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

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Abstract

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.

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References

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Baylac M. 2007. Rmorph: a R geometric and multivariate morphometrics library.baylac@mnhn.fr

  • 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.

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • Bookstein F. L. 1991. Morphometric tools for landmark data: geometry and biology. Cambridge University Press, NY: 1–455.

    Google Scholar 

  • Bookstein F. L. 1996. Biometrics biomathematics and the morphometric synthesis. Bulletin of Mathematical Biology 58: 313–365.

    Article  CAS  PubMed  Google Scholar 

  • Bouvier M. and Hylander W. 1996. The function of secondary osteonal bone. Mechanical or metabolic? Archives of Oral Biology 41: 941–950.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Cook M. J. 1965. The anatomy of the laboratory mouse. Academic Press Inc., U. S., London and NY: 1–143.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Debat V. and David P. 2001. Mapping phenotypes: canalization, plasticity and developmental stability. Trends in Ecology and Evolution 16: 555–561.

    Article  Google Scholar 

  • Delany M. J. 1975. The rodents of Uganda. Trustees of British Museum (Natural History), London 746: 1–165.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Flury B. N. 1984. Common principal components in k groups. Journal of the American Statistical Association 79: 892–898.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Gliwicz J. 1987. Niche segragation in rodent community of Africian dry savanna. Journal of Mammalogy 68: 169–172.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • Le Louarn H. 1971. Détermination de l’age par la pesée des cristallins chez quelques espęces de rongeurs. Mammalia 35: 636–643.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Morris P. 1972. A review of mammalian age determination methods. Mammal Review 2 (3): 69–104.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • Nei M. 1987. Molecular evolutionary genetics. Columbia University Press, NY: 1–512.

    Google Scholar 

  • Palmer A. R. and Strobeck. C. 1986. Fluctuating asymmetry: measurement, analysis, patterns. Annual review of Ecology and Systematics 17: 441–457.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Piersma T. and Drent J. 2003. Phenotypic flexibility and the evolution of organismal design. Trends in Ecology and Evolution 18: 228–233.

    Article  Google Scholar 

  • Polly P. D. 2007. Phylogeographic differentiation inSorex Araneus: morphology in relation to geography and karyotype. Russian Journal of Theriology 6: 73–84.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • Rohlf F. J and Slice D. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39: 40–59.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Watterson G. A. 1978. The homozygosity test of neutrality. Genetics 88: 405–417.

    CAS  PubMed  Google Scholar 

  • Weir B. S. and Cockerham C. C. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. UMR CNRS 5202 - USM 601, Origine, Structure et Evolution de la Biodiversité, Département Systématique et Evolution, Muséum National d’Histoire Naturelle, CP 51, 55 rue Buffon, 75005, Paris, France

    Aude Lalis, Michel Baylac & Christiane Denys

  2. Plate-forme Morphométrie MNHN-CNRS IFR, 10145, rue Buffon, F-75005, Paris, France

    Aude Lalis & Michel Baylac

  3. Centre de Biologie et Gestion des Populations (UMR22), INRA, Campus International de Baillarguet, CS30016, 34988, Montferrier sur Lez cedex, France

    Jean François Cosson

  4. Rodent Research Project, Sokoine University of Agriculture, Morogoro, Tanzania

    Rhodes H. Makundi & Robert S. Machang’u

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  1. Aude Lalis
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  2. Michel Baylac
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  3. Jean François Cosson
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  4. Rhodes H. Makundi
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Correspondence to Aude Lalis.

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Lalis, A., Baylac, M., Cosson, J.F. et al. Cranial morphometric and fine scale genetic variability of two adjacentMastomys natalensis (Rodentia: Muridae) populations. Acta Theriol 54, 171–181 (2009). https://doi.org/10.1007/BF03193173

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