Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics

Reconstruction of body mass evolution in the Cetartiodactyla and mammals using phylogenomic data

10.24072/pcjournal.55 - Peer Community Journal, Volume 1 (2021), article no. e42.

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Reconstructing ancestral characters on a phylogeny is an arduous task because the observed states at the tips of the tree correspond to a single realization of the underlying evolutionary process. Recently, it was proposed that ancestral traits can be indirectly estimated with the help of molecular data, based on the fact that life history traits influence substitution rates. Here we challenge these new approaches in the Cetartiodactyla, a clade of large mammals which, according to paleontology, derive from small ancestors. Analysing transcriptome data in 41 species, of which 22 were newly sequenced, we provide a dated phylogeny of the Cetartiodactyla and report a significant effect of body mass on the overall substitution rate, the synonymous vs. non-synonymous substitution rate and the dynamics of GC-content. Our molecular comparative analysis points toward relatively small Cetartiodactyla ancestors, in agreement with the fossil record, even though our data set almost exclusively consists of large species. This analysis demonstrates the potential of phylogenomic methods for ancestral trait reconstruction and gives credit to recent suggestions that the ancestor to placental mammals was a relatively large and long-lived animal.

Published online:
DOI: 10.24072/pcjournal.55
Type: Research article
Figuet, Emeric 1; Ballenghien, Marion 2; Lartillot, Nicolas 3; Galtier, Nicolas 1

1 ISEM, Univ Montpellier, CNRS, IRD, Montpellier, France
2 Adaptation et Diversité en Milieu Marin, UMR7144, CNRS, Université Pierre et Marie Curie, Sorbonne Universités, Station Biologique de Roscoff, France
3 Laboratoire de Biométrie et Biologie Evolutive, UMR 5558, CNRS, Université Claude Bernard Lyon 1, Villeurbanne, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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Figuet, Emeric; Ballenghien, Marion; Lartillot, Nicolas; Galtier, Nicolas. Reconstruction of body mass evolution in the Cetartiodactyla and mammals using phylogenomic data. Peer Community Journal, Volume 1 (2021), article  no. e42. doi : 10.24072/pcjournal.55. https://peercommunityjournal.org/articles/10.24072/pcjournal.55/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100042

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Agnarsson, I.; May-Collado, L. J. The phylogeny of Cetartiodactyla: The importance of dense taxon sampling, missing data, and the remarkable promise of cytochrome b to provide reliable species-level phylogenies, Molecular Phylogenetics and Evolution, Volume 48 (2008) no. 3, pp. 964-985 | DOI

[2] Archibald, J. D.; Averianov, A. O.; Ekdale, E. G. Late Cretaceous relatives of rabbits, rodents, and other extant eutherian mammals, Nature, Volume 414 (2001) no. 6859, pp. 62-65 | DOI

[3] Asher, R. J.; Meng, J.; Wible, J. R.; McKenna, M. C.; Rougier, G. W.; Dashzeveg, D.; Novacek, M. J. Stem Lagomorpha and the Antiquity of Glires, Science, Volume 307 (2005) no. 5712, pp. 1091-1094 | DOI

[4] Beaulieu, J. M.; Jhwueng, D.-C.; Boettiger, C.; O’Meara, B. C. Modeling stabilizing selection: expanding the ornstein-uhlenbeck model of adaptive evolution, Evolution, Volume 66 (2012) no. 8, pp. 2369-2383 | DOI

[5] Bokma, F.; Godinot, M.; Maridet, O.; Ladevèze, S.; Costeur, L.; Solé, F.; Gheerbrant, E.; Peigné, S.; Jacques, F.; Laurin, M. Testing for Depéret's Rule (Body Size Increase) in Mammals using Combined Extinct and Extant Data, Systematic Biology, Volume 65 (2016) no. 1, pp. 98-108 | DOI

[6] Bromham, L. Molecular Clocks in Reptiles: Life History Influences Rate of Molecular Evolution, Molecular Biology and Evolution, Volume 19 (2002) no. 3, pp. 302-309 | DOI

[7] Bromham, L.; Rambaut, A.; Harvey, P. H. Determinants of rate variation in mammalian DNA sequence evolution, Journal of Molecular Evolution, Volume 43 (1996) no. 6, pp. 610-621 | DOI

[8] Cahais, V.; Gayral, P.; Tsagkogeorga, G.; Melo‐Ferreira, J.; Ballenghien, M.; Weinert, L.; Chiari, Y.; Belkhir, K.; Ranwez, V.; Galtier, N. Reference‐free transcriptome assembly in non‐model animals from next‐generation sequencing data, Molecular Ecology Resources, Volume 12 (2012) no. 5, pp. 834-845 | DOI

[9] Choi, J.-W.; Chung, W.-H.; Lee, K.-T.; Cho, E.-S.; Lee, S.-W.; Choi, B.-H.; Lee, S.-H.; Lim, W.; Lim, D.; Lee, Y.-G.; Hong, J.-K.; Kim, D.-W.; Jeon, H.-J.; Kim, J.; Kim, N.; Kim, T.-H. Whole-genome resequencing analyses of five pig breeds, including Korean wild and native, and three European origin breeds, DNA Research, Volume 22 (2015) no. 4, pp. 259-267 | DOI

[10] Cunningham, C. W.; Omland, K. E.; Oakley, T. H. Reconstructing ancestral character states: a critical reappraisal, Trends in Ecology & Evolution, Volume 13 (1998) no. 9, pp. 361-366 | DOI

[11] Damuth, J. Interspecific allometry of population density in mammals and other animals: the independence of body mass and population energy-use, Biological Journal of the Linnean Society, Volume 31 (1987) no. 3, pp. 193-246 | DOI

[12] Damuth, J. Population density and body size in mammals, Nature, Volume 290 (1981) no. 5808, pp. 699-700 | DOI

[13] Donoghue, M. J. Phylogenies and the Analysis of Evolutionary Sequences, with Examples From Seed Plants, Evolution, Volume 43 (1989) no. 6 | DOI

[14] Duret, L.; Galtier, N. Biased Gene Conversion and the Evolution of Mammalian Genomic Landscapes, Annual Review of Genomics and Human Genetics, Volume 10 (2009) no. 1, pp. 285-311 | DOI

[15] Dutheil, J.; Boussau, B. Non-homogeneous models of sequence evolution in the Bio++ suite of libraries and programs, BMC Evolutionary Biology, Volume 8 (2008) no. 1 | DOI

[16] Dutheil, J. Y.; Galtier, N.; Romiguier, J.; Douzery, E. J.; Ranwez, V.; Boussau, B. Efficient Selection of Branch-Specific Models of Sequence Evolution, Molecular Biology and Evolution, Volume 29 (2012) no. 7, pp. 1861-1874 | DOI

[17] Feldhamer, G. A.; Drickamer, L. C.; Vessey, S. H.; Merritt, J. F.; Krajewski, C. Mammalogy: Adaptation, Diversity, Ecology, JHU Press, 2007

[18] Felsenstein, J. Phylogenies and the Comparative Method, The American Naturalist, Volume 125 (1985) no. 1, pp. 1-15 | DOI

[19] Figuet, E.; Nabholz, B.; Bonneau, M.; Mas Carrio, E.; Nadachowska-Brzyska, K.; Ellegren, H.; Galtier, N. Life History Traits, Protein Evolution, and the Nearly Neutral Theory in Amniotes, Molecular Biology and Evolution, Volume 33 (2016) no. 6, pp. 1517-1527 | DOI

[20] Figuet, E.; Romiguier, J.; Dutheil, J. Y.; Galtier, N. Mitochondrial DNA as a tool for reconstructing past life-history traits in mammals, Journal of Evolutionary Biology, Volume 27 (2014) no. 5, pp. 899-910 | DOI

[21] Galtier, N.; Gouy, M. Inferring pattern and process: maximum-likelihood implementation of a nonhomogeneous model of DNA sequence evolution for phylogenetic analysis, Molecular Biology and Evolution, Volume 15 (1998) no. 7, pp. 871-879 | DOI

[22] Galtier, N.; Piganeau, G.; Mouchiroud, D.; Duret, L. GC-Content Evolution in Mammalian Genomes: The Biased Gene Conversion Hypothesis, Genetics, Volume 159 (2001) no. 2, pp. 907-911 | DOI

[23] Goswami, A.; Prasad, G. V. R.; Upchurch, P.; Boyer, D. M.; Seiffert, E. R.; Verma, O.; Gheerbrant, E.; Flynn, J. J. A radiation of arboreal basal eutherian mammals beginning in the Late Cretaceous of India, Proceedings of the National Academy of Sciences, Volume 108 (2011) no. 39, pp. 16333-16338 | DOI

[24] Groussin, M.; Gouy, M. Adaptation to Environmental Temperature Is a Major Determinant of Molecular Evolutionary Rates in Archaea, Molecular Biology and Evolution, Volume 28 (2011) no. 9, pp. 2661-2674 | DOI

[25] Hahn, M. W.; Nakhleh, L. Irrational exuberance for resolved species trees, Evolution, Volume 70 (2016) no. 1, pp. 7-17 | DOI

[26] Hassanin, A.; Delsuc, F.; Ropiquet, A.; Hammer, C.; Jansen van Vuuren, B.; Matthee, C.; Ruiz-Garcia, M.; Catzeflis, F.; Areskoug, V.; Nguyen, T. T.; Couloux, A. Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes, Comptes Rendus Biologies, Volume 335 (2012) no. 1, pp. 32-50 | DOI

[27] Heim, N. A.; Knope, M. L.; Schaal, E. K.; Wang, S. C.; Payne, J. L. Cope's rule in the evolution of marine animals, Science, Volume 347 (2015) no. 6224, pp. 867-870 | DOI

[28] Hooker, J. J.; Thomas, K. M. A New Species of Amphirhagatherium (Choeropotamidae, Artiodactyla, Mammalia) from the Late Eocene Headon Hill Formation of Southern England and Phylogeny of Endemic European 'anthracotherioids', Palaeontology, Volume 44 (2001) no. 5, pp. 827-853 | DOI

[29] Horvilleur, B.; Lartillot, N. Monte Carlo algorithms for Brownian phylogenetic models, Bioinformatics, Volume 30 (2014) no. 21, pp. 3020-3028 | DOI

[30] Hunt, G. Fitting and comparing models of phyletic evolution: random walks and beyond, Paleobiology, Volume 32 (2006) no. 4, pp. 578-601 | DOI

[31] Jones, K. E.; Bielby, J.; Cardillo, M.; Fritz, S. A.; O'Dell, J.; Orme, C. D. L.; Safi, K.; Sechrest, W.; Boakes, E. H.; Carbone, C.; Connolly, C.; Cutts, M. J.; Foster, J. K.; Grenyer, R.; Habib, M.; Plaster, C. A.; Price, S. A.; Rigby, E. A.; Rist, J.; Teacher, A.; Bininda-Emonds, O. R. P.; Gittleman, J. L.; Mace, G. M.; Purvis, A. PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals, Ecology, Volume 90 (2009) no. 9, p. 2648-2648 | DOI

[32] Kardos, M.; Luikart, G.; Bunch, R.; Dewey, S.; Edwards, W.; McWilliam, S.; Stephenson, J.; Allendorf, F. W.; Hogg, J. T.; Kijas, J. Whole‐genome resequencing uncovers molecular signatures of natural and sexual selection in wild bighorn sheep, Molecular Ecology, Volume 24 (2015) no. 22, pp. 5616-5632 | DOI

[33] Lartillot, N. Phylogenetic Patterns of GC-Biased Gene Conversion in Placental Mammals and the Evolutionary Dynamics of Recombination Landscapes, Molecular Biology and Evolution, Volume 30 (2013) no. 3, pp. 489-502 | DOI

[34] Lartillot, N.; Delsuc, F. Joint reconstruction of divergence times and life-history evolution in placental mammals using a phylogenetic covariance model, Evolution, Volume 66 (2012) no. 6, pp. 1773-1787 | DOI

[35] Lartillot, N.; Poujol, R. A Phylogenetic Model for Investigating Correlated Evolution of Substitution Rates and Continuous Phenotypic Characters, Molecular Biology and Evolution, Volume 28 (2011) no. 1, pp. 729-744 | DOI

[36] Li, L.; Stoeckert, C. J.; Roos, D. S. OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes, Genome Research, Volume 13 (2003) no. 9, pp. 2178-2189 | DOI

[37] Lourenço, J. M.; Glémin, S.; Chiari, Y.; Galtier, N. The determinants of the molecular substitution process in turtles, Journal of Evolutionary Biology, Volume 26 (2013) no. 1, pp. 38-50 | DOI

[38] Lynch, M. The origins of genome architecture, Sinauer Associates Inc., Sunderland, MA, 2007

[39] De Magalhães, J. P.; Costa, J. A database of vertebrate longevity records and their relation to other life‐history traits, Journal of Evolutionary Biology, Volume 22 (2009) no. 8, pp. 1770-1774 | DOI

[40] Martin, A. P.; Palumbi, S. R. Body size, metabolic rate, generation time, and the molecular clock., Proceedings of the National Academy of Sciences, Volume 90 (1993) no. 9, pp. 4087-4091 | DOI

[41] McKenna, M. C.; Bell, S. K. Classification of Mammals above the Species Level, Columbia University Press, New York, 1997

[42] Mendes, F. K.; Hahn, Y.; Hahn, M. W. Gene Tree Discordance Can Generate Patterns of Diminishing Convergence over Time, Molecular Biology and Evolution, Volume 33 (2016) no. 12, pp. 3299-3307 | DOI

[43] Meredith, R. W.; Janecka, J. E.; Gatesy, J.; Ryder, O. A.; Fisher, C. A.; Teeling, E. C.; Goodbla, A.; Eizirik, E.; Simao, T. L. L.; Stadler, T.; Rabosky, D. L.; Honeycutt, R. L.; Flynn, J. J.; Ingram, C. M.; Steiner, C.; Williams, T. L.; Robinson, T. J.; Burk-Herrick, A.; Westerman, M.; Ayoub, N. A.; Springer, M. S.; Murphy, W. J. Impacts of the Cretaceous Terrestrial Revolution and KPg Extinction on Mammal Diversification, Science, Volume 334 (2011) no. 6055, pp. 521-524 | DOI

[44] Montgomery, S. H.; Geisler, J. H.; McGowen, M. R.; Fox, C.; Marino, L.; Gatesy, J. The evolutionary history of cetacean brain and body size, Evolution, Volume 67 (2013) no. 11, pp. 3339-3353 | DOI

[45] Murphy, W. J.; Pringle, T. H.; Crider, T. A.; Springer, M. S.; Miller, W. Using genomic data to unravel the root of the placental mammal phylogeny, Genome Research, Volume 17 (2007) no. 4, pp. 413-421 | DOI

[46] Nabholz, B.; Glemin, S.; Galtier, N. Strong Variations of Mitochondrial Mutation Rate across Mammals--the Longevity Hypothesis, Molecular Biology and Evolution, Volume 25 (2008) no. 1, pp. 120-130 | DOI

[47] Nery, M. F.; González, D. J.; Hoffmann, F. G.; Opazo, J. C. Resolution of the laurasiatherian phylogeny: Evidence from genomic data, Molecular Phylogenetics and Evolution, Volume 64 (2012) no. 3, pp. 685-689 | DOI

[48] Nikolaev, S. I.; Montoya-Burgos, J. I.; Popadin, K.; Parand, L.; Margulies, E. H.; Antonarakis, S. E. Life-history traits drive the evolutionary rates of mammalian coding and noncoding genomic elements, Proceedings of the National Academy of Sciences, Volume 104 (2007) no. 51, pp. 20443-20448 | DOI

[49] Nishihara, H.; Hasegawa, M.; Okada, N. Pegasoferae, an unexpected mammalian clade revealed by tracking ancient retroposon insertions, Proceedings of the National Academy of Sciences, Volume 103 (2006) no. 26, pp. 9929-9934 | DOI

[50] Oakley, T. H.; Cunningham, C. W. INDEPENDENT CONTRASTS SUCCEED WHERE ANCESTOR RECONSTRUCTION FAILS IN A KNOWN BACTERIOPHAGE PHYLOGENY, Evolution, Volume 54 (2000) no. 2 | DOI

[51] Ohta, T. Very slightly deleterious mutations and the molecular clock, Journal of Molecular Evolution, Volume 26 (1987) no. 1-2, pp. 1-6 | DOI

[52] Orliac, M. J.; Ducrocq, S. Eocene raoellids (Mammalia, Cetartiodactyla) outside the Indian Subcontinent: palaeogeographical implications, Geological Magazine, Volume 149 (2011) no. 1, pp. 80-92 | DOI

[53] Popadin, K.; Polishchuk, L. V.; Mamirova, L.; Knorre, D.; Gunbin, K. Accumulation of slightly deleterious mutations in mitochondrial protein-coding genes of large versus small mammals, Proceedings of the National Academy of Sciences, Volume 104 (2007) no. 33, pp. 13390-13395 | DOI

[54] Price, S. A.; Bininda-Emonds, O. R. P.; Gittleman, J. L. A complete phylogeny of the whales, dolphins and even-toed hoofed mammals (Cetartiodactyla), Biological Reviews, Volume 80 (2005) no. 03 | DOI

[55] Psouni, E.; Janke, A.; Garwicz, M. Impact of Carnivory on Human Development and Evolution Revealed by a New Unifying Model of Weaning in Mammals, PLoS ONE, Volume 7 (2012) no. 4 | DOI

[56] Ranwez, V.; Harispe, S.; Delsuc, F.; Douzery, E. J. P. MACSE: Multiple Alignment of Coding SEquences Accounting for Frameshifts and Stop Codons, PLoS ONE, Volume 6 (2011) no. 9 | DOI

[57] dos Reis, M.; Donoghue, P. C. J.; Yang, Z. Neither phylogenomic nor palaeontological data support a Palaeogene origin of placental mammals, Biology Letters, Volume 10 (2014) no. 1 | DOI

[58] dos Reis, M.; Inoue, J.; Hasegawa, M.; Asher, R. J.; Donoghue, P. C. J.; Yang, Z. Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny, Proceedings of the Royal Society B: Biological Sciences, Volume 279 (2012) no. 1742, pp. 3491-3500 | DOI

[59] Rolland, J.; Loiseau, O.; Romiguier, J.; Salamin, N. Molecular evolutionary rates are not correlated with temperature and latitude in Squamata: an exception to the metabolic theory of ecology?, BMC Evolutionary Biology, Volume 16 (2016) no. 1 | DOI

[60] Romiguier, J.; Figuet, E.; Galtier, N.; Douzery, E. J. P.; Boussau, B.; Dutheil, J. Y.; Ranwez, V. Fast and Robust Characterization of Time-Heterogeneous Sequence Evolutionary Processes Using Substitution Mapping, PLoS ONE, Volume 7 (2012) no. 3 | DOI

[61] Romiguier, J.; Ranwez, V.; Douzery, E. J.; Galtier, N. Contrasting GC-content dynamics across 33 mammalian genomes: Relationship with life-history traits and chromosome sizes, Genome Research, Volume 20 (2010) no. 8, pp. 1001-1009 | DOI

[62] Romiguier, J.; Ranwez, V.; Douzery, E.; Galtier, N. Genomic Evidence for Large, Long-Lived Ancestors to Placental Mammals, Molecular Biology and Evolution, Volume 30 (2013) no. 1, pp. 5-13 | DOI

[63] Ronquist, F.; Lartillot, N.; Phillips, M. J. Closing the gap between rocks and clocks using total-evidence dating, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 371 (2016) no. 1699 | DOI

[64] Rose, K. D. Skeleton of Diacodexis, oldest known Artiodactyl, Science, Volume 216 (1982) no. 4546, pp. 621-623 | DOI

[65] Springer, M. S.; Emerling, C. A.; Meredith, R. W.; Janečka, J. E.; Eizirik, E.; Murphy, W. J. Waking the undead: Implications of a soft explosive model for the timing of placental mammal diversification, Molecular Phylogenetics and Evolution, Volume 106 (2017), pp. 86-102 | DOI

[66] Scornavacca, C.; Galtier, N. Incomplete Lineage Sorting in Mammalian Phylogenomics, Systematic Biology, Volume 66 (2017) | DOI

[67] Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models, Bioinformatics, Volume 22 (2006) no. 21, pp. 2688-2690 | DOI

[68] Webster, M. T.; Smith, N. G. C.; Hultin-Rosenberg, L.; Arndt, P. F.; Ellegren, H. Male-Driven Biased Gene Conversion Governs the Evolution of Base Composition in Human Alu Repeats, Molecular Biology and Evolution, Volume 22 (2005) no. 6, pp. 1468-1474 | DOI

[69] White, E. P.; Ernest, S. M.; Kerkhoff, A. J.; Enquist, B. J. Relationships between body size and abundance in ecology, Trends in Ecology & Evolution, Volume 22 (2007) no. 6, pp. 323-330 | DOI

[70] Wible, J. R.; Rougier, G. W.; Novacek, M. J.; Asher, R. J. Cretaceous eutherians and Laurasian origin for placental mammals near the K/T boundary, Nature, Volume 447 (2007) no. 7147, pp. 1003-1006 | DOI

[71] Wible, J. R.; Rougier, G. W.; Novacek, M. J.; Asher, R. J. The Eutherian Mammal Maelestes gobiensis from the Late Cretaceous of Mongolia and the phylogeny of cretaceous eutheria, Bulletin of the American Museum of Natural History, Volume 2009 (2009) no. 327 | DOI

[72] Woolfit, M.; Bromham, L. Population size and molecular evolution on islands, Proceedings of the Royal Society B: Biological Sciences, Volume 272 (2005) no. 1578, pp. 2277-2282 | DOI

[73] Wu, H.; Guang, X.; Al-Fageeh, M. B.; Cao, J.; Pan, S.; Zhou, H.; Zhang, L.; Abutarboush, M. H.; Xing, Y.; Xie, Z.; Alshanqeeti, A. S.; Zhang, Y.; Yao, Q.; Al-Shomrani, B. M.; Zhang, D.; Li, J.; Manee, M. M.; Yang, Z.; Yang, L.; Liu, Y.; Zhang, J.; Altammami, M. A.; Wang, S.; Yu, L.; Zhang, W.; Liu, S.; Ba, L.; Liu, C.; Yang, X.; Meng, F.; Wang, S.; Li, L.; Li, E.; Li, X.; Wu, K.; Zhang, S.; Wang, J.; Yin, Y.; Yang, H.; Al-Swailem, A. M.; Wang, J. Camelid genomes reveal evolution and adaptation to desert environments, Nature Communications, Volume 5 (2014) no. 1 | DOI

[74] Wu, J.; Yonezawa, T.; Kishino, H. Rates of Molecular Evolution Suggest Natural History of Life History Traits and a Post-K-Pg Nocturnal Bottleneck of Placentals, Current Biology, Volume 27 (2017) no. 19 | DOI

[75] Yang, Z. PAML 4: Phylogenetic Analysis by Maximum Likelihood, Molecular Biology and Evolution, Volume 24 (2007) no. 8, pp. 1586-1591 | DOI

[76] Yim, H.-S.; Cho, Y. S.; Guang, X.; Kang, S. G.; Jeong, J.-Y.; Cha, S.-S.; Oh, H.-M.; Lee, J.-H.; Yang, E. C.; Kwon, K. K.; Kim, Y. J.; Kim, T. W.; Kim, W.; Jeon, J. H.; Kim, S.-J.; Choi, D. H.; Jho, S.; Kim, H.-M.; Ko, J.; Kim, H.; Shin, Y.-A.; Jung, H.-J.; Zheng, Y.; Wang, Z.; Chen, Y.; Chen, M.; Jiang, A.; Li, E.; Zhang, S.; Hou, H.; Kim, T. H.; Yu, L.; Liu, S.; Ahn, K.; Cooper, J.; Park, S.-G.; Hong, C. P.; Jin, W.; Kim, H.-S.; Park, C.; Lee, K.; Chun, S.; Morin, P. A.; O'Brien, S. J.; Lee, H.; Kimura, J.; Moon, D. Y.; Manica, A.; Edwards, J.; Kim, B. C.; Kim, S.; Wang, J.; Bhak, J.; Lee, H. S.; Lee, J.-H. Minke whale genome and aquatic adaptation in cetaceans, Nature Genetics, Volume 46 (2014) no. 1, pp. 88-92 | DOI

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