Evolution of the cytochromeb gene of mammals
Abstract
With the polymerase chain reaction (PCR) and versatile primers that amplify the whole cytochrome b gene (approximately 1140 bp), we obtained 17 complete gene sequences representing three orders of hoofed mammals (ungulates) and dolphins (cetaceans). The fossil record of some ungulate lineages allowed estimation of the evolutionary rates for various components of the cytochrome b DNA and amino acid sequences. The relative rates of substitution at first, second, and third positions within codons are in the ratio 10 to 1 to at least 33. For deep divergences (greater than 5 million years) it appears that both replacements and silent transversions in this mitochondrial gene can be used for phylogenetic inference. Phylogenetic findings include the association of (1) cetaceans, artiodactyls, and perissodactyls to the exclusion of elephants and humans, (2) pronghorn and fallow deer to the exclusion of bovids (i.e., cow, sheep, and goat), (3) sheep and goat to the exclusion of other pecorans (i.e., cow, giraffe, deer, and pronghorn), and (4) advanced ruminants to the exclusion of the chevrotain and other artiodactyls. Comparisons of these cytochrome b sequences support current structure-function models for this membrane-spanning protein. That part of the outer surface which includes the Qo redox center is more constrained than the remainder of the molecule, namely, the transmembrane segments and the surface that protrudes into the mitochondrial matrix. Many of the amino acid replacements within the transmembrane segments are exchanges between hydrophobic residues (especially leucine, isoleucine, and valine). Replacement changes at first and second positions of codons approximate a negative binomial distribution, similar to other protein-coding sequences. At four-fold degenerate positions of codons, the nucleotide substitutions approximate a Poisson distribution, implying that the underlying mutational spectrum is random with respect to position.
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The Tragulidae are universally designated as the extant sister group of the pecoran artiodactyls, according to both morphological and molecular data.
“The Tragulidae are universally designated as the extant sister group of the pecoran artiodactyls, according to both morphological (Gentry and Hooker 1988) and molecular data (Irwin et al. 199 1) .”
From Phylogeny of the Bovidae (Artiodactyla, Mammalia), based on mitochondrial ribosomal DNA sequences. (1992) · cites this paper as Irwin et al. 1991
Monophyly of the Bovidae is questionable.
“Several analyses of our data show that monophyly of the Bovidae, which was weakly supported by previous morphological and molecular work, is questionable.”
From Phylogeny of the Bovidae (Artiodactyla, Mammalia), based on mitochondrial ribosomal DNA sequences. (1992) · cites this paper as Irwin et al. 1991
A paraphyletic status for the Bovidae has been presented three times in the literature.
“In fact, a paraphyletic status has been presented three times in the literature (Miyamoto and Goodman 1986;Irwin et al. 199 1;Kraus and Miyamoto 199 1) .”
From Phylogeny of the Bovidae (Artiodactyla, Mammalia), based on mitochondrial ribosomal DNA sequences. (1992) · cites this paper as Irwin et al. 1991
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“For some of the hair and blood samples that were too degraded for the amplification of the entire cytochrome b gene, we performed partial amplifications using L14724 and H15149 (480 bp) (Irwin et al., 1991), and a set of newly designed primers CYTB FAR-L 50-CCATGAGGACAAATATCATTCTGAT-30 and CYTB FAR-H 50-TCCAATAGTAATAA…”
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“Coincidently, it was also the case just in consideration of the third codon of the cytb gene in the bear species, which had been previously reported by Talbot and Shields (1996a,b) [6% Myr of ursids vs 10% Myr of other mammalian species ( Irwin et al., 1991 )].”
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“The entire cytochrome b gene (1.1 kb) was PCR ampliWed with primers GLuDG.L-TGA CTT GAA RAA CCA YCG TTG (Palumbi et al., 1991) and H15915-AAC TGC CAG TCA TCT CCG GGT TAC AAG AC ( Irwin et al., 1991 ).”
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“To mimic a typical mammalian evolutionary study, we amplified the mitochondrial cytochrome-b gene using the universal primers L14724/H15915 (Irwin et al. 1991).”
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“We amplified an ≈800-bp fragment of mitochondrial cytochrome b using primers cytb-L14724 (forward) and cytb-H15506 (reverse) (11,39,40).”
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“the primer pairs L14724/H15149 and C3/H15915 (Irwin et al., 1991; Dubey et al., 2006), and that of the 16S ribosomal sequence”
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“Among the various mtDNA genes, the cytochrome b gene appeared as the most suitable marker for vertebrate identification, particularly in such degraded samples, because it exhibits both large regions of interspecies sequence diversity with low or no intraspecific variation, and several conserved regions allowing the am…”
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“Initially, the universal primers L14724 and H15915 (Irwin et al., 1991) were used to amplify the entire cytochrome b gene by PCR (Saiki et al.”
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“Saturation analyses (Brown et al., 1982; Griffths, 1997; Irwin et al., 1991 ) were conducted in order to determine whether excessive homoplasy resulting from multiple hits was likely to cause divergence dates to be underestimated.”
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“The cytochrome b region of mtDNA was amplified by the polymerase chain reaction (PCR) on samples using a pair of L14724B and H15915R primers described by Irwin et al. (1991) .”
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“We assessed species limits using a broad geographic sample of DNA sequences from the mitochondrial gene cytochrome b in conjunction with morphological character analysis, and we inferred phylogenetic relationships among species using the cytochrome-b dataset in addition to sequences from the mitochondrial genes cytoch…”
BackgroundInfluentialLiu, X., Wei, F., Li, M., Jiang, X., Feng, Z., & Jin-chu, H. (2004) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2004.05.011 · Cited by 72 · see citing works
“In order to obtain the complete sequence of cyt b gene, an approximately 800bp region of the cyt b gene was also amplified using internal primer L15162 (Irwin et al., 1991) and H15915.”
BackgroundMethodInfluentialNicolas, V., Querouil, S., Verheyen, E., Verheyen, W., Mboumba, J., Dillen, M., & Colyn, M. (2006) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2005.11.024 · Cited by 73
“As previously observed (e.g., Hassanin and Douzery, 1999; Irwin et al., 1991), the highest levels of homoplasy and saturation are observed at third codon positions, for which almost all Ti and most Tv are synonymous.”
ResultMiller-Butterworth, C., Eick, G., Jacobs, D., Schoeman, M. C., & Harley, E. H. (2005) · Journal of Mammalogy · doi:10.1644/05-mamm-a-021r1.1 · Cited by 73 · see citing works
“A 604-base pair (bp) fragment of the mitochondrial Cytb gene was amplified and sequenced in representative accessions or voucher specimens of 33 Miniopterus and 2 outgroup taxa (Appendix I) using primers L14724 and H15275 (Irwin et al. 1991).”
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Bužan, E., Kryštufek, B., Hänfling, B., & Hutchinson, W. (2008) · doi:10.1111/j.1095-8312.2008.01024.x · Cited by 72
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PHYLOGENETICS OF SMALL HORSESHOE BATS FROM EAST ASIA BASED ON MITOCHONDRIAL DNA SEQUENCE VARIATION
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Forensic genetic analysis of insect gut contents.
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Unexpected evolutionary diversity in a recently extinct Caribbean mammal radiation
Brace, S., Turvey, S., Weksler, M., Hoogland, M., & Barnes, I. (2015) · Proceedings of the Royal Society of London. Biological Sciences · doi:10.1098/rspb.2014.2371 · Cited by 69
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Smith, D. A., Ralls, K., Hurt, A., Adams, B., Parker, M., & Maldonado, J. E. (2006) · Molecular Ecology · doi:10.1111/j.1365-294x.2005.02841.x · Cited by 68
“1997) and a universal heavy STRAND primer (H15915, Irwin et al. 1991) in a 50- µ L PCR including 0.5 U Ampli Taq Gold (PerkinElmer), 2.5 m m MgCl 2 , 1 × reaction buffer (PerkinElmer) 200 µ m each dNTP, 1.0 mg/mL Fraction-V BSA, and 1 µ m each primer.”
MethodInfluentialCarroll, D., Mills, J., Montgomery, J., Bausch, D., Blair, P., Burans, J., Felices, V., Gianella, A., Iihoshi, N., Nichol, S., et al. (2005) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2005.72.42 · Cited by 68 · see citing works
Brändli, L., Handley, L., Vogel, P., & Perrin, N. (2005) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2005.06.019 · Cited by 67 · see citing works
“a Fumagalli et al. (1996) . b Kocher et al. (1989) . d Irwin et al. (1991) . e Matsubara et al. (2001) . f Hellborg and Ellegren (2003) . Locus Size Accession Forward primer Reverse primer T”
BackgroundWu, C., Wu, J.-P., Bunch, T., Li, Q.-W., Wang, Y.-X., & Zhang, Y.-P. (2005) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2005.05.006 · Cited by 67 · see citing works
“The entire mitochondrial cytb gene was amplified and sequenced using universal primers L14724 and H15915 (Irwin et al., 1991) and L14841 and H15149 (Kocher et al., 1989).”
BackgroundMethodInfluentialIvory identification by DNA profiling of cytochrome b gene
Lee, J. C.-I., Hsieh, H.-M., Huang, L.-H., Kuo, Y.-C., Wu, J.-H., Chin, S.-C., Lee, A.-H., Linacre, A., & Tsai, L. (2009) · Zeitschrift für Rechtsmedizin · doi:10.1007/s00414-008-0264-0 · Cited by 66
“[21].”
Vallo, P., Guillén-Servent, A., Benda, P., Pires, D., & Koubek, P. (2008) · doi:10.3161/150811008x414782 · Cited by 66
“Complete cytochrome b gene (cytb) was amplified by the polymerase chain reaction (PCR) using universal primers L14724 and H15915 (Irwin et al., 1991) or their slightly modified versions L14724ag and H15915ag (Guillén-Servent and Francis, 2006).”
MethodArellano, E., González-Cózatl, F. X., & Rogers, D. S. (2005) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2005.07.021 · Cited by 64 · see citing works
“Light strand internal primers used included 700L (5-CCC AGC ACA TAT TAA ACC AGA AT-3) (Peppers and Bradley, 2000), F1 (5-TGA GGA CAR ATA TCH TTY TGR GG) (Whiting et al., 2003), L15162 (5TCG YCT YCC ATG AGG RCA TAT ATC-3) ( Irwin et al., 1991 ), MVZ 45 (5-GTH ATA GCH ACA GCA TTY ATA GG-3) (Smith and Patton, 1993), MVZ…”
BackgroundMethodResultInfluentialDurbin, J., Funk, S., Hawkins, F., Hills, D., Jenkins, P., Moncrieff, C., & Ralainasolo, F. B. (2010) · Systematics and Biodiversity · doi:10.1080/14772001003756751 · Cited by 63 · see citing works
“Thus, we used a polymerase chain reaction (PCR) to amplify the whole cyt b gene using universal primers H15149 and L15146 ( Kocher et al. , 1989 ), H15915 and L14724 ( Irwin et al.”
MethodMusilová, Z., Říčan, O., Janko, K., & Novák, J. (2008) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2007.10.011 · Cited by 63 · see citing works
Li, M., Wei, F., Goossens, B., Feng, Z., Tamate, H., Bruford, M., & Funk, S. (2005) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2004.12.016 · Cited by 63
“Cyt b was amplified using the primer pairs L16457 (50-TGTACCTCTTCTCGCTCCGGG-30) and H16781 (50-TTATGTCCTGTG-ACCATTGACTG A-30) and L14724 (50-GATATGAAAACCCATCGTT G-30; Irwin et al., 1991) and H15149 (50-CTCAGAATG ATATTTGTCCTCA-30; Kocher et al.”
MethodAntitropicality of Pacific Fishes: Molecular Insights
Burridge, C. (2002) · Environmental Biology of Fishes · doi:10.1023/a:1020040515980 · Cited by 63 · see citing works
“Application of a third codon higher vertebrate clock calibration of 10% divergence per million years ( Irwin et al. 1991 ) suggests 0.2–0.3 My isolation (Grant et al. 1998), while the calibrations of Martin et al. (1992) and Bermingham et al. (1997) suggest divergence 0.6–1.3 Mya.”
BackgroundInfluentialAnalysis of directional mutation pressure and nucleotide content in mitochondrial cytochrome b genes
Jermiin, L., Graur, D., Lowe, R. M., & Crozier, R. (1994) · Journal of Molecular Evolution · doi:10.1007/bf00163805 · Cited by 63 · see citing works
Genetic analyses reveal further cryptic lineages within the Myotis nattereri species complex
Puechmaille, S. J., Allegrini, B., Boston, E. S. M., Dubourg-Savage, M., Evin, A., Knochel, A., Bris, Y. L., Lecoq, V., Lemaire, M., Rist, D., et al. (2012) · doi:10.1016/j.mambio.2011.11.004 · Cited by 62
Kokita, T., & Nohara, K. (2011) · Molecular Ecology · doi:10.1111/j.1365-294x.2010.04920.x · Cited by 62
“A fragment containing complete region (c. 1141 bp) of mitochondrial cytochrome b gene (cyt b) was amplified using Gludg-L (5¢-TGACTTGAARAACCAYCGTTG-3¢) (Palumbi et al. 1991) and H15915 (5¢-AACTGCAGTCATCTCCGGTTTACAAGAC-3¢) (Irwin et al. 1991).”
MethodBranch, L. C., Clark, A., Moler, P., & Bowen, B. W. (2003) · Conservation Genetics · doi:10.1023/a:1023398908793 · Cited by 62
“The strong genetic divergence (d = 8.4%) between the two oldest ridges – Lake Wales Ridge (E. e. lividus) and Mt. Dora Ridge (E. e. onocrepis) – suggests a separation of approximately 4 MY based on conventional estimates of molecular evolutionary rates for cytochrome b ( Irwin et al. 1991 ), a time frame that overlaps…”
BackgroundInfluentialCRYPTIC SPECIES IN AN INSECTIVOROUS BAT, SCOTOPHILUS DINGANII
Jacobs, D., Eick, G., Schoeman, M. C., & Matthee, C. (2006) · doi:10.1644/04-mamm-a-132r2.1 · Cited by 61
“A 604-base pari (bp) fragment of the mitochondrial Cytb gene was amplified using primers L14724 and H15275 (Irwin et al. 1991).”
MethodKasapidis, P., Peristeraki, P., Tserpes, G., & Magoulas, A. (2007) · doi:10.3391/ai.2007.2.1.9 · Cited by 61
“Amplification was carried out using the universal primers CB2H (Kocher et al. 1989) and L14724 (Irwin et al. 1991).”
MethodTakada, T., Kikkawa, Y., Yonekawa, H., Kawakami, S., & Amano, T. (1997) · Biochemical Genetics · doi:10.1023/a:1021869704889 · Cited by 60 · see citing works
“To investigate the relationships among wild and domestic goats, we chose the mitochondrial cytochrome b gene ( Irwin et al., 1991 ) and the mitochondrial displacement loop (D-loop) region as phylogenetic probes, because the complete sequences from other ungulates are now fully available.”
MethodNovel primers for complete mitochondrial cytochrome b gene sequencing in mammals
Naidu, A., Fitak, R., Munguía-Vega, A., & Culver, M. (2012) · Molecular Ecology Resources · doi:10.1111/j.1755-0998.2011.03078.x · Cited by 59
“The primers described by Irwin et al. (1991) amplify the entire cyt b but were tested in a limited set of mammalian species.”
BackgroundMethodDNA typing in wildlife crime: recent developments in species identification
Tobe, S. S., & Linacre, A. (2010) · Forensic Science, Medicine, and Pathology · doi:10.1007/s12024-010-9168-7 · Cited by 59
“There is a range of universal primer sets for mammalian species, such that a sample from any mammalian species will generate the same size product after amplification using the polymerase chain reaction (PCR) [62, 63, 71, 79, 81–83].”
BackgroundMethodden Tex, R.-J., Thorington, R., Maldonado, J., & Leonard, J. (2010) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2009.12.023 · Cited by 58
“DNA was extracted by phenol–chloroform and concentrated in Centricons as in Leonard et al. (2005) or by DNeasy animal tissue and blood extraction kit (Qiagen, Hilden, Germany) following the animal tissue protocol.”
MethodPiaggio, A. J., & Perkins, S. L. (2005) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2005.03.029 · Cited by 50 · see citing works
High-latitude diversification within Eurasian least shrews and Alaska tiny shrews (Soricidae)
Hope, A., Waltari, E., Dokuchaev, N., Abramov, S., Dupal, T., Tsvetkova, A., Henttonen, H., Macdonald, S. O., & Cook, J. A. (2010) · Journal of Mammalogy · doi:10.1644/09-mamm-a-402.1 · Cited by 57 · see citing works
Finding Nemo: molecular phylogeny and evolution of the unusual life style of anemonefish.
Santini, S., & Polacco, G. (2006) · Gene · doi:10.1016/j.gene.2006.03.028 · Cited by 57 · see citing works
EVOLUTIONARY HISTORY OF THE ARCTIC GROUND SQUIRREL (SPERMOPHILUS PARRYII) IN NEARCTIC BERINGIA
Eddingsaas, A. A., Jacobsen, B., Lessa, E., & Cook, J. A. (2004) · Journal of Mammalogy · doi:10.1644/brb-204 · Cited by 57 · see citing works
“Starting parameters (base frequency A, 0.29; C, 0.26; G, 0.12; T, 0.33; substitution model Ti/Tv ¼ 10.22, Gamma ¼ 0.3791) are typical for mammalian Cytb (Irwin et al. 1991).”
BackgroundInfluentialOchoa, L., Roxo, F., Donascimiento, C., Sabaj, M., Datovo, A., Alfaro, M., & Oliveira, C. (2017) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2017.07.007 · Cited by 56
Multiple Co-infections of Rodents with Hantaviruses, Leptospira, and Babesia in Croatia
Tadin, A., Turk, N., Korva, M., Margaletić, J., Beck, R., Vucelja, M., Habuš, J., Svoboda, P., Županc, T. A., Henttonen, H., et al. (2012) · Vector Borne and Zoonotic Diseases · doi:10.1089/vbz.2011.0632 · Cited by 56
“A cytochrome b fragment was amplified using DNA isolated from Apodemus rodents using the primers L 14771 (5¢-CA ACATTCGTAAAACCCACC-3¢) and H 15149 (5¢-AAACTG CAGCCCCTCAGAATGATATTTGTCCTCA-3¢) (Irwin et al. 1991).”
MethodFlauzino, J., Nguyen, E., Yang, Q.-Y., Rosati, G., Panáček, D., Brito-Madurro, A. G., Madurro, J. M., Bakandritsos, A., Otyepka, M., & Merkoçi, A. (2021) · Biosensors & bioelectronics · doi:10.1016/j.bios.2021.113628 · Cited by 55 · see citing works
Lamb, J., Ralph, T. M. C., Goodman, S., Bogdanowicz, W., Fahr, J., Gajewska, M., Bates, P. J. J., Eger, J., Benda, P., & Taylor, P. (2008) · Acta Chiropterologica · doi:10.3161/150811008x331063 · Cited by 55 · see citing works
“For the majority of the samples, the cytochrome b gene was PCR-amplified (Saiki et al., 1988) as two overlapping double-stranded fragments using the following primer pairs: L 14723 (5’-ACC AATGCAATGAAAAATCATCGTT-3’) and H 15553 (5’- TAGGCAAATAGGAAATATCATTCTGGT-3’); L15146 (5’- CATGAGGACAAATATCATTCTGAG-3’) and H15915 (…”
BackgroundGomard, Y., Dietrich, M., Wieseke, N., Ramasindrazana, B., Lagadec, E., Goodman, S., Dellagi, K., & Tortosa, P. (2016) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiw037 · Cited by 53
Yannic, G., Basset, P., & Hausser, J. (2008) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2008.01.029 · Cited by 53
Sistemática, taxonomía y domesticación de alpacas y llamas: nueva evidencia cromosómica y molecular
Marin, J. C., Zapata, B., González, B. A., Bonacic, C., Wheeler, J. V., Casey, C., Bruford, M., Palma, R., Poulin, E., Alliende, M., et al. (2007) · doi:10.4067/s0716-078x2007000200001 · Cited by 53
“%) de todos los taxa, concordando con lo observado en otros mamíferos (Irwin et al. 1991).”
BackgroundŘíčan, O., & Kullander, S. (2006) · Journal of Zoological Systematics & Evolutionary Research = Zeitschrift für zoologische Systematik und Evolutionsforschung · doi:10.1111/j.1439-0469.2005.00347.x · Cited by 53
“L-TGA CTT GAA RAA CCA YCG TTG (Palumbi et al. 1991) and H15915-AAC TGC CAG TCA TCT CCG GGT TAC AAG AC (Irwin et al. 1991).”
BackgroundEvolutionary genetics of the suiformes as reconstructed using mtDNA sequencing
Randi, E., Lucchini, V., & Diong, C. H. (1996) · Journal of Mammalian Evolution · doi:10.1007/bf01454360 · Cited by 65 · see citing works
Goodman, S., Maminirina, C. P., Weyeneth, N., Bradman, H. M., Christidis, L., Ruedi, M., & Appleton, B. (2009) · doi:10.1111/j.1463-6409.2008.00377.x · Cited by 52
“The cyt-b gene was amplified and sequenced using the primers L14724 and H15915 (Irwin et al. 1991).”
Method
- Authors
- Irwin, D. M., Kocher, T. D., & Wilson, A. C.
- Affiliations
- University of California, Berkeley (US)
- Venue
- Journal of Molecular Evolution
- Published
- 1991-02
- Volume
- 32
- Issue
- 2
- Pages
- 128-144
- ISSN
- 0022-2844 (ISSN-L)
- 1432-1432
- OpenAlex
- W1491713847
- Cited by
- 2,315
- References
- 0
- Citations by year
- 2026: 37 · 2025: 44 · 2024: 56 · 2023: 74 · 2022: 51 · 2021: 63 · 2020: 60 · 2019: 57 · 2018: 55 · 2017: 50 · 2016: 58 · 2015: 64 · 2014: 86 · 2013: 84 · 2012: 69
- FWCI
- 86.05
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Journal of Molecular Evolution (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Keywords
- cytochrome b, mitochondrial DNA, ungulates, cetaceans, molecular evolution rate, phylogenetic inference, mammalian phylogeny, transmembrane helices, mutation spectrum, structural-functional model, pronghorn, fallow deer, Bovidae, Artiodactyla, perissodactyls, chevrotains
- MeSH terms
- Amino Acid Sequence, Animals, Base Composition, Base Sequence, Cytochrome b Group, DNA, Biological Evolution, Humans, Mammals, Molecular Sequence Data, Mutation, Phylogeny, Sequence Homology, Nucleic Acid, Time Factors, Genetic Variation, Polymerase Chain Reaction
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