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Intraspecific variation and micro-macroevolution connection: illustration with the late Miocene genus Progonomys (Rodentia, Muridae)

  • Vincent Lazzari (a1), Jean-Pierre Aguilar (a2) and Jacques Michaux (a3)
Abstract

Recent progresses in our knowledge of mouse odontogenesis have enhanced rodent tooth morphology as a model for Evo-Devo studies. Deciphering the connection between macroevolution and microevolution, however, especially in the case of mammalian teeth, requires examples to illustrate how morphological differences among species, or higher taxa, can stem from population-level processes. In this paper we use paleontological material to study intraspecific variation of tooth morphology in the late Miocene species Progonomys clauzoni, over a short span of geological time in a restricted area. Progonomys is of particular interest as a stem genus of all murine rodents (Old World rats and mice). We use morphometrical and statistical methods to illustrate how change in the amplitude in variation at the population level through geological time is associated with the emergence of new characters. Some of these new characters, including functional ones, become fixed in parallel in distinct murine lineages. Nine million years ago, Progonomys clauzoni displayed variational properties of the developmental system shared by the Murinae, which can also explain some singular tooth characteristics that now are scattered among the diverse lineages. Further morphometric studies, however, are necessary to explain how the variety of cusp patterns observed in Progonomys clauzoni can be explained by developmental properties.

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Aguilar, J. P., Calvet, M., and Michaux, J. 1986. Description des rongeurs Pliocènes de la faune du Mont-Hélène (Pyrénées-Orientales, France), nouveau jalon entre les faunes de Perpignan (Serrat d'en Vacquer) et de Sète. Palaeovertebrata 16:127144.
Aguilar, J. P., and Michaux, J. 1996. The beginning of the age of Murinae (Mammalia: Rodentia) in southern France. Acta Zoologica Cracoviensia 39:3545.
Aguilar, J. P., Calvet, M., and Michaux, J. 1991. Présence de Progonomys (Muridae, Rodentia, Mammalia) dans une association de rongeurs de la fin du Miocene moyen (Castelnou 1B; Pyrénées-Orientales, France). Geobios 24:503508.
Aguilar, J. P., Lazzari, V., Michaux, J., Sabatier, M., and Calvet, M. 2007a. Lo Fournas 16-M (Miocène supérieur) et Lo Fournas 16-P (Pliocène moyen), nouvelles localités karstiques à Baixas, Sud de la France, Part. I. Particularités et implications géodynamiques. Géologie de la France 1:5562.
Aguilar, J. P., Michaux, J., and Lazzari, V. 2007b. Lo Fournas 16-M (Miocène supérieur) et Lo Fournas 16-P (Pliocène moyen), nouvelles localités karstiques à Baixas, Sud de la France. Part. II — Les faunes de rongeurs et les nouvelles espèces. Géologie de la France 1:6381.
Agustí, J., and Solà, S. Moyà 1991. Spanish Neogene mammal succession and its bearing on continental biochronology. Newsletter on Stratigraphy 25:91114.
Ameur, R., Jaeger, J.-J., and Michaux, J. 1976. Radiometric age of early Hipparion fauna in North-West Africa. Nature 261:3839.
Bookstein, F. L., Gingerich, P. D., and Kluge, A. G. 1978. Hierarchical linear modeling of the tempo and mode of evolution. Paleobiology 4:120134.
Bruijn, H. de., Sondaar, P., and Zachariasse, W. J. 1971. Mammalia and Foraminifera from the Neogene of Kastellios Hill (Crete): a correlation of continental and marine biozones. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen B 74:122.
Bush, A., Powell, M. G., Arnold, W. S., Bert, T. M., and Daley, G. M. 2002. Time-averaging, evolution, and morphological variation. Paleobiology 28:925.
Butler, P. M. 1985. Homology of cusps and crests, and their bearing on assessments of rodent phylogeny. Pp. 381401 in Luckett, W. P. and Hartenberger, J.-L., eds. Evolutionary relationships among rodents. Plenum, New York.
Charles, C. 2008. Evo-Dévo des dents chez les rongeurs murinés: des gènes à la morphologic . Université de Poitiers, Poitiers.
Charles, C., Pantalacci, S., Peterkova, R., Tafforeau, P., Laudet, V., and Viriot, L. 2009a. Effect of eda loss of function on upper jugal tooth morphology. Anatomical Record 292:299308.
Charles, C., Pantalacci, S., Tafforeau, P., Headon, D., Laudet, V., and Viriot, L. 2009b. Distinct Impacts of Eda and Edar Loss of Function on the Mouse Dentition. PLOS One 4(4):e4985. doi:10.1371/journal.pone.0004985.
Cheema, I. U., Raza, S. Mahmood, Flynn, L. J., Rapjar, A. R., and Tomida, Y. 2000. Miocene small mammals from Jalalpur, Pakistan, and their biochronologic implications. Bulletin of the National Science Museum, Tokyo, C 26:5777.
Crampton, J. S. 1995. Elliptic Fourier shape analysis of fossil bivalves: some practical considerations. Lethaia 28:179186.
Darwin, C. 1859. The origin of species by means of natural selection. John Murray, London.
Faillat, J.-P., Aguilar, J. P., Calvet, M., and Michaux, J. 1990. Les fissures à remplissages fossilifères néogènes du plateau de Baixas (Pyrénées-Orientales, France), témoins de la distension oligo-miocène. Comptes Rendus de l'Académie des Sciences de Paris II 311:205212.
Farjanel, G., and Mein, P., 1984. Une association de mammifères et de pollens dans la formation des ‘Marnes de Bresse’ d'âge Miocène supérieur, à Ambérieu (Ain). Géologie de la France 1–2:131148.
Goodwin, H. T. 1998. Supernumerary teeth in Pleistocene, recent, and hybrid individuals of the Spermophilus richardsonii complex (Sciuridae). Journal of Mammalogy 79:11611169.
Hammer, Ø., Harper, D. A. T., and Ryan, P. D. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4. http://palaeo-electronica.org/2001_1/past/issue1_01.htm
Horacek, I., Mihevc, A., Hajna, N. Zupan, Pruner, P., and Bosak, P. 2007. Fossil vertebrates and paleomagnetism update of one of the earlier stages of cave evolution in the classical karst, Slovenia: Pliocene of Crnotice II in Raciske Pecine. Acta Carsologica 36:453468.
Hunt, G. 2004. Phenotypic variance in inflation of fossil samples: an empirical assessment. Paleobiology 30:487506.
Jacobs, L. L. 1977. A new genus of murid from the Miocene of Pakistan and comments on the origin of the Muridae. PaleoBios 25:111.
Jacobs, L. L. 1978. Fossil rodents (Rhizomyidae and Muridae) from Neogene Siwalik deposits, Pakistan. Museum of Northern Arizona Bulletin 52:1103.
Jacobs, L. L., Flynn, L. J., and Downs, W. R. 1989. Neogene Rodentia of Southern Asia. In Black, C. C. and Dawson, M. R., eds. Papers on fossil rodents in honor of Albert Elmer Wood. Natural History Museum, Los Angeles County, Science Series No. 33:157177.
Jernvall, J. 2000. Linking development with generation of novelty in mammalian teeth. Proceedings of the National Academy of Sciences USA 97:26412645.
Jernvall, J., and Jung, H.-S. 2000. Genotype, Phenotype, and Developmental Biology of Molar Tooth Characters. Yearbook of Physical Anthropology 43:171190.
Jernvall, J., and Thesleff, I. 2000. Reiterative signaling and patterning during mammalian tooth morphogenesis. Mechanisms of Development 92:1929.
Jernvall, J., Keränen, S., and Thesleff, I. 2000. Evolutionary modification of development in mammalian teeth: Quantifying gene expression patterns and topography. Proc. Natl. Acad. Sci. USA 97:1444414448.
Kangas, A. T., Evans, A. R., Thesleff, I., and Jernvall, J. 2004. Nonindependence of mammalian dental characters. Nature 432:211214.
Kuhl, F. P., and Giardina, C. R. 1982. Elliptic Fourier features of a closed contour. Computer Graphics and Image Processing 18:236258.
Lazzari, V., Tafforeau, P., Aguilar, J. P., and Michaux, J. 2008. Topographic maps applied to comparative molar morphology: the case of murine and cricetine dental plans (Rodentia, Muroidea). Paleobiology 34:4664.
Lecompte, E., Aplin, K., Denys, C., Catzeflys, F., Chades, M., and Chevret, P. 2008. Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences, with a new tribal classification of the subfamily. BMC Evolutionary Biology 8:199. http://www.biomedcentral.com/1471–2148/8/199
MacFadden, B. J. 1989. Dental character variation in paleopopulations and morphospecies of fossil horses and extant analogs. Pp. 128141 in Prothero, D. R. and Schoch, R. M., eds. The evolution of perissodactyls. Oxford University Press, New York.
Marcus, L. F. 1993. Some aspects of multivariate statistics for morphometrics. Pp. 95130 in Marcus, L. F., Bello, E., and Garcia-Valdecasas, A., eds. Contribution to morphometrics. Museo National de Ciencas Naturales, Madrid.
Martin, R. E. 1999. Taphonomy: a process approach. Cambridge University, Cambridge.
Mein, P. 1999. The Late Miocene small mammal succession from France, with emphasis on the Rhone Valley localities. Pp. 140164 in Agustí, J., Rook, L., and Andrews, P., eds. Hominoid evolution and climatic change in Europe. Vol. 1. The evolution of Neogene terrestrial ecosystems in Europe. Cambridge University Press, Cambridge.
Michaux, J. 1967. Origine du dessin dentaire “Apodemus“ (Rodentia, Mammalia). Comptes Rendus de l'Académie des Sciences de Paris II 264:711714.
Michaux, J. 1971. Muridae (Rodentia) néogènes d'Europe sudoccidentale. Evolution et rapport avec les formes actuelles. Paléobiologie Continentale II 167.
Miller, E. S. 1912. Catalogue of the mammals of Western Europe in the collection of the British Museum. British Museum, London.
Misonne, X. 1969. African and Indo-Australian Muridae: evolutionary trends. Annales du Musée Royal de l'Afrique Centrale, Tervuren, Belgium, série IN–8, Sciences Zoologiques 172:1219.
Musser, G. G., and Carleton, M. D. 2005. Superfamily Muroidea. Pp. 8941531 in Wilson, D. E. and Reeder, D. M., eds. Mammal species of the world, 3d ed. John Hopkins University Press, Baltimore.
Polly, P. D. 1998. Variability, selection, and constraints: development and evolution in viverravid (Carnivora, Mammalia) molar morphology. Paleobiology 24:409429.
Qiu, Z. D., Zheng, S. H., Sen, S., and Zhang, Z. Q. 2003. Late Miocene micromammals from the Bahe Formation, Lantian, China. DEINSEA 10:443454.
Renaud, S., Michaux, J., Jaeger, J.-J., and Auffray, J.-C. 1996. Fourier analysis applied to Stephanomys (Rodentia, Muridae) molars: non progressive evolutionary pattern in a gradual lineage. Paleobiology 22:255265.
Renaud, S., Benammi, M., and Jaeger, J.-J. 1999a. Morphological evolution of the murine rodent Paraethomys in reponse to climatic variations (Mio-Pleistocene of North Africa). Paleobiology 25:369382.
Renaud, S., Michaux, J., Mein, P., Aguilar, J. P., and Auffray, J.-C. 1999b. Patterns of size and shape differentiation during the evolutionary radiation of the European murine rodents. Lethaia 32:6171.
Renaud, S., Michaux, J., Schmidt, D. N., Aguilar, J. P., Mein, P., and Auffray, J.-C. 2005. Morphological evolution, ecological diversification and climate change in rodents. Proceedings of the Royal Society of London B 272:607617.
Renaud, S., Auffray, J.-C., and Michaux, J. 2006. Conserved phenotypic variation patterns, evolution along lines of least resistance, and departure due to selection in fossil rodents. Evolution 60:17011717.
Simpson, G. G. 1937. Patterns of phyletic evolution. Geological Society of America Bulletin 48:303313.
Simpson, G. G., Roe, A., and Lewontin, R. C. 1960. Quantitative zoology. Harcourt, Brace and Co., New York.
Steppan, S. J., Adkins, R. M., and Anderson, J. 2004. Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Systematic Biology 53:533553.
Storch, G. 1987. The Neogene mammalian faunas of Ertemte and Harr Obo in Inner Mongolia (Nei Mongol), China. 7. Muridae (Rodentia). Lethaia 67:401431.
Storch, G., and Ni, X. 2002. New Late Miocene murids from China (Mammalia, Rodentia). Geobios 35:515521.
Van Dam, J. A. 1997. The small mammals from the Upper Miocene of the Teruel-Alfambra region (Spain): paleobiology and paleoclimatic reconstructions. Geologica Ultraiectina 156:1204.
Van de Weerd, A. 1976. Rodent faunas of the Mio-Pliocene continental sediments of the Teruel–Alfambra region, Spain. Utrecht Micropaleontoly Bulletins, Special Publication 2:1217.
Vianey-Liaud, M., and Legendre, S. 1986. Les faunes des phosphorites du Quercy: principes méthodologiques en paléontologie des mammifères; homogénéité chronologique des gisements de mammifères fossiles. Eclogae Geologicae Helvetiae 79:917944.
Weiss, K. M., Stock, D. W., and Zhao, Z. 1998. Dynamic interactions and the evolutionary genetics of dental patterning. Critical Reviews in Oral Biology and Medicine 9:369398.
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