Acta Theriologica

, Volume 54, Issue 2, pp 171–181 | Cite as

Cranial morphometric and fine scale genetic variability of two adjacentMastomys natalensis (Rodentia: Muridae) populations

  • Aude Lalis
  • Michel Baylac
  • Jean François Cosson
  • Rhodes H. Makundi
  • Robert S. Machang’u
  • Christiane Denys


The objective of this multidisciplinary project was to study the intra-specific morphometric and genetic variability between two adjacent populations ofMastomys natalensis Smith, 1834 living in different environments. The study of micro-evolutionary processes at work by using geometrical morphometrics allowed us to define two groups, characterized by different features of the skull shape. Using molecular microsatellites analysis, we showed that the two populations exchanged high gene flow and could be considered as a single panmictic unit. These results suggest that this widely-distributed species exhibits a local population-level differentiation in shape variation of skulls, probably due to different ecological situations. We speculate that the variability in the cranial characteristics (connected with the feeding ability) could reveal a local adaptation preferentially based on the food availability. We propose an explanation linking the shape differences to the fitness gain in the exploitation of resources available in the two environments. Since we suggest a potential differentiation process between populations, we believe that the two groups constitute even better models to understand the factors involved in the early stages of local adaptations.

Key words

Mastomys natalensis intra-specific variability skull shape variation geometric morphometrics genetic differentiation microsatellites analysis Tanzania Tanzania 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Airoldi J. P. and Flury B. K. 1988. An application of common principal component analysis to cranial morphometry ofMicrotus californicus andM. ochrogaster (Mammalia, Rodentia). Journal of Zoology, London 216: 21–36.CrossRefGoogle Scholar
  2. Alibert P., Fel-Clair F., Manolakou K., Britton-Davidian J. and Auffray J. C. 1997. Developmental stability, fitness, and trait size in laboratory hybrids between European subspecies of the house mouse. Evolution 51: 1284–1295.CrossRefGoogle Scholar
  3. Auffray J. C., Alibert P., Renaud S. and Bonhomme F. 1996. Fluctuating asymmetry in Mus musculus subspecific hybridization traditional and Procrustes comparative approach. [In: Advances in morphometrics. L. F. Marcus, M. Corti, A. Loy, G. J. P. Naylor and D. E. Slice, eds]. Ser. A Life Sci., Plenum Press, NY: 284: 275–283.Google Scholar
  4. Baylac M. 2007. Rmorph: a R geometric and multivariate morphometrics library.baylac@mnhn.frGoogle Scholar
  5. Baylac M. and Friess M. 2005. Fourier descriptors, Procrustes superimposition, and data dimensionality: An exemple of cranial shape analysis in modern human populations. [In: Modern morphometrics in physical anthropology. D. Slice, ed]. Kluwer 145–166.Google Scholar
  6. Beecher R. M., Corruccini R. S. and Freeman M. 1983. Cranio-facial correlates of dietary consistency in a nonhuman primate. Journal of Craniofacial Genetics and Developmental Biology 3: 193–202.PubMedGoogle Scholar
  7. Belkhir K. 1999. GENETIX (v4.04): A Windows program for population genetic analysis. Laboratorie Genome, Populations: Interactions UPR 5000 du CNRS, Universite Montpellier II, Montpellier (France).Google Scholar
  8. Bookstein F. L. 1991. Morphometric tools for landmark data: geometry and biology. Cambridge University Press, NY: 1–455.Google Scholar
  9. Bookstein F. L. 1996. Biometrics biomathematics and the morphometric synthesis. Bulletin of Mathematical Biology 58: 313–365.PubMedCrossRefGoogle Scholar
  10. Bouvier M. and Hylander W. 1996. The function of secondary osteonal bone. Mechanical or metabolic? Archives of Oral Biology 41: 941–950.PubMedCrossRefGoogle Scholar
  11. Cardini A. and O’Higgins P. 2004. Patterns of morphological evolution in Marmota (Rodentia, Sciuridae): geometric morphometrics of the cranium in the context of marmot phylogeny, ecology and conservation. Biological Journal of the Linnean Society 82: 385–407.CrossRefGoogle Scholar
  12. Cardini A., Tongiorgi P., Sala L. and O’Higgins P. 2003. Skull form and evolution in Marmota. [In: Adaptive strategies and diversity in marmots. R. Ramousse, D. Allainé and M. Le Berre, eds]. International Marmot Network, Lyon: 63–68.Google Scholar
  13. Cook M. J. 1965. The anatomy of the laboratory mouse. Academic Press Inc., U. S., London and NY: 1–143.Google Scholar
  14. Cordeiro-Estrela P., Baylac M., Denys C. and Marinho-Filho J. 2006. Inter-specific morphological patterns of skull variation between two sympatric brazilian vesper mice: a geometric morphometrics assessment. Journal of Mammalogy 87: 1270–1279.CrossRefGoogle Scholar
  15. Debat V., Alibert P., David P., Paradis E. and Auffray J. C. 2000. Independence between developmental stability and canalization in the skull of the house mouse. Proceedings of the Royal Society of London 267: 423–430.CrossRefGoogle Scholar
  16. Debat V. and David P. 2001. Mapping phenotypes: canalization, plasticity and developmental stability. Trends in Ecology and Evolution 16: 555–561.CrossRefGoogle Scholar
  17. Delany M. J. 1975. The rodents of Uganda. Trustees of British Museum (Natural History), London 746: 1–165.Google Scholar
  18. Demby A. H., Inapogui A., Kargbo K., Koninga J., Kourouma K., Kanu J., Coulibaly M., Wagoner K. D., Ksiazek T. G., Peters C. J., Rollin P. E. and Bausch D. G. 2001. Variability among pest species of rodent 179 Lassa Fever in Guinea II. Distribution and prevalence of Lassa virus infection in small mammals. Vector Borne and Zoonotic Diseases 1: 283–297.PubMedCrossRefGoogle Scholar
  19. Dobigny G., Baylac M. and Denys C. 2002. Geometric morphometrics, neural networks and diagnosis of sibling Taterillus species. Biological Journal of the Linnean Society 77:319–3277.CrossRefGoogle Scholar
  20. Dos Reis S. F., Duarte L. C., Monteiro L. R. and Von Zuben F. J. 2002a. Geographic variation in cranial morphology in Trichomys apereoides (Rodentia: Echimyidae). I. Geometric descriptors and patterns of variation in shape. Journal of Mammalogy 83: 333–344.CrossRefGoogle Scholar
  21. Dos Reis S. F., Duarte L. C., Monteiro L. R. and Von Zuben F. J. 2002b. Geographic variation in cranial morphology inTrichomys apereoides (Rodentia: Echimyidae). II. Geographic units, morphological discontinuities, and sampling gaps. Journal of Mammalogy 83: 345–353.CrossRefGoogle Scholar
  22. Duarte L. C., Monteiro L. R., Von Zuben F. J. and Dos Reis S. F. 2000. Variation in mandible shape inTrichomys Apereoides (Mammalia: Rodentia): geometric analysis of a complex morphological structure. Systematic Biology 49: 563–578.PubMedCrossRefGoogle Scholar
  23. Duplantier J. M. 1988. Biologie evolutive de populations du genre Mastomys au Sénégal. PhD thesis, Université des Sciences et techniques du Languedoc, Montpellier: 1–215.Google Scholar
  24. Dynes J., Magnan P., Bernathxez L. and Rodriguez M. A. 1999. Genetic and morphological variation between two forms of lacustrine brook charr. Journal of Fish Biology 54: 955–972.CrossRefGoogle Scholar
  25. Engström C., Kiliaridis S. and Thilander B. 1986. The relationship between masticatory muscle function and cranial morphology. II. A histological study in the growing rat fed a soft diet. European Journal of Orthodontics 8: 271–279.PubMedGoogle Scholar
  26. Flury B. N. 1984. Common principal components in k groups. Journal of the American Statistical Association 79: 892–898.CrossRefGoogle Scholar
  27. Galan M., Van Hooft W. F., Legrand D., Berthier K., Loiseau A., Granjon L. and Cosson J. F. 2004. A multiplex panel of microsatellite markers for widespread sub-Saharan rodents of the genus Mastomys. Molecular Ecology Notes 4: 321–323.CrossRefGoogle Scholar
  28. Gliwicz J. 1987. Niche segragation in rodent community of Africian dry savanna. Journal of Mammalogy 68: 169–172.CrossRefGoogle Scholar
  29. Gockel J., Harr B., Schlötterer C., Arnold W., Gerlach G. and Tautz D. 1997. Isolation and characterization of microsatellite loci fromApodemus flavicollis (Rodentia, Muridae) andClethrionomys glareolus (Rodentia, Cricetidae). Molecular Ecology 6: 597–599.PubMedCrossRefGoogle Scholar
  30. Granjon L., Duplantier J. M., Catalan J. and Britton-Davidian J. 1997. Systematics of the genusMastomys. Belgian Journal of Zoology 127: 7–18.Google Scholar
  31. Gratz N. G. 1997. The burden of rodent-borne diseases in Africa south of the Sahara. Belgian Journal of Zoology 127: 71–84.Google Scholar
  32. Herring S. W. 1993. Epigenetic and functional influences on skull growth. [In: The skull. Volume I. Development. J. Hanken and B. K. Hall, eds]. Univeristy of Chicago Press, Chicago: 153–206.Google Scholar
  33. Hinten G., Maguiri T., Rossetto M. and Baverstock P. 1999. Isolation and characterization of microsatellite loci from the bush rat,Rattus fuscipes greyii. Molecular Ecology 8: 1351–1362.PubMedGoogle Scholar
  34. Kiliaridis S., Engström C. and Thilander B. 1986. The relationship between masticatory muscle function and cranial morphology. I. A Cephalometric longitudinal analysis in the growing rat fed a soft diet. European Journal of Orthodontics 7: 273–283.Google Scholar
  35. Kilonzo B. S., Mbise T. J. and Makundi R. H. 1992. Plague in Lusho district, Tanzania, 1980–1988. Transactions of the Royal Society of Tropical Medecine and Hygiene 86: 444–445.CrossRefGoogle Scholar
  36. Kingsolver J. G., Pfennig D. W. and Servedio M. R. 2002. Migration, local adaptation and the evolution of plasticity. Trends in Ecology and Evolution 17: 540–541.CrossRefGoogle Scholar
  37. Lalis A., Lecompte E., Cornette R., Moulin S., Machangu R. S., Makundi R., Aniskine V. M. and Denys C. 2006. Polymorphism of age population structure of two wildMastomys natalensis (Rodentia: Muridae) Tanzanian habitat samples: a multicriteria comparison. Mammalia 70: 293–299.CrossRefGoogle Scholar
  38. Leary R. F. and Allendorf F. W. 1989. Fluctuating asymmetry as an indicator of stress in conservation biology. Trends in Ecology and Evolution 4: 214–217.CrossRefPubMedGoogle Scholar
  39. Leirs H. 1995. Population ecology ofMastomys natalensis (Smith, 1834). Implications for rodent control in Africa. PhD thesis, University of Antwerp, Brussels: 1–273.Google Scholar
  40. Leirs H., Stuyck J., Verhagen R. and Verheyen W. 1990. Seasonal variation in growth ofMastomys natalensis (Rodentia: Muridae) in Morogoro, Tanzania. African Journal of Ecology 28: 298–306.CrossRefGoogle Scholar
  41. Le Louarn H. 1971. Détermination de l’age par la pesée des cristallins chez quelques espęces de rongeurs. Mammalia 35: 636–643.CrossRefGoogle Scholar
  42. Lieberman D. E., Krovitz G. E., Yates F. W., Devlin M. and Claire M. S. 2004. Effects of food processing on masticatory strain and craniofacial growth in a retrognathic face. Journal of Human Evolution 46: 655–677.PubMedCrossRefGoogle Scholar
  43. Lima M., Stenseth N. C., Leirs H. and Jaksic F. M. 2003. Population dynamics of small mammals in semi-arid regions: a comparative study of demographic variability in two species. Proceedings of the Royal Society of London 270: 1997–2007.CrossRefGoogle Scholar
  44. Marchand H., Paillat G., Montuire S. and Butet A. 2003. Fluctuating asymmetry in bank vole populations (Rodentia, Arvicolinae) reflects stress caused by landscape fragmentation in the Mont Saint Michel Bay. Biological Journal of the Linnean Society 80: 37–44.CrossRefGoogle Scholar
  45. Monath T. P., Newhouse V. F., Kemp G. E., Setzer H. W. and Cacciapuoti A. 1974. Lassa virus isolation fromMastomys natalensis rodents during an epidemic in Sierra Leone. Science 185: 263–265.PubMedCrossRefGoogle Scholar
  46. Monteiro L. R., Duarte L. C. and Dos Reis S. F. 2003. Environmental correlates of geographical variation in skull and mandible shape of the punare ratTrichomys apereoides. Journal of Zoology, London 261: 47–57.CrossRefGoogle Scholar
  47. Monteiro L. R., Lessal G. and Abe A. S. 1999. Ontogenetic variation in skull shape ofTrichomys apereoides (Rodentia: Echimyidae). Journal of Mammalogy 80: 102–111.CrossRefGoogle Scholar
  48. Morris P. 1972. A review of mammalian age determination methods. Mammal Review 2 (3): 69–104.CrossRefGoogle Scholar
  49. Mossman A. C. and Waser P. M. 2001. Effects of habitat fragmentation on population genetic structure in the white-footed mouse (Peromyscus leucopus). Canadian Journal of Zoology 79: 285–295.CrossRefGoogle Scholar
  50. Mullin S. K., Taylor P. J. and Pillay N. 2004. Skull size and shape ofDasymys (Rodentia, Muridae) from sub-Saharan Africa. Mammalia 68: 185–220.CrossRefGoogle Scholar
  51. Mwanjabe P. S. and Leirs H. 1997. An early warning system for IPM-based rodent control in smallholder farming systems in Tanzania. Belgian Journal of Zoology 127 (Supplement): 49–58.Google Scholar
  52. Mwanjabe P. S., Sirima F. B. and Lusingu J. 2002. Crop losses due to outbreaks ofMastomys natalensis (Smith, 1834) Muridae, Rodentia, in the Lindi Region of Tanzania. International Biodeterioration and Biodegradation 49: 133–137.CrossRefGoogle Scholar
  53. Nei M. 1987. Molecular evolutionary genetics. Columbia University Press, NY: 1–512.Google Scholar
  54. Palmer A. R. and Strobeck. C. 1986. Fluctuating asymmetry: measurement, analysis, patterns. Annual review of Ecology and Systematics 17: 441–457.CrossRefGoogle Scholar
  55. Patton J. J. and Brylski P. V. 1987. Pocket gophers in alfalfa fields: causes and consequences of habitat-related body size variation. The American Naturalist 130: 493–506.CrossRefGoogle Scholar
  56. Piersma T. and Drent J. 2003. Phenotypic flexibility and the evolution of organismal design. Trends in Ecology and Evolution 18: 228–233.CrossRefGoogle Scholar
  57. Polly P. D. 2007. Phylogeographic differentiation inSorex Araneus: morphology in relation to geography and karyotype. Russian Journal of Theriology 6: 73–84.Google Scholar
  58. Poulet A. R. 1980. Détermination de l’âge par la pesée des cristallins chez cinq espęces de rongeurs Muridés et Gerbillidés de l’Ouest de l’Afrique. Mammalia 44: 381–398.CrossRefGoogle Scholar
  59. Pucek Z. and Lowe V. P. W. 1975. Age criteria in small mammals. [In: Small mammals: their productivity and population dynamics. F. B. Golley, K. Petrusewicz and L. Ryszkowski, eds]. Cambridge University Press, Cambridge: 55–72.Google Scholar
  60. Rahman Abdel E. H. A. 2005. Systematics of Nile ratsArvicanthis (Rodentia: Muridae) from Sudan. PhD thesis, University of KwaZulu-Natal, South Africa: 1–255.Google Scholar
  61. Raymond M. and Rousset F. 1995. Genepop (version1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248–249.Google Scholar
  62. Rohlf F. J. 2000. On the use of shape scales to compare morphometric methods. Hystrix, Italian Journal of Mammalogy, New Series 11: 8–24.Google Scholar
  63. Rohlf F. J and Slice D. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39: 40–59.CrossRefGoogle Scholar
  64. Smithers R. N. H. and Wilson V. J. 1979. Checklist and Atlas of the Mammals of Zimbabwe Rhodesia. Museum Memoir N9, National Museums and Monuments Rhodesia, Bulawayo: 1–147.Google Scholar
  65. Stenseth N. C., Leirs H., Mercelis S. and Mwanjabe P. 2001. Comparing strategies for controlling an African pest rodent: an empirically based theoretical study. Journal of Applied Ecology 38: 1020–1031.CrossRefGoogle Scholar
  66. Taylor P. J., Kumirai A. and Contrafatto G. 2005. Species with fuzzy borders: the taxonomic status and species limits of saunders’vlei rat,Otomys saundersiae Roberts, 1929 (Rodentia, Muridae, Otomyini). Mammalia 69: 297–322.CrossRefGoogle Scholar
  67. Watterson G. A. 1978. The homozygosity test of neutrality. Genetics 88: 405–417.PubMedGoogle Scholar
  68. Weir B. S. and Cockerham C. C. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.CrossRefGoogle Scholar
  69. Wood B. and Lieberman D. E. 2001. Craniodental variation in Paranthropus boisei: a developmental and functional perspective. American Journal of Physical Anthropology 116: 13–25.PubMedCrossRefGoogle Scholar
  70. Yamada K. and Kimmel D. B. 1991. The effect of dietary consistency on bone mass and turnover in the rgowing rat mandible. Archives of Oral Biology 36: 129–138.PubMedCrossRefGoogle Scholar
  71. Yu H. T. and Peng Y. H. 2002. Population differentiation and gene flow revealed by microsatellite DNA markers in the house mouse (Mus musculus castaneus) in Taiwan. Zoological Science 19: 475–483.PubMedCrossRefGoogle Scholar

Copyright information

© Mammal Research Institute, Bialowieza, Poland 2009

Authors and Affiliations

  • Aude Lalis
    • 1
    • 2
  • Michel Baylac
    • 1
    • 2
  • Jean François Cosson
    • 3
  • Rhodes H. Makundi
    • 4
  • Robert S. Machang’u
    • 4
  • Christiane Denys
    • 1
  1. 1.UMR CNRS 5202 - USM 601, Origine, Structure et Evolution de la Biodiversité, Département Systématique et EvolutionMuséum National d’Histoire NaturelleParisFrance
  2. 2.Plate-forme Morphométrie MNHN-CNRS IFRParisFrance
  3. 3.Centre de Biologie et Gestion des Populations (UMR22)INRAMontferrier sur Lez cedexFrance
  4. 4.Rodent Research ProjectSokoine University of AgricultureMorogoroTanzania

Personalised recommendations