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

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.

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References

  1. 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 

  2. 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.

    PubMed  Article  CAS  Google Scholar 

  3. 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.

    PubMed  Article  Google Scholar 

  4. 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.

    PubMed  Article  CAS  Google Scholar 

  5. 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.

    PubMed  Article  Google Scholar 

  6. 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.

    PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  9. 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.

    PubMed  Article  Google Scholar 

  10. 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.

    PubMed  Article  Google Scholar 

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

    Google Scholar 

  12. 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 

  13. 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 

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

    Google Scholar 

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

    PubMed  Article  Google Scholar 

  16. 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 

  17. 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.

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  Google Scholar 

  19. 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 

  20. 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.

    PubMed  Article  CAS  Google Scholar 

  21. 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 

  22. 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.

    PubMed  Article  CAS  Google Scholar 

  23. 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.

    PubMed  Article  CAS  Google Scholar 

  24. 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.

    PubMed  Article  Google Scholar 

  25. 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 

  26. 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.

    PubMed  Article  CAS  Google Scholar 

  27. 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 

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

    PubMed  Article  Google Scholar 

  29. 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.

    PubMed  Article  CAS  Google Scholar 

  30. 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.

    PubMed  Article  CAS  Google Scholar 

  31. 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.

    PubMed  Article  CAS  Google Scholar 

  32. 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.

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

    Article  Google Scholar 

  34. 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 

  35. 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 

  36. 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.

    PubMed  Article  CAS  Google Scholar 

  37. 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 

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

  39. 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 

  40. 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 

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

    PubMed  Article  CAS  Google Scholar 

  42. 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/.

  43. 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.

    PubMed  Article  Google Scholar 

  44. 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 

  45. 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 

  46. 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.

    PubMed  Article  CAS  Google Scholar 

  47. 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 

  48. 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.

    PubMed  Article  CAS  Google Scholar 

  49. 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 

  50. 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 

  51. 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.

    PubMed  Article  CAS  Google Scholar 

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

    Google Scholar 

  53. 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.

    PubMed  Article  Google Scholar 

  54. 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 

  55. 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 

  56. 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.

    PubMed  Article  CAS  Google Scholar 

  57. 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 

  58. 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 

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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).

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The authors have no conflict of interest to declare.

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Correspondence to Valeria Bernal.

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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

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Keywords

  • Evo-devo
  • Inhibitory cascade model
  • Primates
  • Molar ratios
  • Phylogenetic generalized least-squares model