006 The road from Santa Rosalia: a faster tempo of evolution in tropical climates. Proc. Natl Acad. Sci. USA 103, 7718-7722. (doi:10.1073/pnas.0510383103) Crossref, PubMed, Web of Science, Google Scholar - 23.
Wright SD, Ross HA, Keeling DJ, McBride P, Gillman LN . 2011 Thermal energy and the rate of genetic evolution in marine fishes. Evol. Ecol. 25, 525-530. (doi:10.1007/s10682-010-9416-z) Crossref, Web of Science, Google Scholar - 24.
Lourenco JM, Glemin S, Chiari Y, Galtier N . 2013 The determinants of the molecular substitution process in turtles. J. Evol. Biol. 26, 38-50. (doi:10.1111/jeb.12031) Crossref, PubMed, Web of Science, Google Scholar - 25.
Bleiweiss R . 1998 Slow rate of molecular evolution in high-elevation hummingbirds. Proc. Natl Acad. Sci. USA 95, 612-616. (doi:10.1073/pnas.95.2.612) Crossref, PubMed, Web of Science, Google Scholar - 26.
Gillman LN, Keeling DJ, Ross HA, Wright SD . 2009 Latitude, elevation and the tempo of molecular evolution in mammals. Proc. Biol. Sci. 276, 3353-3359. (doi:10.1098/rspb.2009.0674) Link, Web of Science, Google Scholar - 27.
Gillman LN, Wright SD . 2014 Species richness and evolutionary speed: the influence of temperature, water and area. J. Biogeogr. 41, 39-51. (doi:10.1111/jbi.12173) Crossref, Web of Science, Google Scholar - 28.
Rolland J, Loiseau O, Romiguier J, Salamin N . 2016 Molecular evolutionary rates are not correlated with temperature and latitude in Squamata: an exception to the metabolic theory of ecology? BMC Evol. Biol. 16, 95. (doi:10.1186/s12862-016-0666-4) Crossref, PubMed, Web of Science, Google Scholar - 29.
Bromham L, Cardillo M . 2003 Testing the link between the latitudinal gradient in species richness and rates of molecular evolution. J. Evol. Biol. 16, 200-207. (doi:10.1046/j.1420-9101.2003.00526.x) Crossref, PubMed, Web of Science, Google Scholar - 30.
Brown JH, Gillooly JF, Allen AP, Savage VM, West GB . 2004 Toward a metabolic theory of ecology. Ecology 857, 1771-1789. (doi:10.1890/03-9000) Crossref, Google Scholar - 31.
Lanfear R, Thomas JA, Welch JJ, Brey T, Bromham L . 2007 Metabolic rate does not calibrate the molecular clock. Proc. Natl Acad. Sci. USA 104, 15 388-15 393. (doi:10.1073/pnas.0703359104) Crossref, Web of Science, Google Scholar - 32.
Orton MG, May JA, Ly W, Lee DJ, Adamowicz SJ . 2019 Is molecular evolution faster in the tropics? Heredity (Edinb) 122, 513-524. (doi:10.1038/s41437-018-0141-7) Crossref, PubMed, Web of Science, Google Scholar - 33.
Felsenstein J . 1985 Phylogenies and the comparative method. Am. Nat. 125, 1-15. (doi:10.1086/284325) Crossref, Web of Science, Google Scholar - 34.
Wang Y, Obbard DJ . 2023 Experimental estimates of germline mutation rate in eukaryotes: a phylogenetic meta-analysis. Evol. Lett. 7, 216-226. (doi:10.1093/evlett/qrad027) Crossref, PubMed, Web of Science, Google Scholar - 35.
Engqvist MKM . 2018 Correlating enzyme annotations with a large set of microbial growth temperatures reveals metabolic adaptations to growth at diverse temperatures. BMC Microbiol. 18, 177. (doi:10.1186/s12866-018-1320-7) Crossref, PubMed, Web of Science, Google Scholar - 36.
Pinney MM 2021 Parallel molecular mechanisms for enzyme temperature adaptation. Science 371, eaay2784. (doi:10.1126/science.aay2784) Crossref, PubMed, Web of Science, Google Scholar - 37.
Shen X, Song S, Li C, Zhang J . 2022 Synonymous mutations in representative yeast genes are mostly strongly non-neutral. Nature 606, 725-731. (doi:10.1038/s41586-022-04823-w) Crossref, PubMed, Web of Science, Google Scholar - 38.
Lind PA, Berg OG, Andersson DI . 2010 Mutational robustness of ribosomal protein genes. Science 330, 825-827. (doi:10.1126/science.1194617) Crossref, PubMed, Web of Science, Google Scholar - 39.
Sharon E, Chen SA, Khosla NM, Smith JD, Pritchard JK, Fraser HB . 2018 Functional genetic variants revealed by massively parallel precise genome editing. Cell 175, 544-557. (doi:10.1016/j.cell.2018.08.057) Crossref, PubMed, Web of Science, Google Scholar - 40.
Rosen MJ, Davison M, Fisher DS, Bhaya D . 2018 Probing the ecological and evolutionary history of a thermophilic cyanobacterial population via statistical properties of its microdiversity. PLoS ONE 13, e0205396. (doi:10.1371/journal.pone.0205396) Crossref, PubMed, Web of Science, Google Scholar - 41.
Baliga C, Majhi S, Mondal K, Bhattacharjee A, VijayRaghavan K, Varadarajan R . 2016 Rational elicitation of cold-sensitive phenotypes. Proc. Natl Acad. Sci. USA 113, E2506-E2515. (doi:10.1073/pnas.1604190113) Crossref, PubMed, Web of Science, Google Scholar - 42.
Ben-Aroya S, Coombes C, Kwok T, O'Donnell KA, Boeke JD, Hieter P . 2008 Toward a comprehensive temperature-sensitive mutant repository of the essential genes of Saccharomyces cerevisiae. Mol. Cell 30, 248-258. (doi:10.1016/j.molcel.2008.02.021) Crossref, PubMed, Web of Science, Google Scholar - 43.
Li Z 2011 Systematic exploration of essential yeast gene function with temperature-sensitive mutants. Nat. Biotechnol. 29, 361-367. (doi:10.1038/nbt.1832) Crossref, PubMed, Web of Science, Google Scholar - 44.
Moir D, Stewart SE, Osmond BC, Botstein D . 1982 Cold-sensitive cell-division-cycle mutants of yeast: isolation, properties, and pseudoreversion studies. Genetics 100, 547-563. (doi:10.1093/genetics/100.4.547) Crossref, PubMed, Web of Science, Google Scholar - 45.
Berger D, Stangberg J, Baur J, Walters RJ . 2021 Elevated temperature increases genome-wide selection on de novo mutations. Proc. Biol. Sci. 288, 20203094. (doi:10.1098/rspb.2020.3094) Link, Web of Science, Google Scholar - 46.
Davenport ES, Agrelius TC, Harmon KB, Dudycha JL . 2021 Fitness effects of spontaneous mutations in a warming world. Evolution 75, 1513-1524. (doi:10.1111/evo.14208) Crossref, PubMed, Web of Science, Google Scholar - 47.
Kumar S, Nussinov R . 2001 How do thermophilic proteins deal with heat? Cell. Mol. Life Sci. 58, 1216-1233. (doi:10.1007/Pl00000935) Crossref, PubMed, Web of Science, Google Scholar - 48.
Luke KA, Higgins CL, Wittung-Stafshedel P . 2007 Thermodynamic stability and folding of proteins from hyperthermophilic organisms. FEBS J. 274, 4023-4033. (doi:10.1111/j.1742-4658.2007.05955.x) Crossref, PubMed, Google Scholar - 49.
Cherry JL . 2010 Highly expressed and slowly evolving proteins share compositional properties with thermophilic proteins. Mol. Biol. Evol. 27, 735-741. (doi:10.1093/molbev/msp270) Crossref, PubMed, Web of Science, Google Scholar - 50.
Paradis E, Claude J, Strimmer K . 2004 APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290. (doi:10.1093/bioinformatics/btg412) Crossref, PubMed, Web of Science, Google Scholar - 51.
Kumar S, Suleski M, Craig JM, Kasprowicz AE, Sanderford M, Li M, Stecher G, Hedges SB . 2022 TimeTree 5: an expanded resource for species divergence times. Mol. Biol. Evol. 39, msac174. (doi:10.1093/molbev/msac174) Crossref, PubMed, Web of Science, Google Scholar - 52.
Parks DH, Chuvochina M, Rinke C, Mussig AJ, Chaumeil PA, Hugenholtz P . 2022 GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Nucleic Acids Res. 50, D785-D794. (doi:10.1093/nar/gkab776) Crossref, PubMed, Web of Science, Google Scholar - 53.
Sievers F 2011 Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539. (doi:10.1038/msb.2011.75) Crossref, PubMed, Web of Science, Google Scholar - 54.
Yang Z . 1997 PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555-556. PubMed, Google Scholar - 55.
Yang J.R., Zhuang S.M, Zhang J . 2010 Impact of translational error-induced and error-free misfolding on the rate of protein evolution. Mol. Syst. Biol. 6, 421. (doi:10.1038/msb.2010.78) Crossref, PubMed, Web of Science, Google Scholar - 56.
Liu H, Sun M, Zhang J . 2023Genomic estimates of mutation and substitution rates contradict the evolutionary speed hypothesis of the latitudinal diversity gradient . Figshare. (doi:10.6084/m9.figshare.c.6877871) Google Scholar
