A multi-calibrated mitochondrial phylogeny of extant Bovidae (Artiodactyla, Ruminantia) and the importance of the fossil record to systematics

BMC Evolutionary Biology

Faysal Bibi¹ 

[1] Museum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin, Invalidenstrasse 43, Berlin 10115, Germany

关键词: Neogene;    Phylogenetic systematics;    Bayesian analysis;    Ruminantia;    Fossil calibration;   

Others  :  1086663
DOI  :  10.1186/1471-2148-13-166

 received in 2013-05-20, accepted in 2013-08-06,  发布年份 2013

【 摘 要 】

Background

Molecular phylogenetics has provided unprecedented resolution in the ruminant evolutionary tree. However, molecular age estimates using only one or a few (often misapplied) fossil calibration points have produced a diversity of conflicting ages for important evolutionary events within this clade. I here identify 16 fossil calibration points of relevance to the phylogeny of Bovidae and Ruminantia and use these, individually and together, to construct a dated molecular phylogeny through a reanalysis of the full mitochondrial genome of over 100 ruminant species.

Results

The new multi-calibrated tree provides ages that are younger overall than found in previous studies. Among these are young ages for the origin of crown Ruminantia (39.3–28.8 Ma), and crown Bovidae (17.3–15.1 Ma). These are argued to be reasonable hypotheses given that many basal fossils assigned to these taxa may in fact lie on the stem groups leading to the crown clades, thus inflating previous age estimates. Areas of conflict between molecular and fossil dates do persist, however, especially with regard to the base of the rapid Pecoran radiation and the sister relationship of Moschidae to Bovidae. Results of the single-calibrated analyses also show that a very wide range of molecular age estimates are obtainable using different calibration points, and that the choice of calibration point can influence the topology of the resulting tree. Compared to the single-calibrated trees, the multi-calibrated tree exhibits smaller variance in estimated ages and better reflects the fossil record.

Conclusions

The use of a large number of vetted fossil calibration points with soft bounds is promoted as a better approach than using just one or a few calibrations, or relying on internal-congruency metrics to discard good fossil data. This study also highlights the importance of considering morphological and ecological characteristics of clades when delimiting higher taxa. I also illustrate how phylogeographic and paleoenvironmental hypotheses inferred from a tree containing only extant taxa can be problematic without consideration of the fossil record. Incorporating the fossil record of Ruminantia is a necessary step for future analyses aiming to reconstruct the evolutionary history of this clade.

【 授权许可】

   
2013 Bibi; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Donoghue PCJ, Benton MJ: Rocks and clocks: calibrating the tree of life using fossils and molecules. Trends Ecol Evol 2007, 22:424-431.
• [2]Parham JF, Donoghue PCJ, Bell CJ, Calway TD, Head JJ, Holroyd PA, Inoue JG, Irmis RB, Joyce WG, Ksepka DT: Best practices for justifying fossil calibrations. Syst Biol 2012, 61:346-359.
• [3]Reisz RR, Müller J: Molecular timescales and the fossil record: a paleontological perspective. Trends Genet 2004, 20:237-241.
• [4]Graur D, Martin W: Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends Genet 2004, 20:80-86.
• [5]Müller J, Reisz RR: Four well-constrained calibration points from the vertebrate fossil record for molecular clock estimates. Bioessays 2005, 27:1069-1075.
• [6]Parham JF, Irmis RB: Caveats on the use of fossil calibrations for molecular dating: a comment on Near et al. Am Nat 2008, 171:132-136.
• [7]Bibi F, Vrba ES: Unraveling bovin phylogeny: accomplishments and challenges. BMC Biol 2010, 8:50. BioMed Central Full Text
• [8]Hassanin A, Delsuc F, Ropiquet A, Hammer C, Jansen van Vuuren B, Matthee C, Ruiz-Garcia M, Catzeflis F, Areskoug V, Nguyen TT, Couloux A: Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. C R Biol 2012, 335:32-50.
• [9]Spaulding M, O’Leary MA, Gatesy J: Relationships of Cetacea (Artiodactyla) among mammals: increased taxon sampling alters interpretations of key fossils and character evolution. PLoS ONE 2009, 4:e7062.
• [10]Hassanin A, Douzery EJP: Molecular and morphological phylogenies of Ruminantia and the alternative position of the Moschidae. Syst Biol 2003, 52:206-228.
• [11]Guha S, Goyal SP, Kashyap VK: Molecular phylogeny of musk deer: a genomic view with mitochondrial 16S rRNA and cytochrome b gene. Mol Phylogen Evol 2007, 42:585-597.
• [12]Gibbard PL, Head MJ, Walker MJ: Formal ratification of the quaternary system/period and the pleistocene series/epoch with a base at 2.58 Ma. J Quat Sci 2010, 25:96-102.
• [13]de Queiroz K: Toward an integrated system of clade names. Syst Biol 2007, 56:956-974.
• [14]O’Leary MA, Bloch JI, Flynn JJ, Gaudin TJ, Giallombardo A, Giannini NP, Goldberg SL, Kraatz BP, Luo Z-X, Meng J, et al.: The placental mammal ancestor and the post-K-Pg radiation of placentals. Science 2013, 339:662-667.
• [15]Nowak RM: Walker’s Mammals of the World, vol. 2. 6th edition. Baltimore, USA: Johns Hopkins University Press; 1999.
• [16]Vrba ES, Schaller G (Eds): Antelopes, Deer, and Relatives. New Haven: Yale University Press; 2000.
• [17]IUCN red list of threatened species 2012.2. [http://www.iucnredlist.org webcite. Accessed April 2013]
• [18]Heller R, Frandsen P, Lorenzen E, Siegismund H: Are there really twice as many bovid species as we thought? Syst Biol 2013.
• [19]Groves C, Grubb P: Ungulate Taxonomy. Baltimore: Johns Hopkins Univ; 2011.
• [20]Janis CM, Scott KM: The interrelationships of higher ruminant families with special emphasis on the members of the Cervoidea. Am Mus Novit 1987, 2893:1-85.
• [21]Gentry AW, Rössner GE, Heizmann EPJ: Suborder Ruminantia. In The Miocene Land Mammals of Europe. Edited by Rössner GE, Heissig K. Munich: Verlag Friedrich Pfeil; 1999:225-258.
• [22]Gradstein FM, Ogg JG, Smith AG: A Geologic Time Scale 2004. Cambridge: Cambridge University Press; 2004.
• [23]Solounias N, Barry JC, Bernor RL, Lindsay EH, Raza SM: The oldest bovid from the Siwaliks, Pakistan. J Vertebr Paleontol 1995, 15:806-814.
• [24]Agustí J, Cabrera L, Garces M, Krijgsman W, Oms O, Pares JM: A calibrated mammal scale for the Neogene of Western Europe. State of the art. Earth-Sci Rev 2001, 52:247-260.
• [25]Pilgrim GE: The fossil Bovidae of India. Palaeontol Indica 1939, NS 26:1-356.
• [26]Bibi F: Origin, paleoecology, and paleobiogeography of early Bovini. Palaeogeogr Palaeoclimatol Palaeoecol 2007, 248:60-72.
• [27]Bibi F: Evolution, Systematics, and Paleoecology of Bovinae (Mammalia: Artiodactyla) from the Late Miocene to the Recent. Yale University, Geology & Geophysics; 2009. [Ph.D. thesis]
• [28]Barry JC, Morgan ME, Flynn LJ, Pilbeam D, Behrensmeyer AK, Raza SM, Khan IA, Badgley C, Hicks J, Kelley J: Faunal and environmental change in the late Miocene Siwaliks of northern Pakistan. Paleobiology 2002, 28(S2):1-71.
• [29]Badgley C, Barry JC, Morgan ME, Nelson SV, Behrensmeyer AK, Cerling TE, Pilbeam D: Ecological changes in miocene mammalian record show impact of prolonged climatic forcing. Proc Natl Acad Sci 2008, 105:12145-12149.
• [30]Alcalá L, Morales J: A primitive caprine from the Upper Vallesian of La Roma 2 (Alfambra, Teruel, Aragón, Spain). Comptes Rendus de l’Académie des Sciences-Series IIA-Earth and Planetary Science 1997, 324:947-953.
• [31]Van Dam JA, Alcalá L, Zarza AA, Calvo JP, Garcés M, Krijgsman W: The upper miocene mammal record from the Teruel-Alfambra region (Spain). The MN system and continental stage/age concepts discussed. J Vertebr Paleontol 2001, 21:367-385.
• [32]Geraads D, Blondel C, Likius A, Mackaye HT, Vignaud P, Brunet M: New Hippotragini (Bovidae, Mammalia) from the late miocene of Toros-Menalla (Chad). J Vertebr Paleontol 2008, 28:231-242.
• [33]Lebatard AE, Bourles DL, Duringer P, Jolivet M, Brauchert R, Carcaillet J, Schuster M, Arnaud N, Monie P, Lihoreau F, et al.: Cosmogenic nuclide dating of Sahelanthropus tchadensis and Australopithecus bahrelghazali: mio-pliocene hominids from Chad. Proc Natl Acad Sci 2008, 105:3226-3231.
• [34]Thomas H: Les bovidés du Miocène supérieur des couches de Mpesida et de la formation de Lukeino (district de Baringo, Kenya). In Proceedings of the 8th Panafrican Congress of Prehistory and Quaternary Studies (Nairobi 1977). Edited by Leakey REF, Ogot BA. Nairobi; 1980:82-91.
• [35]Haile-Selassie Y, Vrba ES, Bibi F: Ardipithecus kadabba: Late Miocene Evidence from the Middle Awash, Ethiopia. In Bovidae. Edited by Haile-Selassie Y, WoldeGabriel G. Berkeley: University of California Press; 2009:277-330.
• [36]WoldeGabriel G, Haile-Selassie Y, Renne PR, Hart WK, Ambrose SH, Asfaw B, Heiken G, White T: Geology and palaeontology of the late miocene middle Awash valley, Afar rift, Ethiopia. Nature 2001, 412:175-178.
• [37]Deino AL, Tauxe L, Monaghan M, Hill A: Ar-40/Ar-30 geochronology and paleomagnetic stratigraphy of the Lukeino and lower Chemeron formations at Tabarin and Kapcheberek, Tugen Hills, Kenya. J Hum Evol 2002, 42:117-140.
• [38]Renne PR, WoldeGabriel G, Hart WK, Heiken G, White TD: Chronostratigraphy of the miocene-pliocene Sagantole formation, middle Awash valley, Afar rift, Ethiopia. Geol Soc Am Bull 1999, 111:869-885.
• [39]Gentry AW: Fossil Bovidae (Mammalia) from Langebaanweg, South Africa. Ann S Afr Mus 1980, 79:213-337.
• [40]Vrba ES: New fossils of Alcelaphini and Caprinae (Bovidae; Mammalia) from Awash, Ethiopia, and phylogenetic analysis of Alcelaphini. Palaeontol Afr 1997, 34:127-198.
• [41]Hendey QB: Geological succession at Langebaanweg, Cape province, and global events of the late tertiary. S Afr J Sci 1981, 77:33-38.
• [42]Vrba ES, Gatesy J: New antelope fossils from Awash, Ethiopia, and phylogenetic analysis of Hippotragini (Bovidae, Mammalia). Palaeontol Afr 1994, 31:55-72.
• [43]Gentry AW: Bovidae. In Paleontology and Geology of Laetoli: Human Evolution in Context Volume 2. Edited by Harrison T. New York: Springer; 2011:363-465.
• [44]Deino AL: 40Ar/39Ar dating of Laetoli, Tanzania. In Paleontology and Geology of Laetoli: Human Evolution in Context. Edited by Harrison T. Dordrecht: Springer; 2011:77-97.
• [45]Bibi F: Tragelaphus nakuae: Evolutionary change, biochronology, and turnover in the African plio-pleistocene. Zool J Linn Soc 2011, 162:699-711.
• [46]WoldeGabriel G, Endale T, White TD, Thouveny N, Hart WK, Renne PR, Asfaw B: The role of Tephra studies in African paleoanthropology as exemplified by the Sidi Hakoma Tuff. J Afr Earth Sci 2013, 77:41-58.
• [47]Reed K, Bibi F: Fossil Tragelaphini (Artiodactyla: Bovidae) from the Hadar formation, Afar Regional State, Ethiopia. J Mamm Evol 2011, 1:57-69.
• [48]Gentry AW: The Bovidae of the Omo Group deposits, Ethiopia (French and American collections). In Les faunes Plio-Pléistocènes de la basse Vallée de l’Omo (Ethiopie); I: Perissodactyles-Artiodactyles (Bovidae). Volume 1985. Edited by Coppens Y, Howell FC. Paris, France: CNRS; 1985:119-191. Cahiers de Paléontologie
• [49]Feibel CS, Brown FH, Mcdougall I: Stratigraphic context of fossil hominids from the Omo group deposits - northern Turkana Basin, Kenya and Ethiopia. Am J Phys Anthropol 1989, 78:595-622.
• [50]Gentry AW, Gentry A: Fossil Bovidae (Mammalia) of Olduvai Gorge, Tanzania; Part I. Bulletin of the British Museum Natural History Geology Series 1978, 29:289-446.
• [51]Gentry AW: Bovidae. In Cenozoic Mammals of Africa. Edited by Werdelin L, Sanders WJ. Berkeley: University of California Press; 2010:747-803.
• [52]Hay RL: Geology of the Olduvai Gorge: A Study of Sedimentation in a Semiarid Basin. Berkeley: University of California Press; 1976.
• [53]Deino AL: 40Ar/39Ar dating of Bed I, Olduvai Gorge, Tanzania, and the chronology of early pleistocene climate change. J Hum Evol 2012, 63:251-273.
• [54]Clark JD, de Heinzelin J, Schick KD, Hart WK, White TD, WoldeGabriel G, Walter RC, Suwa G, Asfaw B, Vrba E: African Homo erectus: old radiometric ages and young Oldowan assemblages in the middle Awash valley, Ethiopia. Science 1994, 264:1907-1910.
• [55]Pulquerio MJ, Nichols RA: Dates from the molecular clock: how wrong can we be? Trends Ecol Evol 2007, 22:180-184.
• [56]Drummond AJ, Ho SY, Phillips MJ, Rambaut A: Relaxed phylogenetics and dating with confidence. PLoS Biol 2006, 4:e88.
• [57]Lanfear R, Welch JJ, Bromham L: Watching the clock: studying variation in rates of molecular evolution between species. Trends Ecol Evol 2010, 25:495-503.
• [58]Ho SY: An examination of phylogenetic models of substitution rate variation among lineages. Biol Lett 2009, 5:421-424.
• [59]Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TLL, Stadler T, et al.: Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 2011, 334:521-524.
• [60]Near TJ, Meylan PA, Shaffer HB: Assessing concordance of fossil calibration points in molecular clock studies: an example using turtles. Am Nat 2005, 165:137-146.
• [61]Sanders KL, Lee MS: Evaluating molecular clock calibrations using Bayesian analyses with soft and hard bounds. Biol Lett 2007, 3:275-279.
• [62]Marshall CR: A simple method for bracketing absolute divergence times on molecular phylogenies using multiple fossil calibration points. Am Nat 2008, 171:726-742.
• [63]Lukoschek V, Keogh JS, Avise JC: Evaluating fossil calibrations for dating phylogenies in light of rates of molecular evolution: a comparison of three approaches. Syst Biol 2012, 61:22-43.
• [64]Rutschmann F, Eriksson T, Salim KA, Conti E: Assessing calibration uncertainty in molecular dating: the assignment of fossils to alternative calibration points. Syst Biol 2007, 56:591-608.
• [65]Ayala FJ: Molecular clock mirages. Bioessays 1999, 21:71-75.
• [66]Wilke T, Schultheiss R, Albrecht C: As time goes by: a simple fool’s guide to molecular clock approaches in invertebrates. Am Malacol Bull 2009, 27:25-45.
• [67]Hugall AF, Lee MS: The likelihood node density effect and consequences for evolutionary studies of molecular rates. Evolution 2007, 61:2293-2307.
• [68]Ho SY, Phillips MJ, Cooper A, Drummond AJ: Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 2005, 22:1561-1568.
• [69]Phillips MJ: Branch-length estimation bias misleads molecular dating for a vertebrate mitochondrial phylogeny. Gene 2009, 441:132-140.
• [70]Ho SY, Phillips MJ: Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst Biol 2009, 58:367-380.
• [71]Benton MJ, Ayala FJ: Dating the tree of life. Science 2003, 300:1698-1700.
• [72]Linder HP, Hardy CR, Rutschmann F: Taxon sampling effects in molecular clock dating: an example from the African Restionaceae. Mol Phylogen Evol 2005, 35:569-582.
• [73]Ronquist F, Klopfstein S, Vilhelmsen L, Schulmeister S, Murray DL, Rasnitsyn AP: A total-evidence approach to dating with fossils, applied to the early radiation of the Hymenoptera. Syst Biol 2012, 61:973-999.
• [74]Métais G, Vislobokova I: Basal ruminants. In The Evolution of Artiodactyls. Edited by Prothero DR, Foss SE. Baltimore: Johns Hopkins University Press; 2007:189-212.
• [75]Métais G, Chaimanee Y, Jaeger JJ, Ducrocq S: New remains of primitive ruminants from Thailand; evidence of the early evolution of the Ruminantia in Asia. Zool Scr 2001, 30:231-248.
• [76]Janis CM, Scott KM: The phylogeny of the Ruminantia (Artiodactyla, Mammalia). In The Phylogeny and Classification of Tetrapods; Volume 2, Mammals. Volume 35b. Edited by Benton MJ. London-New York: International: Academic Press [for the] Systematics Association; 1988:273-282. Systematics Association Special Volume
• [77]O’Leary MA, Gatesy J: Impact of increased character sampling on the phylogeny of Cetartiodactyla (Mammalia): combined analysis including fossils. Cladistics 2008, 24:397-442.
• [78]Vislobokova I, Lavrov A: The earliest musk deer of the genus Moschus and their significance in clarifying of evolution and relationships of the family Moschidae. Paleontol J 2009, 43:326-338.
• [79]Prothero DR: Family Moschidae. In The Evolution of Artiodactyls. Edited by Prothero D, Foss S. Baltimore: Johns Hopkins University Press; 2007:221-226.
• [80]Barry JC, Cote S, MacLatchy L, Lindsay EH, Kityo R, Rajpar AR: Oligocene and Early Miocene Ruminants (Mammalia, Artiodactyla) from Pakistan and Uganda. Palaeontol Electron 2005, 8:22A-29p.
• [81]Prothero DR: Foss SE (Eds.): The Evolution of Artiodactyls . Baltimore: Johns Hopkins University; 2007.
• [82]Gilbert C, Ropiquet A, Hassanin A: Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia): systematics, morphology, and biogeography. Mol Phylogen Evol 2006, 40:101-117.
• [83]Azanza B, Morales J: Tethytragus nov. gen et Gentrytragus nov. gen. Deux nouveaux Bovidés (Artiodactyla, Mammalia) du Miocène moyen. Proceedings, Koninklijke Nederlandse Akademie Van Wetenschappen 1994, B 97:249-282.
• [84]Made J: The bovid Pseudoeotragus seegrabensis nov. gen., nov. sp. from the Aragonia (Miocene) of Seegraben near Leoben (Austria). Proceedings Koninklijke Nederlandse Akademie Van Wetenschappen Ser B 1989, 92:215-240.
• [85]Thomas H: Les Bovidés anté-hipparions des Siwaliks inférieurs (Plateau du Potwar, Pakistan). Mémoires de la Société Géologique de France, Nouvelle Série 1984, 145:1-68.
• [86]Gentry AW: The Bovidae (Mammalia) of the Fort Ternan fossil fauna. In Fossil Vertebrates of Africa, Vol 2. London: Academic Press; 1970:243-323.
• [87]Köhler M: Boviden des turkischen Miozäns (Känozoikum und Braunkohlen der Türkei). Paleontologia y Evolució 1987, 21:133-246.
• [88]Gentry AW: The miocene differentiation of old world Pecora (Mammalia). Hist Biol 1994, 7:115-158.
• [89]Shipman P, Walker A, Van Couvering JA, Hooker PJ, Miller JA: The Fort Ternan hominoid site, Kenya: geology, age, taphonomy and paleoecology. J Hum Evol 1981, 10:49-72.
• [90]Hassanin A, An J, Ropiquet A, Nguyen TT, Couloux A: Combining multiple autosomal introns for studying shallow phylogeny and taxonomy of Laurasiatherian mammals: application to the tribe Bovini (Cetartiodactyla, Bovidae). Mol Phylogen Evol 2013, 766-775.
• [91]Vrba ES, Schaller G: Phylogeny of Bovidae based on behavior, glands, skulls, and postcrania. In Antelopes, Deer, and Relatives. Edited by Vrba ES, Schaller G. New Haven: Yale University Press; 2000:203-222.
• [92]Groves C, Schaller G: The phylogeny and biogeography of the newly discovered anamite artiodactyls. In Antelopes, Deer, and Relatives. Edited by Vrba ES, Schaller G. New Haven: Yale University Press; 2000:261-282.
• [93]Vrba ES, Vaisnys JR, Gatesy JE, Desalle R, Wei KY: Analysis of pedomorphosis using allometric characters – the example of Reduncini antelopes (Bovidae, Mammalia). Syst Biol 1994, 43:92-116.
• [94]Omland KE: Correlated rates of molecular and morphological evolution. Evolution 1997, 51:1381-1393.
• [95]Thomas H: Anatomie crânienne et relations phylogénétiques du nouveau bovidé (Pseudoryx nghetinensis) découvert dans la cordillère annamitique au Vietnam. Mammalia 1994, 58:453-481.
• [96]Gatesy J, Arctander P: Hidden morphological support for the phylogenetic placement of Pseudoryx nghetinhensis with bovine bovids: a combined analysis of gross anatomical evidence and DNA sequences from five genes. Syst Biol 2000, 49:515-538.
• [97]Ropiquet A, Hassanin A: Molecular evidence for the polyphyly of the genus Hemitragus (Mammalia, Bovidae). Mol Phylogen Evol 2005, 36:154-168.
• [98]Verkaar ELC, Nijman IJ, Beeke M, Hanekamp E, Lenstra JA: Maternal and paternal lineages in cross-breeding bovine species. Has wisent a hybrid origin? Mol Biol Evol 2004, 21:1165-1170.
• [99]Nijman IJ, Van Boxtel DCJ, Van Cann LM, Marnoch Y, Cuppen E, Lenstra JA: Phylogeny of Y chromosomes from bovine species. Cladistics 2008, 24:723-726.
• [100]Buntjer JB, Otsen M, Nijman IJ, Kuiper MTR, Lenstra JA: Phylogeny of bovine species based on AFLP fingerprinting. Heredity 2002, 88:46-51.
• [101]Pidancier N, Jordan S, Luikart G, Taberlet P: Evolutionary history of the genus Capra (Mammalia, Artiodactyla): discordance between mitochondrial DNA and Y-chromosome phylogenies. Mol Phylogen Evol 2006, 40:739-749.
• [102]Bibi F, Fack F, Vrba ES: A new fossil caprin and a combined molecular and morphological bayesian analysis of Caprini (Mammalia: Bovidae). J Evol Biol 2012, 25:1843-1854.
• [103]Moodley Y, Bruford MW, Bleidorn C, Wronski T, Apio A, Plath M: Analysis of mitochondrial DNA data reveals non-monophyly in the bushbuck (Tragelaphus scriptus) complex. Mamm Biol 2009, 74:418ñ422.
• [104]Vrba ES: The significance of bovid remains as indicators of environment and predation patterns. In Fossils in the Making: Vertebrate Taphonomy and Paleoecology. Edited by Behrensmeyer AK, Hill A. Chicago: Univ. of Chicago Press; 1980:247-271.
• [105]Shipman P, Harris JM: Habitat preference and paleoecology of Australopithecus boisei in Eastern Africa. 1988, 343ñ381. [Evolutionary history of the ìrobustî australopithecines New York: Aldine de Gruyter]
• [106]Bobe R, Eck GG: Responses of African bovids to pliocene climatic change. Paleobiology 2001, 27:1-47.
• [107]White TD, Ambrose SH, Suwa G, Su DF, DeGusta D, Bernor RL, Boisserie J-R, Brunet M, Delson E, Frost S, et al.: Macrovertebrate paleontology and the pliocene habitat of Ardipithecus ramidus. Science 2009, 326:50-56.
• [108]Grubb P, Sandrock O, Kullmer O, Kaiser TM, Schrenk F: Relationships between eastern and southern African mammal faunas. In African Biogeography, Climate Change and Early Hominid Evolution. Edited by Bromage TG, Schrenk F. New York: Oxford University Press; 2000:253-267.
• [109]Geraads D, Brunet M, Mackaye HT, Vignaud P: Pliocene Bovidae (Mammalia) from the Koro Toro Australopithecine sites, Chad. J Vertebr Paleontol 2001, 21:335-346.
• [110]de Heinzelin J, Clark JD, White T, Hart W, Renne P, WoldeGabriel G, Beyene Y, Vrba ES: Environment and behavior of 2.5-million-year-old Bouri hominids. Science 1999, 284:625-629.
• [111]Gilbert WH: Bovidae. In Homo erectus: Pleistocene Evidence from the Middle Awash, Ethiopia. Edited by Gilbert WH, Asfaw B. Berkeley: Univ. of California Press; 2008:45-94.
• [112]Gentry AW: Bovidae of the Omo group deposits. In Earliest man and environments in the Lake Rudolf Basin; stratigraphy, paleoecology, and evolution. Edited by Coppens Y, Howell FC, Isaac GL, Leakey REF. Chicago, Ill., United States: Univ. Chicago Press; 1976:275-292.
• [113]Bärmann EV, Rössner GE, Wörheide G: A revised phylogeny of Antilopini (Bovidae, Artiodactyla) using combined mitochondrial and nuclear genes. Mol Phylogen Evol 2013, 484-493.
• [114]Gentry AW: Ruminantia (Artiodactyla). In Geology and Paleontology of the Miocene Sinap Formation, Turkey. Edited by Fortelius M, Kappelman J, Sen S, Bernor RL. New York: Columbia University Press; 2003.
• [115]Bibi F: Mio-pliocene faunal exchanges and African biogeography: the record of fossil bovids. PLoS ONE 2011, 6:e16688.
• [116]Harris JM: Bovidae from the Lothagam succession. In Lothagam: The Dawn of Humanity in Eastern Africa. Edited by Leakey MG, Harris JM. New York: Columbia University Press; 2003:531-579.
• [117]Vignaud P, Duringer P, Mackaye HT, Likius A, Blondel C, Boisserie JR, de Bonis L, Eisenmann V, Etienne ME, Geraads D, et al.: Geology and palaeontology of the upper miocene Toros-Menalla hominid locality, Chad. Nature 2002, 418:152-155.
• [118]Thomas H: Les Bovidae (Artiodactyla; Mammalia) du Miocène du sous-continent indien, de la péninsule arabique et de l’Afrique: biostratigraphie, biogéographie et écologie. Palaeogeogr, Palaeoclimatol, Palaeoecol 1984, 45:251-299.
• [119]Gentry AW: A new bovine (Bovidae, Artiodactyla) from the Hadar formation, Ethiopia. Trans R Soc S Afr 2006, 61:41-50.
• [120]Bibi F, Hill A, Beech M, Yasin W: Late Miocene fossils from the Baynunah Formation, United Arab Emirates: summary of a decade of new work. In Fossil Mammals of Asia: Neogene Biostratigraphy and Chronology. Edited by Wang X, Flynn LJ, Fortelius M. New York: Columbia Univ. Press; 2013:583-594.
• [121]Pyron RA: Divergence time estimation using fossils as terminal Taxa and the origins of Lissamphibia. Syst Biol 2011, 60:466.
• [122]Drummond AJ, Suchard MA, Xie D, Rambaut A: Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012, 29:1969-1973.
• [123]Kumar S, Skjaeveland A, Orr R, Enger P, Ruden T, Mevik B-H, Burki F, Botnen A, Shalchian-Tabrizi K: AIR: a batch-oriented web program package for construction of supermatrices ready for phylogenomic analyses. BMC Bioinformatics 2009, 10:357. BioMed Central Full Text
• [124]Darriba D, Taboada GL, Doallo R, Posada D: jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012, 9:772-772.
• [125]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
• [126]Yang Z, Rannala B: Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Mol Biol Evol 2006, 23:212-226.