Skip to main content

Advertisement

SpringerLink
Log in

The Evolution of Dental Eruption Sequence in Artiodactyls

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

The sequence of eruption of the second generation of teeth varies across taxa, is highly functional, and is strongly influenced by genetic effects. We assessed postcanine dental eruption sequence across artiodactyls in order to test two hypotheses: 1) dental eruption sequence is a good phylogenetic character for artiodactyls; and, 2) eruption sequence is adaptive and associated with life history variables like postnatal growth and longevity in artiodactyls (Schultz’s Rule). We examined postcanine eruption sequence in 81 genera (100 species) spanning ten families of Artiodactyla. Our ancestral state reconstruction supports the interpretation that the third molar erupted last in the ancestor of Artiodactyla, and that the fourth premolar erupted after the third molar in the ancestor of Ruminantia. Our results indicate that eruption of the third molar last evolved secondarily in the caprines, likely sometime in the Miocene. Overall, our results support the hypothesis that dental eruption sequence is phylogenetically conserved in artiodactyls. Caprines occupy high elevation habitats, and we hypothesize that evolution of their unique dental eruption sequence may be associated with limited resource availability in high elevation mountain systems and the necessity to process a wide range of vegetation types.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arnold C, Matthews LJ, Nunn CL (2010) The 10kTrees website: a new online resource for primate phylogeny. Evol Anthropol 19:114–118

    Article  Google Scholar 

  • Bibi F (2013) A multi-calibrated mitochondrial phylogeny of extant Bovidae (Artiodactyla, Ruminantia) and the importance of the fossil record to systematics. BMC Evol Biol 13(1):166–171

    Article  PubMed  PubMed Central  Google Scholar 

  • Bibi F, Vrba E, Fack F (2012) A new African fossil caprin and a combined molecular and morphological bayesian phylogenetic analysis of caprini (Mammalia: Bovidae). J Evol Biol 25(9):1843–1854

    Article  CAS  PubMed  Google Scholar 

  • Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57(4):717–745

    Article  PubMed  Google Scholar 

  • Blondel C (2001) The Eocene–Oligocene ungulates from Western Europe and their environment. Palaeogeogr Palaeoclimatol Palaeoecol 168(1):125–139

    Article  Google Scholar 

  • Böhme M (2003) The Miocene Climatic Optimum: evidence from ectothermic vertebrates of Central Europe. Palaeogeogr Palaeoclimatol Palaeoecol 195(3):389–401

  • Bover P, Alcover JA (1999) The evolution and ontogeny of the dentition of Myotragus balearicus Bate, 1909 (Artiodactyla, Caprinae): evidence from new fossil data. Biol J Linn Soc 68(3):401–428

    Article  Google Scholar 

  • Bowyer R (1997) The role of moose in landscape processes: effects of biogeography, population dynamics and predation. In: Bissonette J (ed) Wildlife and Landscape Ecology: Effects of Sequence and Scale. Springer-Verlag, New York, pp 265–287

  • Brandborg SM (1950) The life history and ecology of the mountain goat in Idaho and Montana. Dissertation, University of Idaho

    Google Scholar 

  • Brooks DM, Tarifa T, Rojas JM, Vargas RJ, Aranibar H (2001) A preliminary assessment of the mammalian fauna of the eastern Bolivian panhandle. Mammalia 65(4):509–520

    Article  Google Scholar 

  • Bryant HN (1990) Implications of the dental eruption sequence in Barbourofelis (Carnivora, Nimravidae) for the function of upper canines and the duration of parental care in sabretoothed carnivores. J Zool 222(4):585–590

    Article  Google Scholar 

  • Buzan EV, Bryja J, Zemanová B, Kryštufek B (2013) Population genetics of chamois in the contact zone between the Alps and the Dinaric Mountains: uncovering the role of habitat fragmentation and past management. Conserv Genet 14(2):401–412

    Article  Google Scholar 

  • Byrd KE (1981) Sequences of dental ontogeny and callitrichid taxonomy. Primates 22(1):103–118

    Article  Google Scholar 

  • Coddington JA (1988) Cladistic tests of adaptational hypotheses. Cladistics 4(1):3–22

    Article  Google Scholar 

  • Donoghue MJ (1989) Phylogenies and the analysis of evolutionary sequences, with examples from seed plants. Evolution 43(6):1137–1156

    Article  PubMed  Google Scholar 

  • Erfurt J, Métais G (2007) Endemic European Paleogene artiodactyls. In: Prothero DR, Foss SE (eds) The Evolution of Artiodactyls. Johns Hopkins University Press, Baltimore, pp 59–84

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Fernández MH, Vrba ES (2005) A complete estimate of the phylogenetic relationships in Ruminantia: a dated species-level supertree of the extant ruminants. Biol Rev 80(2):269–302

    Article  Google Scholar 

  • Fortelius M (1985) Ungulate cheek teeth: developmental, functional, and evolutionary interrelations. Acta Zoologica Fennica 180:1–76

    Google Scholar 

  • Ge RL, Cai Q, Shen YY, San A, Lan M, Zhang Y, Yi X, Chen Y, Yang L, Huang Y, He R, Hui Y, Hao M, Li Y, Wang B, Ou X, Xu J, Zhang Y, Wu K, Geng C, Zhou W, Zhou T, Irwin D, Yang Y, Ying L, Bao H, Kim J, Larkin D, Ma J, Lewin H, Xing J, Platt II R, Ray D, Auvil L, Capitanu B, Zhang X, Zhang G, Murphy R, Wang J, Zhang Y, Wang J (2013) Draft genome sequence of the Tibetan antelope. Nat Commun 4:1–7

    Article  CAS  Google Scholar 

  • Geisler JH, Theodor JM, Uhen MD, Foss SE (2007) Phylogenetic relationships of cetaceans to terrestrial artiodactyls. In: Prothero DR, Foss S (eds) The Evolution of Artiodactyls. John Hopkins University Press, Baltimore, pp 19–31

  • Gentry AW (2000) The ruminant radiation. In: Vrba ES, Schaller GB (eds) Antelopes, Deer, and Relatives. Yale University Press, New Haven, pp 11–25

  • Gentry AW, Heizmann EPJ (1996) Miocene ruminants of the central and eastern Tethys and Paratethys. In: Bernor R, Fahlbusch V, Mittmann H (eds) The Evolution of Western Eurasian Neogene Mammal Faunas. Columbia University Press, New York, pp 378–391

  • Green MJB (1987) Scent-marking in the Himalayan musk deer (Moschus chrysogaster). J Zool 1:721–737

    Article  Google Scholar 

  • Grzimek B (1990) Grzimek’s animal Life Encyclopedia: Mammals I-IV. McGraw-Hill Publishing Company, New York

  • Hassanin A, Douzery EJ (1999) The tribal radiation of the family Bovidae (Artiodactyla) and the evolution of the mitochondrial cytochrome b gene. Mol Phylogenet Evol 13(2): 227–243

    Article  CAS  PubMed  Google Scholar 

  • Hassanin A, Pasquet E, Vigne JD (1998) Molecular systematics of the subfamily Caprinae (Artiodactyla, Bovidae) as determined from cytochrome b sequences. J Mammal Evol 5(3):217–236

    Article  Google Scholar 

  • Hassanin, A, Delsuc F, Ropiquet A, Hammer C, van Vuuren BJ, Matthee C, Ruiz-Garcia M, Catzeflis F, Areskoug V, Nguyen TT, Couloux A (2012) Sequence and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. C R Biol 335(1):32–50

    Article  PubMed  Google Scholar 

  • Hillson S (2005) Teeth. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Hlusko LJ, Sage RD, Mahaney MC (2011) Modularity in the mammalian dentition: mice and monkeys share a common dental genetic architecture. J Exp Zool B Mol Dev Evol 316(1):21–49

    Article  PubMed  PubMed Central  Google Scholar 

  • Hogue AS, Ravosa MJ (2001) Transverse masticatory movements, occlusal orientation, and symphyseal fusion in selenodont artiodactyls. J Morphol 249(3):221–241

    Article  CAS  PubMed  Google Scholar 

  • Janis CM (1989) A climatic explanation for patterns of evolutionary diversity in ungulate mammals. Palaeontology 32(3):463–481

    Google Scholar 

  • Janis CM (1995) Correlations between craniodental morphology and feeding behavior in ungulates: reciprocal illumination between living and fossil taxa. In: Thomason J (ed) Functional Morphology in Vertebrate Paleontology. Cambridge University Press, New York, pp 76–98

  • Järvinen E, Tummers M, Thesleff I (2009) The role of the dental lamina in mammalian tooth replacement. J Exp Zool B Mol Dev Evol 312(4):281–291

    Article  Google Scholar 

  • Jordana X, Köhler M (2011) Enamel microstructure in the fossil bovid Myotragus balearicus (Majorca, Spain): implications for life-history evolution of dwarf mammals in insular ecosystems. Palaeogeogr Palaeoclimatol Palaeoecol 300(1):59–66

  • Jordana X, Marín-Moratalla N, Moncunill-Solé B, Bover P, Alcover JA, Köhler M (2013) First fossil evidence for the advance of replacement teeth coupled with life history evolution along an anagenetic mammalian lineage. PLoS One 8(7):e70743

  • Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  CAS  PubMed  Google Scholar 

  • Kerr GR (1966) The ecology of mountain goats in west central Alberta. Dissertation, University of Alberta (Calgary)

  • Khan SM, Page S, Ahmad H, Ullah Z, Shaheen H, Ahmad M, Harper DM (2013) Phyto-climatic gradient of vegetation and habitat specificity in the high elevation western Himalayas. Pak J Bot 45:223–230

    Google Scholar 

  • Köhler M (1987) Boviden des türkischen Miozäns (Känozoikum und Braunkohlen der Türkei). Paleontologia i Evolució 21:133–246

    Google Scholar 

  • Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392(6679):917–920

    Article  CAS  PubMed  Google Scholar 

  • Lalueza-Fox C, Castresana J, Sampietro L, Marquès-Bonet T, Alcover JA, Bertranpetit J (2005) Molecular dating of caprines using ancient DNA sequences of Myotragus balearicus, an extinct endemic Balearic mammal. BMC Evol Biol 5:70–81

    Article  PubMed  PubMed Central  Google Scholar 

  • Leigh SR, Setchell JM, Charpentier M, Knapp LA, Wickings EJ (2008) Canine tooth size and fitness in male mandrills (Mandrillus sphinx). J Hum Evol 55(1):75–85

    Article  PubMed  Google Scholar 

  • Leslie DM Jr (2010) Przewalskium albirostre (Artiodactyla: Cervidae). Mammal Species 42(1):7–18

    Article  Google Scholar 

  • Macho GA, Berner ME (1993) Enamel thickness of human maxillary molars reconsidered. Am J Phys Anthropol 92(2):189–200

  • Maddison WP, Maddison DR (2015) Mesquite: a modular system for evolutionary analysis (Version 3.04). http://mesquiteproject.org

  • Matthee CA, Burzlaff JD, Taylor JF, Davis SK (2001) Mining the mammalian genome for artiodactyl systematics. Syst Biol 50(3):367–390

    Article  CAS  PubMed  Google Scholar 

  • McKenna MC, Bell SK (1997) Classification of Mammals above the Species Level. Columbia University Press, New York

  • Meredith R, Janečka J, Gatesy J, Ryder O, Fisher C, Teeling E, Goodbla A, Eizirik E, Simão T, Stadler T, Rabosky D, Honeycutt R, Flynn J, Ingram C, Steiner C, Williams T, Robinson T, Burk-Herrick A, Westerman M, Ayoub N, Springer M, Murphy W (2011) Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334(6055):521–524

  • Métais G, Vislobokova N (2007) Basal ruminants. In: Prothero DR, Foss S (eds) The Evolution of Artiodactyls. John Hopkins University Press, Baltimore, pp 189–212

  • Molvar E, Bowyer R, Van Ballenberghe V (1993) Moose herbivory, browse quality and nutrient cycling in an Alaskan tree line community. Oecologia 94:472–479

    Article  PubMed  Google Scholar 

  • Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O’Brien SJ (2001) Molecular phylogenetics and the origins of placental mammals. Nature 409(6820):614–618.

    Article  CAS  PubMed  Google Scholar 

  • Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W (2015) The caper package: comparative analysis of phylogenetics and evolution in R. R package version 5(2)

  • Osborn JW, Crompton AW (1973) The evolution of mammalian from reptilian dentitions. Breviora 399:1–18

    Google Scholar 

  • Owen-Smith N, Fryxell JM, Merrill EH (2010) Foraging theory upscaled: the behavioural ecology of herbivore movement. Phil Trans R Soc Lond B Biol Sci 365(1550):2267–2278

    Article  CAS  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20(2):289–290

    Article  CAS  PubMed  Google Scholar 

  • Pfretzschner HU (1992) Enamel microstructure and hypsodonty in large mammals. In: Smith P, Tchernov E (eds) Structure, function and evolution of teeth. Freund Publishing House, London, pp 147–162

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org/

  • Revell LJ, Harmon LJ, Collar DC (2008) Phylogenetic signal, evolutionary process, and rate. Syst Biol 57(4):591–601

    Article  PubMed  Google Scholar 

  • Ricklefs RE, Starck JM (1996) Applications of phylogenetically independent contrasts: a mixed progress report. Oikos 77(1):167–172

    Article  Google Scholar 

  • Ropiquet A, Hassanin A (2005) Molecular evidence for the polyphyly of the genus Hemitragus (Mammalia, Bovidae). Mol Phylogenet Evol 36(1):154–168.

    Article  CAS  PubMed  Google Scholar 

  • Ropiquet A, Hassanin A (2006) Hybrid origin of the Pliocene ancestor of wild goats. Mol Phylogenet Evol 41(2):395–404

    Article  CAS  PubMed  Google Scholar 

  • Schultz AH (1935) Eruption and decay of the permanent teeth in primates. Am J Phys Anthropol 19(1):489–581

    Article  Google Scholar 

  • Schultz AH (1956) Postembryonic age changes. In: Hofer H, Schultz AH, Starck D (eds) Primatologia. Karger, Basel, pp 887–964

    Google Scholar 

  • Schultz AH (1960) Age changes in primates and their modification in man. In: Tanner JM (ed) Human Growth vol III. Pergamon Press, Oxford, pp 1–20

  • Schwartz JH (1974) Dental development and eruption in the prosimians and its bearing on their evolution. Dissertation, Columbia University

    Google Scholar 

  • Shafer A, Hall J (2010) Placing the mountain goat: a total evidence approach to testing alternative hypotheses. Mol Phylogenet Evol 55(1):18–25

    Article  CAS  PubMed  Google Scholar 

  • Shaheen H, Shinwari ZK (2012) Phyto diversity and endemic richness of Karambar Lake vegetation from Chitral, Hindukush-Himalayas. Pak J Bot 44(1):17–21

    Google Scholar 

  • Smith BH (1994) Sequence of emergence of the permanent teeth in Macaca, Pan, Homo, and Australopithecus: its evolutionary significance. Am J Hum Biol 6:61–76

    Article  PubMed  Google Scholar 

  • Smith BH (2000) ‘Schultz’s rule’ and the evolution of tooth emergence and replacement patterns inprimates and ungulates. In: Teaford MF, Smith MM, Ferguson MW (eds) Development, function and evolution of teeth. Cambridge University Press, Cambridge, pp 212–227

  • Spaulding M, O’Leary MA, Gatesy J (2009) Relationships of Cetacea (Artiodactyla) among mammals: increased taxon sampling alters interpretations of key fossils and character evolution. PLoS One 4(9):e7062

  • Strömberg CA (2011) Evolution of grasses and grassland ecosystems. Annu Rev Earth Planet Sci 39:517–544

    Article  Google Scholar 

  • Sudre J (1974) D’importants restes de Diplobune minor Filhol à Itardies (Quercy). Palaeovertebrata 6:47–54

    Google Scholar 

  • Suri L, Gagari E, Vastardis H (2004) Delayed tooth eruption: pathogenesis, diagnosis, and treatment. Am J Orthod Dentofacial Orthop 126(4):432–445

    Article  PubMed  Google Scholar 

  • Tacutu R, Craig T, Budovsky A, Wuttke D, Lehmann G, Taranukha D, Costa J, Fraifeld VE, de Magalhaes JP (2013) Human ageing genomic resources: integrated databases and tools for the biology and genetics of ageing. Nucleic Acids Res 41(D1):D1027-D1033

    Article  CAS  PubMed  Google Scholar 

  • Tattersall I, Schwartz JH (1974) Craniodental morphology and the systematics of the Malagasy lemurs (Primates, Prosimii). Anthropol Pap Am Mus Nat Hist 52:139–192

    Google Scholar 

  • Theodor JM, Erfurt J, Métais G (2007) The earliest artiodactyls. In: Prothero DR, Foss S (eds) The Evolution of Artiodactyls. John Hopkins University Press, Baltimore, pp 32–58

  • Tranquillini W (1964) The physiology of plants at high altitudes. Annu Rev Plant Biol 15(1):345–362

    Article  CAS  Google Scholar 

  • Tsujikawa H (2005) The updated late Miocene large mammal fauna from Samburu Hills, northern Kenya. Afr Study Monogr Suppl 32:1–50

    Google Scholar 

  • Vázquez GJA, Givnish TJ (1998) Altitudinal gradients in tropical forest composition, structure, and diversity in the Sierra de Manantlan. J Ecol 86(6):999–1020

    Article  Google Scholar 

  • Veitschegger K, Sánchez-Villagra MR (2016) Tooth eruption sequences in cervids and the effect of morphology, life history, and phylogeny. J Mammal Evol 23:251–263

    Article  Google Scholar 

  • Vrba ES, Schaller GB (2000a) Introduction. In: Vrba ES, Schaller GB (eds) Antelopes, Deer, and Relatives. Yale University Press, New Haven, pp 1–10

  • Vrba ES, Schaller GB (2000b) Phylogeny of bovidae based on behavior, glands, skulls and postcrania. In: Vrba ES, Schaller GB (eds) Antelopes, Deer, and Relatives. Yale University Press, New Haven, pp 203–222

  • Wise GE, Frazier-Bowers S, D’souza RN (2002) Cellular, molecular, and genetic determinants of tooth eruption. Crit Rev Oral Biol Med 13(4):323–335

    Article  CAS  PubMed  Google Scholar 

  • Wolfe JA (1985) Distribution of major vegetational types during the tertiary. In: Sundquist ET, Broecker WS (eds) The Carbon Cycle and Atmospheric CO: Natural Variations Archean to Present. American Geophysical Union, Washington, D.C., pp 357–375

  • Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292(5517):686–693

    Article  CAS  PubMed  Google Scholar 

  • Zhou L, Su YC, Thomas DC, Saunders RM (2012) ‘Out-of-Africa’ dispersal of tropical floras during the Miocene climatic optimum: evidence from Uvaria (Annonaceae). J Biogeogr 39(2):322–335

    Article  Google Scholar 

  • Zhou X, Xu S, Yang Y, Zhou K, Yang G (2011) Phylogenomic analyses and improved resolution of Cetartiodactyla. Mol Phylogenet Evol 61(2):255–264

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Chris Conroy (MVZ), Esther Langan (NMNH), Darrin Lunde (NMNH), and John Ososky (NMNH) for access to specimens. We would like to thank Marianne Brasil, Andrew Weitz, and the MVZ community for providing helpful feedback and discussion, and Madeleine Zuercher for assistance with the literature review. The authors would also like to thank Eva Bärmann, one anonymous reviewer, and Editor-in-Chief John R. Wible for their thoughtful comments and suggestions that greatly improved this manuscript. Funding for this study and presentation of results was generously provided by the Museum of Vertebrate Zoology, the J. Desmond Clark Human Evolution Research Center, and the Department of Integrative Biology, UC Berkeley.

Author Contributions

TAM collected the data, conducted the analyses, and wrote the manuscript. LJH supervised the project and edited the manuscript.

Author information

Authors and Affiliations

  1. Department of Integrative Biology, 3040 Valley Life Sciences Building, #3140, UC Berkeley, Berkeley, CA, 94720, USA

    Tesla A. Monson & Leslea J. Hlusko

Authors
  1. Tesla A. Monson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leslea J. Hlusko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tesla A. Monson.

Electronic supplementary material

ESM 1

(XLSX 64 kb)

ESM 2

(PDF 91 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Monson, T.A., Hlusko, L.J. The Evolution of Dental Eruption Sequence in Artiodactyls. J Mammal Evol 25, 15–26 (2018). https://doi.org/10.1007/s10914-016-9362-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-016-9362-9

Keywords

Search

Navigation