Correlation structure of the cheek teeth enamel crown patterns in the genus Equus (Mammalia: Equidae): an analysis by geometric morphometrics with outline points

Correlation structure of the cheek teeth enamel crown patterns in the genus Equus (Mammalia: Equidae): an analysis by geometric morphometrics with outline points

Pavlinov I.Ya., Spasskaya N.N.

P. 70-81

Correlation structure of the cheek teeth enamel crown patterns in the genus Equus was studied by means of geometric morphometrics using outline points as descriptors to reveal the levels of morphological integration of the toothrow elements. Crown patterns in 34 upper and 31 lower toothrows (260 teeth in total) from 30 horse species were analyzed, the respective sets of 70 to 150 outline points were processed using the elliptic Fourier, principal component, and cluster analyses. The most correlated were shown to be the serial homologous crown elements within premolar and molar toothrow portions and less across the total toothrow. Correlation between occluding upper and lower teeth was shown to be low. Such correlation structure allowed identifying several levels of integration of the cheek teeth crown patterns in the genus Equus. A possibility of considering the serial homologous crown elements as the modules of the evolutionary developmental structure of the equine toothrows was discussed. Certain perspectives of similar studies in the specialized artiodactyles were emphasized.DOI: 10.15298/rusjtheriol.20.1.08

Литература
  • Alberdi M.T., Arroyo-Cabrales J., Marín-Leyva A.H. & Polaco O.J. 2014. Study of Cedral horses and their place in the Mexican Quaternary // Revista Mexicana de Ciencias Geológicas. Vol.31. No.2. P.221–237.
  • Azzaroli A. 1989. The genus Equus in Europe // Lindsay E.H., Fahlbusch V. & Mein P. (eds.). European Neogene mammal chronology. New York: Plenum Press. P.339–356.
  • Barrón-Ortiz C.I., Rodrigues A.T., Theodor J.M., Kooyman B.P., Yang D.Y. & Speller C.F. 2017. Cheek tooth morphology and ancient mitochondrial DNA of late Pleistocene horses from the western interior of North America: Implications for the taxonomy of North American Late Pleistocene Equus // PLoS ONE. Vol.12. No.8. e0183045.
  • Berg R.L. 1960. The ecological significance of correlation pleiades // Evolution. Vol.14. No.1. P.171–180.
  • Berkovitz B.K.B. & Shellis R.P. 2018. The teeth of mammalian vertebrates. London: Academic Press. 346 p.
  • Bernor R.L., Cirilli O., Jukar A.M., Potts R., Buskianidze M. & Rook L. 2019. Evolution of early Equus in Italy, Georgia, the Indian subcontinent, East Africa, and the origins of African zebras // Frontiers in Ecology and Evolution. Vol.7. P.166.
  • Bolker J.A. 2000. Modularity in development and why it matters to evo-devo // American Zoologist. Vol.40. No.5. P.770–776.
  • Bonnet E. & de Peer Y. 2002. Zt: A software tool for simple and partial Mantel tests // Journal of Statistical Softwear. Vol.7. No.10. P.1–12.
  • Bookstein F.L. 1991. Morphometric tools for landmark data: Geometry and biology. New York: Cambridge University Press. 435 p.
  • Bookstein F.L. 1997. Landmark methods for forms without landmarks: Localizing group differences in outline shape // Medical Image Analysis. Vol.1. No.3. P.225–243.
  • Boulbes N. & van Asperen E.N. 2019. Biostratigraphy and palaeoecology of European Equus // Frontiers in Ecology and Evolution. Vol.7. P.301.
  • Bravo-Cuevas V.M., Jiménez-Hidalgo E. & Priego-Vargas J. 2011. Taxonomía y hábito alimentario de Equus conversidens (Perissodactyla, Equidae) del Pleistoceno Tardío (Rancholabreano) de Hidalgo, centro de México // Revista Mexicana de Ciencias Geológicas. Vol.28. No.1. P.65–82.
  • Callebaut W. & Rasskin-Gutman D. 2005. Modularity. Understanding the development and evolution of natural complex systems. Cambridge (MA): The MIT Press. 472 p.
  • Cardini A. 2003. The geometry of the marmot (Rodentia: Sciuridae) mandible: Phylogeny and patterns of morphological evolution // Systematic Biology. Vol.52. No.2. P.186–205.
  • Cheverud J.M. 1982. Phenotypic, genetic, and environmental morphological integration in the cranium // Evolution. Vol.36. No.3. P.499–516.
  • Cheverud J.M. 1995. Morphological integration in the Saddle-Back Tamarin (Saguinus fuscicollis) cranium // The American Naturalist. Vol.145. No.1. P.63–89.
  • Cheverud J.M., Wagner G.P. & Dow M.M. 1989. Methods for the comparative analysis of variation patterns // Systematic Zoology. Vol.38. No.3. P.201–213.
  • Chuang R. & Bonhomme V. 2019. Rethinking the dental morphological differences between domestic equids // Journal of Archaeological Sciences. Vol.101. No.1. P.140–148.
  • Churcher C.S. 1993. Equus grevyi // Mammalian Species. No.453. P.1–9.
  • Cochard L.R. 1981. Patterns of size variation and correlation in the dentition of the red colobus monkey (Colobus badius) // American Journal of Physical Anthropology. Vol.54. No.1. P.139–146.
  • Cucchi T., Mohaseb A., Peigné S., Debue K., Orlando L. & Mashkour M. 2017. Detecting taxonomic and phylogenetic signals in equid cheek teeth: Towards new palaeontological and archaeological proxies // Royal Society Open Science. No.4. 160997.
  • Dalquest W.W. & Dame J.T.H. 1965. The Pleistocene horse, Equus conversidens // American Midland Naturalist. Vol.74. No.2. P.408–417.
  • Dayan T., Wool D. & Simberloff D. 2002. Variation and covariation of skulls and teeth: Modern carnivores and the interpretation of fossil mammals // Paleobiology. Vol.28. No.4. P.508–526.
  • Dyurst U. 1936. [Exterior of the horse]. Moscow-Leningrad: Selkhozgiz. 344 p. [in Russian].
  • Eisenmann V. 2020. Equidés monodactyles fossiles (Equus, Allohippus, Plesippus, Hippidion). https://vera-eisenmann.com/-equides-monodactyles-fossiles-equus-allohippus-plesippus-?lang=en
  • Ferson S.F., Rohlf F.J. & Koehn R.K. 1985. Measuring shape variation of two-dimensional outlines // Systematic Zoology. Vol.34. No.1. P.59–68.
  • Foronova I.V. 2002. Late quaternary equids (genus Equus) of South-western and South-central Siberia // Mashkour M. (ed.). Equids in time and space: Papers in honour of Véra Eisenmann. Oxford: Oxbow Books. P.20–30.
  • Gidley J.W. 1901. Tooth characters and revision of the North American species of the genus Equus // Bulletin of the American Museum of Natural History. Vol.14. P.91–142.
  • Gingerich P.D. & Winkler D.A. 1979. Patterns of variation and correlation in the dentition of the red fox, Vulpes vulpes // Journal of Mammalogy. Vol.60. No.4. P.691–704.
  • Gómez-Robles A. & Polly P.D. 2012. Morphological integration in the hominin dentition: evolutionary, developmental, and functional factors // Evolution. Vol.66. No.4. P.1024–1043.
  • Goswami A. 2006. Morphological integration in the carnivoran skull // Evolution. Vol.60. No.1. P.169–183.
  • Goswami A. & Polly P.D. 2010. Methods for studying morphological integration and modularity // The Paleontological Society Papers. Vol.16. P.213–243.
  • Gould S.J. & Garwood R.A. 1969. Levels of integration in mammalian dentitions: An analysis of correlations in Nesophontes micrus (Insectivora) and Oryzomys couesi (Rodentia) // Evolution. Vol.23. No.3. P.276–300.
  • Hall B.K. 1995. Homology and embryonic development // Hecht M.K., Macintyre R.J. & Clegg M.T. (eds.). Evolutionary Biology. Boston: Springer. P.1–36.
  • Hallgrímsson B., Jamniczky H., Young N.M., Rolian C., Parsons T.E., Boughner J.C. & Marcucio R.S. 2009. Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation // Evolutionary Biology. Vol.36. No.4. P.355–376.
  • Hammer Ø., Harper D. & Ryan P.D. 2001. PAST. PAleontological STatistics software package for education and data analysis // Palaeontologia Electronica. Vol.4. No.1. P.1–9.
  • Hay O.P. 1915. Contributions to the knowledge of the mammals of the Pleistocene of North America // Proceedings of the United States National Museum. Vol.48. No.2086. P.515–575.
  • Heck L., Wilson L.A.B., Evin A., Stange M. & Sánchez-Villagra M.R. 2018. Shape variation and modularity of skull and teeth in domesticated horses and wild equids // Frontiers in Zoology. Vol.15. P.14.
  • Hibbard C.W. 1953. Equus (Asinus) calobatus Troxell and associated vertebrates from the Pleistocene of Kansas // Transactions of the Kansas Academy of Science. Vol.56. No.1. P.111–126.
  • Hulbert R.C. 1995. Equus from Leisey Shell Pit La and other Irvingtonian localities from Florida // Bulletin of the Florida Museum of Natural History. Vol.37. No.17. P.553–602.
  • Jernvall J. 1995. Mammalian molar cusp patterns: Developmental mechanisms of diversity // Acta Zoologica Fennica. Vol.198. P.1–61.
  • Jernvall J. 2000. Linking development with generation of novelty in mammalian teeth // Proceedings of the National Academy of Sciences. Vol.97. P.2641–2645.
  • Jernvall J., Hunter J.P. & Fortelius M. 2000. Trends in the evolution of molar crown types in ungulate mammals: evidence from the Northern Hemisphere // Teaford M.F., Smith M.M. & Ferguson M.W.J. (eds.). Development, function and evolution of teeth. Cambridge (UK): Cambridge University Press. P.269–281.
  • Klingenberg C.P. 2005. Developmental constraints, modules and evolvability // Hallgrimsson B. & Hall B.K. (eds.). Variation: A central concept of biology. Oxford: Academic Press. P. 219–247.
  • Klingenberg C.P. 2008a. Morphological integration and developmental modularity // Annual Review of Ecology, Evolution, and Systematics. Vol.39. P.115–132.
  • Klingenberg C.P. 2008b. Novelty and “homology-free” morphometrics: What’s in a name? // Evolutionary Biology. Vol.35. No.1. P.186–190.
  • Klingenberg C.P. 2009. Morphometric integration and modularity in configurations of landmarks: Tools for evaluating a priori hypotheses // Evolution & Development. Vol.11. No.4. P.405–421.
  • Klingenberg C.P. 2014. Studying morphological integration and modularity at multiple levels: Concepts and analysis // Philosophical Transactions of the Royal Society B: Biological Sciences. Vol.369. No.1649. 20130249.
  • Kuhl F.P. & Giardina C.R. 1982. Elliptic Fourier analysis of a closed contour // Computer Graphics and Image Processing. Vol.18. No.3. P.236–258.
  • Kurtén B. 1953. On the variation and population dynamics of fossil and recent mammal populations // Acta Zoologica Fennica Vol.76. P.1–122.
  • Kurtén B., 1968. Pleistocene mammals of Europe. Chicago: Aldine. 217 p.
  • Labonne G., Navarro N., Laffont R., Chateau-Smith C. & Montuire S. 2014. Developmental integration in a functional unit: Deciphering processes from adult dental morphology // Evolution & Development. Vol.16. No.4. P.224–232.
  • Laffont R., Renvoise E., Navarro N., Alibert P. & Montuirea S. 2009. Morphological modularity and assessment of developmental processes within the vole dental row (Microtus arvalis, Arvicolinae, Rodentia) // Evolution & Development. Vol.11. No.3. P.302–311.
  • Laubichler M.D. & Maienschein J. 2008. Evolving pathways: Key themes in evolutionary developmental biology. New York: Cambridge University Press. 446 p.
  • 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. Vol.5. No.11. e15470.
  • Lyakh A.M. 2019. Analysis of biological shapes on the basis of coordinated coefficients of elliptic Fourier transformation // Science in the South of Russia. Vol.15. No.4. P.63–70
  • MacFadden B.J. 1993. Fossil horses: Systematics, paleobiology, and evolution of the family Equidae. Cambridge University Press, Cambridge (UK). 384 p.
  • MacFadden B.J. 2013 Dispersal of Pleistocene Equus (family Equidae) into South America and calibration of GABI 3 based on evidence from Tarija, Bolivia // PLoS ONE. Vol.8. No.3. e59277.
  • Magwene P.M. 2008. Using correlation proximity graphs to study phenotypic integration // Evolutionary Biology. Vol.35. No.3. P.191–198.
  • Mitteroecker P. 2009. The developmental basis of variational modularity: Insights from quantitative genetics, morphometrics, and developmental biology // Evolutionary Biology. Vol.36. No.4. P.377–385.
  • Mitteroecker P. & Gunz P. 2009. Advances in geometric morphometrics // Evolutionary Biology. Vol.36. No.4. P.235–247.
  • Monteiro L.R., Bonato V. & dos Reis S.F. 2005. Evolutionary integration and morphological diversification in complex morphological structures: Mandible shape divergence in spiny rats (Rodentia, Echimyidae) // Evolution & Development. Vol.7. No.5. P.429–439.
  • Murren C.J. 2002. Phenotypic integration in plants // Plant Species Biology. Vol.17. No.2–3. P.89–99.
  • Navarro N., Zararain X. & Montuire S. 2004. Effects of morphometric descriptor change on statistical classification and morphospaces // Biological Journal of the Linnean Society. Vol.83. No.2. P.243–260.
  • Olson E.C. & Miller R.L. 1958. Morphological integration. Chicago: University of Chicago Press. 376 p.
  • Parner E.T., Heidmann J.M., Kjær I., Væth M. & Poulsen S. 2002. Biological interpretation of the correlation of emergence times of permanent teeth // Journal of Dental Research. Vol.81. No.7. P.451–454.
  • Pavlicev M.C., James M. & Wagner G.P. 2009. Measuring morphological integration using eigenvalue variance // Evolutionary Biology. Vol.36. No.4. P.157–170.
  • Pavlinov I.Ya. 2011. Morphological disparity: An attempt to widen and to formalize the concept // Pavlinov I.Ya. (ed.). Research in biodiversity: Models and applications. Rejeka: InTech Open. P.341–364.
  • Pavlinov I.Ya. & Mikeshina N.G. 2002. [Principles and methods of geometric morphometrics] // Journal of General Biology. Vol.63. No.6. P.473–493. [in Russian, with English summary]
  • Pavlinov I.Ya., Nanova O.G. & Lissovsky A.A. 2008a. [Correlation analysis of the structure of the cheek toothrow in the Arctic fox (Alopex lagopus, Canidae)] // Zoological Journal. Vol.87. No.7. P.862–875. [in Russian, with English summary]
  • Pavlinov I.Ya., Nanova O.G. & Spasskaya N.N. 2008b. [To exploration of the morphological disparity of the measurable traits of the mammalian skull. 1. On the relation of different forms of the group variation] // Journal of General Biology. Vol.69. No.5. P.453–459. [in Russian, with English summary]
  • Pengilly D. 1984. Developmental versus functional explanations for patterns of variability and correlation in the dentitions of foxes // Journal of Mammalogy. Vol.65. No.1. P.34–43.
  • Prothero D.R. & Foss S.E. 2007. The evolution of artiodactyls. Baltimore: John Hopkins University Press. 384 p.
  • Renaud S., Pantalacci S., Quéré J.-P., Laudet V. & Auffrayd J.-C. 2009. Developmental constraints revealed by co-variation within and among molar rows in two murine rodents // Evolution & Development. Vol.11. No.5. P.590–602.
  • Rohlf F.J. 1993. Relative warps analysis and example of its application to mosquito wings // Marcus L.F., Bello E. & Garcia-Valdecasas A. (eds.). Contributions to morphometrics. Madrid: C.S.C.I. P.131–160.
  • Rohlf F.J. 2017. tpsDig2 ver. 2.31. State University at Stony Brook, New York, NY (program).
  • Rohlf F.J. 2019. tpsUtil ver. 1.78. State University at Stony Brook, New York, NY (program).
  • Rostova N.S. 2002. [Correlations, their structure and variability] // Trudy Sanct-Petersburg Soc. Naturalists. Vol.94. No.1. 306 p. [in Russian, with English summary]
  • Schlosser G. & Wagner G.P. 2004. Modularity in development and evolution. Chicago: University of Chicago Press. 600 p.
  • Seetah K., Cardini A. & Barker G. 2016. A “long-fuse domestication” of the horse? Tooth shape suggests explosive change in modern breeds compared with extinct populations and living Przewalski’s horses // The Holocene. Vol.26. No.8. P.1326–1333.
  • Soana S., Gnudi G. & Bertoni G. 1999. The teeth of the horse: Evolution and anatomo-morphological and radiographic study of their development in the foetus // Anatomia, Histologia, Embryologia. Vol.28. No.5–6. P.273–280.
  • Spasskaya N.N. & Pavlinov I.Ya. 2008. [Variation and correlations structure of the cheek toothrow in the Przewalski’s horse (Equus przewalskii; Mammalia: Equidae)] // Bulletin of Moscow Society of Naturalists. Biological series. Vol.113. No.2. P.3–13. [in Russian, with English summary]
  • StatSoft Inc. 2014. Statistica (Data Analysis Software System), Version 12 (program).
  • Stock D.W. 2001. The genetic basis of modularity in the development and evolution of the vertebrate dentition // Philosophical Transactions of the Royal Society B: Biological Sciences. Vol.356. No.1414. P.1633–1653.
  • Suna B., Deng T. & Liu Y. 2019. Early Pleistocene Equus (Equidae, Perissodactyla) from Andersson Loc. 32 in Qixian, Shanxi, China // Historical Biology. Vol.31. No.2. P.211–222.
  • Van Valen L. 1965. The study of morphological integration // Evolution. Vol.19. No.3. P.347–349.
  • Vasil’ev A.G., Vasil’eva I.A. & Shkurihin A.O. 2018. [Geometric morphometry: from theory to practice]. Moscow: KMK Scientific Press. 471 p. [in Russian]
  • Wagner G.P. & Altenberg L. 1996. Perspective: Complex adaptations and the evolution of evolvability // Evolution. Vol.50. No.3. P.967–976.
  • Young N.M. & Hallgrimsson B. 2005. Serial homology and the evolution of mammalian limb covariation structure // Evolution. Vol.59. No.12. P.2691–2704.
  • Zelditch M.L. & Swiderski D.L., Sheets H.D. 2012. Geometric morphometrics for biologists: A primer. 2nd ed. Amsterdam: Elsevier. 443 p.
  • Zelditch M.L., Wood, A.R. & Swiderski D.L. 2009. Building developmental integration into functional systems: Function-induced integration of mandibular shape // Evolutionary Biology. Vol.36. No.1. P.71–87.