Skip to main content

Advertisement

SpringerLink
Log in

Developmental Processes, Evolvability, and Dental Diversification of New World Monkeys

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

The developmental processes that contribute to variation of morphological traits are the subject of considerable interest when attempting to understand phenotypic evolution. It is well demonstrated that most characteristics of tooth pattern can be modified by tinkering conserved signal pathways involved in dental development. This effect can be evaluated by comparing developmental models with naturally occurring variation within explicit phylogenetic contexts. Here, we assess whether evolutionary changes in lower molar (M) ratios among platyrrhines were channelled by alterations in the balance of activators and inhibitors as predicted by the inhibitory cascade (IC) model (Kavanagh et al. in Nature 449:427–432, 2007). Ordinary linear regression adjusted to M2/M1 versus M3/M1 ratios of 38 species of platyrrhines indicated that the slope and intercept were significantly different from the IC model. Conversely, when the phylogeny was incorporated into the regression analyses (PGLS), variation in molar ratios did not differ from the developmental model. PGLS also showed that changes in molar proportions are not an allometric effect associated with body size. Discrepancies between phylogenetically corrected and non-corrected analyses are mainly due to the departure of Callitrichines from the predicted values. This subfamily displays agenesis of M3 with higher than expected M2/M1 ratios, indicating that M3 fails to develop even when the inhibition by M1 on the subsequent molars is not increased. Our results show that evolution in molar ratios is concordant with slight changes in the proportion of activators and inhibitors that regulate molar development; however, other processes are required to account for variation in the number of teeth.

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
Fig. 3

Similar content being viewed by others

References

  • Blomberg, S. P., Garland, T., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57(4), 717–745. doi:10.1111/j.0014-3820.2003.tb00285.x.

    PubMed  Google Scholar 

  • Cai, J., Cho, S.-W., Kim, J.-Y., Lee, M.-J., Cha, Y.-G., & Jung, H.-S. (2007). Patterning the size and number of tooth and its cusps. Developmental Biology, 304(2), 499–507. doi:10.1016/j.ydbio.2007.01.002.

    Article  PubMed  CAS  Google Scholar 

  • Catón, J., Bringas, P, Jr, & Zeichner-David, M. (2005). IGFs increase enamel formation by inducing expression of enamel mineralizing specific genes. Archives of Oral Biology, 50(2), 123–129. doi:10.1016/j.archoralbio.2004.11.012.

    Article  PubMed  Google Scholar 

  • Cho, S.-W., Kwak, S., Woolley, T. E., Lee, M.-J., Kim, E.-J., Baker, R. E., et al. (2011). Interactions between Shh, Sostdc1 and Wnt signaling and a new feedback loop for spatial patterning of the teeth. Development, 138(9), 1807–1816. doi:10.1242/dev.056051.

    Article  PubMed  CAS  Google Scholar 

  • Drummond, A. J., Ho, S. Y. W., Phillips, M. J., & Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology, 4(5), e88. doi:10.1371/journal.pbio.0040088.

    Article  PubMed  Google Scholar 

  • Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214. doi:10.1186/1471-2148-7-214.

    Article  PubMed  Google Scholar 

  • Felsenstein, J. (1985). Phylogenies and the comparative method. The American Naturalist, 125(1), 1–15.

    Article  Google Scholar 

  • Fleagle, J. G. (1999). Primate adaptation and evolution (2nd ed.). San Diego: Academic Press.

    Google Scholar 

  • Freckleton, R. P., Cooper, N., & Jetz, W. (2011). Comparative methods as a statistical fix: The dangers of ignoring an evolutionary model. The American Naturalist, 178(1), E10–E17. doi:10.1086/660272.

    Article  PubMed  Google Scholar 

  • Garland, T., Bennett, A. F., & Rezende, E. L. (2005). Phylogenetic approaches in comparative physiology. Journal of Experimental Biology, 208(16), 3015–3035. doi:10.1242/jeb.01745.

    Article  PubMed  Google Scholar 

  • Gould, S. J. (1977). Ontogeny and phylogeny. Cambridge, MA: Belknap Press of Harvard University Press.

    Google Scholar 

  • Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 9.

    Google Scholar 

  • Hartwig, W. C. (1996). Perinatal life history traits in New World monkeys. American Journal of Primatology, 40(2), 99–130. doi:10.1002/(SICI)1098-2345(1996)40:2<99:AID-AJP1>3.0.CO;2-V.

    Article  Google Scholar 

  • Harvey, P. H., & Pagel, M. D. (1991). The comparative method in evolutionary biology (1st ed.). Oxford: Oxford University Press.

    Google Scholar 

  • Henderson, E. (2007). Platyrrhine dental eruption sequences. American Journal of Physical Anthropology, 134(2), 226–239. doi:10.1002/ajpa.20658.

    Article  PubMed  Google Scholar 

  • Hendrikse, J. L., Parsons, T. E., & Hallgrímsson, B. (2007). Evolvability as the proper focus of evolutionary developmental biology. Evolution & Development, 9(4), 393–401. doi:10.1111/j.1525-142X.2007.00176.x.

    Article  Google Scholar 

  • Hu, B., Nadiri, A., Kuchler-Bopp, S., Perrin-Schmitt, F., Peters, H., & Lesot, H. (2006). Tissue engineering of tooth crown, root, and periodontium. Tissue Engineering, 12(8), 2069–2075. doi:10.1089/ten.2006.12.2069.

    Article  PubMed  CAS  Google Scholar 

  • Ives, A. R., & Zhu, J. (2006). Statistics for correlated data: Phylogenies, space, and time. Ecological Applications, 16(1), 20–32.

    Article  PubMed  Google Scholar 

  • Jernvall, J. (2000). Linking development with generation of novelty in mammalian teeth. Proceedings of the National Academy of Sciences, 97(6), 2641–2645. doi:10.1073/pnas.050586297.

    Article  CAS  Google Scholar 

  • Jumlongras, D., Lin, J.-Y., Chapra, A., Seidman, C. E., Seidman, J. G., Maas, R. L., et al. (2004). A novel missense mutation in the paired domain of PAX9 causes non-syndromic oligodontia. Human Genetics, 114(3), 242–249. doi:10.1007/s00439-003-1066-6.

    Article  PubMed  CAS  Google Scholar 

  • Kanazawa, E., & Rosenberger, A. (1988). Reduction index of the upper M2 in marmosets. Primates, 29(4), 525–533. doi:10.1007/BF02381139.

    Article  Google Scholar 

  • Kavanagh, K. D., Evans, A. R., & Jernvall, J. (2007). Predicting evolutionary patterns of mammalian teeth from development. Nature, 449(7161), 427–432. doi:10.1038/nature06153.

    Article  PubMed  CAS  Google Scholar 

  • Klein, M. L., Nieminen, P., Lammi, L., Niebuhr, E., & Kreiborg, S. (2005). Novel mutation of the initiation codon of PAX9 causes oligodontia. Journal of Dental Research, 84(1), 43–47. doi:10.1177/154405910508400107.

    Article  PubMed  CAS  Google Scholar 

  • Ledevin, R., Quéré, J.-P., & Renaud, S. (2010). Morphometrics as an insight into processes beyond tooth shape variation in a bank vole population. PLoS ONE, 5(11), e15470. doi:10.1371/journal.pone.0015470.

    Article  PubMed  Google Scholar 

  • Lemey, P., Salemi, M., & Vandamme, A.-M. (Eds.). (2009). The phylogenetic handbook: A practical approach to phylogenetic analysis and hypothesis testing (2nd ed.). Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Lidral, A. C., & Reising, B. C. (2002). The role of MSX1 in human tooth agenesis. Journal of Dental Research, 81(4), 274–278. doi:10.1177/154405910208100410.

    Article  PubMed  CAS  Google Scholar 

  • Marroig, G., & Cheverud, J. M. (2005). Size as a line of least evolutionary resistance: Diet and adaptive morphological radiation in New World monkeys. Evolution, 59(5), 1128–1142. doi:10.1111/j.0014-3820.2005.tb01049.x.

    PubMed  Google Scholar 

  • Müller, G. B. (2007). Evo–devo: Extending the evolutionary synthesis. Nature Reviews Genetics, 8(12), 943–949. doi:10.1038/nrg2219.

    Article  PubMed  Google Scholar 

  • Nieminen, P. (2009). Genetic basis of tooth agenesis. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 312B(4), 320–342. doi:10.1002/jez.b.21277.

    Article  PubMed  CAS  Google Scholar 

  • Nieminen, P., Arte, S., Tanner, D., Paulin, L., Alaluusua, S., Thesleff, I., et al. (2001). Identification of a nonsense mutation in the PAX9 gene in molar oligodontia. European Journal of Human Genetics: EJHG, 9(10), 743–746. doi:10.1038/sj.ejhg.5200715.

    Article  PubMed  CAS  Google Scholar 

  • Opazo, J. C., Wildman, D. E., Prychitko, T., Johnson, R. M., & Goodman, M. (2006). Phylogenetic relationships and divergence times among New World monkeys (Platyrrhini, Primates). Molecular Phylogenetics and Evolution, 40(1), 274–280. doi:10.1016/j.ympev.2005.11.015.

    Article  PubMed  CAS  Google Scholar 

  • Orme, C. D. L., Freckleton, R. P., Thomas, G. H., Petzoldt, T., Fritz, S. A. & Isaac, N. J. B. (2012). Caper: Comparative analyses of phylogenetics and evolution. In R. R package version 0.5. Available: http://cran.r-project.org/web/packages/caper/index.html. Accessed 28 June 2012.

  • Oster, G., & Alberch, P. (1982). Evolution and bifurcation of developmental programs. Evolution, 36(3), 444–459. doi:10.2307/2408093.

    Article  Google Scholar 

  • Parker, J. (2011). Morphogens, nutrients, and the basis of organ scaling. Evolution & Development, 13(3), 304–314. doi:10.1111/j.1525-142X.2011.00481.x.

    Article  Google Scholar 

  • Pereira, T. V., Salzano, F. M., Mostowska, A., Trzeciak, W. H., Ruiz-Linares, A., Chies, J. A. B., et al. (2006). Natural selection and molecular evolution in primate PAX9 gene, a major determinant of tooth development. Proceedings of the National Academy of Sciences, 103(15), 5676–5681. doi:10.1073/pnas.0509562103.

    Article  CAS  Google Scholar 

  • Perelman, P., Johnson, W. E., Roos, C., Seuánez, H. N., Horvath, J. E., Moreira, M. A. M., et al. (2011). A molecular phylogeny of living primates. PLoS Genetics, 7(3), e1001342. doi:10.1371/journal.pgen.1001342.

    Article  PubMed  CAS  Google Scholar 

  • Perez, S. I., Klaczko, J., & dos Reis, S. F. (2012). Species tree estimation for a deep phylogenetic divergence in the New World monkeys (Primates: Platyrrhini). Molecular Phylogenetic and Evolution, 65, 621–630. doi:10.1016/j.ympev.2012.07.014.

    Article  Google Scholar 

  • Plavcan, J. M. (1990). Sexual dimorphism in the dentition of extant anthropoid primates. Ph.D. Dissertation, University of Michigan Microfilms.

  • Plavcan, J. M., & Gomez, A. (1993). Dental scaling in the callitrichinae. International Journal of Primatology, 14(1), 177–192. doi:10.1007/BF02196511.

    Article  Google Scholar 

  • Plikus, M. V., Zeichner-David, M., Mayer, J.-A., Reyna, J., Bringas, P., Thewissen, J. G. M., et al. (2005). Morphoregulation of teeth: Modulating the number, size, shape and differentiation by tuning Bmp activity. Evolution & Development, 7(5), 440–457. doi:10.1111/j.1525-142X.2005.05048.x.

    Article  CAS  Google Scholar 

  • Polly, P. D. (2007). Evolutionary biology: Development with a bite. Nature, 449(7161), 413–415. doi:10.1038/449413a.

    Article  PubMed  CAS  Google Scholar 

  • R-Development Core Team (2012). R: A language and environment for statistical computing. R Foundation for statistical Computing, Vienna, Austria. http://www.R-project.org/.

  • Renvoisé, E., Evans, A. R., Jebrane, A., Labruère, C., Laffont, R., & Montuire, S. (2009). Evolution of mammal tooth patterns: New insights from a developmental prediction model. Evolution, 63(5), 1327–1340. doi:10.1111/j.1558-5646.2009.00639.x.

    Article  PubMed  Google Scholar 

  • Rohlf, F. J. (2001). Comparative methods for the analysis of continuous variables: Geometric interpretations. Evolution, 55(11), 2143–2160. doi:10.1111/j.0014-3820.2001.tb00731.x.

    PubMed  CAS  Google Scholar 

  • Rosenberger, A. L. (1984). Fossil New World monkeys dispute the molecular clock. Journal of Human Evolution, 13(8), 737–742. doi:10.1016/S0047-2484(84)80023-8.

    Article  Google Scholar 

  • Rosenberger, A. L. (1992). Evolution of feeding niches in New World monkeys. American Journal of Physical Anthropology, 88(4), 525–562. doi:10.1002/ajpa.1330880408.

    Article  PubMed  CAS  Google Scholar 

  • Rosenberger, A. L., Tejedor, M. F., Cooke, S., Halenar, L., & Pekar, S. (2009). Platyrrhine ecophylogenetics in space and time. In P. A. Garber, A. Estrada, J. C. Bicca-Marques, E. W. Heymann, & K. B. Strier (Eds.), South American primates: Comparative perspectives in the study of behavior, ecology and conservation (pp. 69–113). New York: Springer.

    Google Scholar 

  • Salazar-Ciudad, I., & Jernvall, J. (2010). A computational model of teeth and the developmental origins of morphological variation. Nature, 464(7288), 583–586. doi:10.1038/nature08838.

    Article  PubMed  CAS  Google Scholar 

  • Shingleton, A. W. (2011). Evolution and the regulation of growth and body size. In T. Flatt & A. Heyland (Eds.), Mechanisms of life history evolution. The genetics and physiology of life history traits and trade-offs (pp. 43–55). Oxford: Oxford University Press.

    Google Scholar 

  • Smith, B. H. (1989). Dental development as a measure of life history in primates. Evolution, 43(3), 683–688. doi:10.2307/2409073.

    Article  Google Scholar 

  • Smith, R. J., & Jungers, W. L. (1997). Body mass in comparative primatology. Journal of Human Evolution, 32(6), 523–559. doi:10.1006/jhev.1996.0122.

    Article  PubMed  CAS  Google Scholar 

  • Tejedor, M. F. (2008). The origin and evolution of Neotropical primates. Arquivos do Museu Nacional, 66, 251–269.

    Google Scholar 

  • Tummers, M., & Thesleff, I. (2009). The importance of signal pathway modulation in all aspects of tooth development. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 312B(4), 309–319. doi:10.1002/jez.b.21280.

    Article  PubMed  Google Scholar 

  • Ungar, P. S. (2007). Dental functional morphology: The known, the unknown and the unknowable. In P. S. Ungar (Ed.), Evolution of the human diet: The known, the unknown, and the unknowable, human evolution series (pp. 39–55). Oxford: Oxford University Press.

    Google Scholar 

  • Wagner, G. P., & Altenberg, L. (1996). Perspective: Complex adaptations and the evolution of evolvability. Evolution, 50(3), 967–976. doi:10.2307/2410639.

    Article  Google Scholar 

  • Wildman, D. E., Jameson, N. M., Opazo, J. C., & Yi, S. V. (2009). A fully resolved genus level phylogeny of Neotropical primates (Platyrrhini). Molecular Phylogenetics and Evolution, 53(3), 694–702. doi:10.1016/j.ympev.2009.07.019.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, L. A. B., Madden, R. H., Kay, R. F., & Sánchez-Villagra, M. R. (2012). Testing a developmental model in the fossil record: Molar proportions in South American ungulates. Paleobiology, 38, 308–321. doi:10.1666/11001.1.

    Article  Google Scholar 

  • Wilson, D. E., & Reeder, D. M. (Eds.). (2005). Mammal species of the world: A taxonomic and geographic reference (3rd ed.). Baltimore, MD: Johns Hopkins University Press.

    Google Scholar 

Download references

Acknowledgments

The authors would like to acknowledge the contribution of Michael Plavcan for providing dental measurements for several of the species analyzed here and for reading and commenting on the manuscript. This work was supported by Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de La Plata and Grants from the FONCyT, PICT-2011-0307 (V. B and S. I. P). P. N. G was supported by a fellowship from Alberta Innovates Health Solutions and the CIHR Training Program in Genetics, Child Development and Health (Alberta Children’s Hospital).

Conflict of interest

The authors have no conflict of interest to declare.

Author information

Authors and Affiliations

  1. División Antropología, Museo de La Plata, Universidad Nacional de La Plata, CONICET, Paseo del Bosque s/n, 1900, La Plata, Argentina

    Valeria Bernal & S. Ivan Perez

  2. Department of Cell Biology and Anatomy, University of Calgary, 3280 Hospital Drive NW, Calgary, AB, T2N 4Z6, Canada

    Paula N. Gonzalez

  3. Facultad de Ciencias Veterinarias, Instituto de Genética Veterinaria, UNLP-CCT La Plata, CONICET, La Plata, Argentina

    Paula N. Gonzalez

Authors
  1. Valeria Bernal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paula N. Gonzalez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Ivan Perez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Valeria Bernal.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 29 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bernal, V., Gonzalez, P.N. & Perez, S.I. Developmental Processes, Evolvability, and Dental Diversification of New World Monkeys. Evol Biol 40, 532–541 (2013). https://doi.org/10.1007/s11692-013-9229-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-013-9229-4

Keywords

Search

Navigation