Abstract
A total of 204 specimens belonging to eight species of the genus Lemniscomys were examined with standard morphometric measurements. Our results show that the seven Sub-Saharan species seem to follow a latitudinal gradient from the Center to the South of the African continent. The only North African species L. barbarus looks close to L. griselda and L. rosalia. We also applied a molecular analysis through PCR (Polymerase Chain Reaction) method for the amplification of the 16S rRNA gene. For the purpose of constructing a phylogenetic tree with Maximum Likelihood method, we extracted eight sequences from the GenBank library; seven belonging to the genus Lemniscomys and one to the genus Arvicanthis used as outgroup. We managed to identify a region comprised of 458 nucleotides of which 388 were common for all species and 70 were variable. The phylogenetic tree shows us that the sister group L. bellieri and L. macculus, is the most basal, while L. striatus and L. rosalia appears to be close to the sister group L. barbarus and L. zebra. We also noticed a difference between morphometric and molecular results; the latter are more in agreement with pelage patterns subdivision between Lemniscomys species. These differences can be explained by a high rate of phenotypic evolution that can surpass the molecular counterpart as in the case of the genus Gerbillus.
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References
Abiadh A (2012) Statut taxonomique du genre Gerbillus (Rongeurs, Gerbillinae) en Tunisie. Approches morphologique, cytogénétique et moléculaire. PhD Thesis, Faculty of Sciences of Tunis, Tunisia
Abiadh A, Chetoui M, Cheniti TL, Capanna E, Colangelo P (2010) Molecular phylogenetics of the genus Gerbillus (Rodentia, Gerbillinae): implication for systematics, taxonomy and chromosomal evolution. Mol Phylogenet Evol 56:513–518. https://doi.org/10.1016/j.ympev.2010.04.018
Bellier L, Gautun JC (1967) Notes sur les Lemniscomys de Côte d’Ivoire. Rev Zool Bot Afr 75:282–287
Ben Faleh A (2011) Étude systématique, biogéographique et génétique de la petite gerboise Jacculus jacculus en Tunisie. PhD thesis, Institute of Biotechnology of Monastir, Tunisia
Ben Faleh A, Cornette R, Annabi A, Saïd K, Denys C (2013) Patterns of size and shape skull variability in Tunisian populations of Jacculus jacculus. Acta Zool Bulg 65(2):217–223
Ben Salem I, Ben Ibrahim A, Chetoui M, Nouira S (2017) Morpho-geometric analysis of eight grass mouse species of the genus Lemniscomys (Rodentia: Muridae). Pakistan. J Zool 49(1):351–354. https://doi.org/10.17582/journal.pjz/2017.49.1.sc1
Boonstra R (2015) Rodentia. The Canadian encyclopedia. http://www.thecanadianencyclopedia.ca/en/article/rodentia/. Accessed 20 May 2016
Cainé L, Lima G, Pontes L, Abrantes D, Pereira M, Pinheiro MF (2006) Species identification by cytochrome b gene: casework samples. Int Congr Ser 1288:145–147. https://doi.org/10.1016/j.ics.2005.09.152
Carleton MD, Van der Straeten E (1997) Morphological differentiation among Subsaharan and north African populations of the Lemniscomys barbarus complex (Rodentia, Muridae). Proc Biol Soc Wash 110(4):640–680
Castiglia R, Fadda C, Corti M, Scanzani A, Verheyen W, Capanna E (2002) Chromosomal evolution in the African Arvicanthine rats (Murinae, Rodentia): comparative cytogenetics of Lemniscomys (L. zebra, L. rosalia, L. striatus) and Arvicanthis dembeesis. J Zool Syst Evol Res 40:223–231. https://doi.org/10.1046/j.1439-0469.2002.00185.x
Chappellier A (1927a) Essais de mensuration sur des Muridés (Mammalia, Rodentia). Bull Mus Nat Hist Natur 5:343–349
Chappellier A (1927b) Essais de mensuration sur des Muridés (Mammalia, Rodentia) - Suite. Bull Mus Nat Hist Natur 6:480–485
Çiçek K, Ayaz D, Bayrakci Y (2011) Morphology of the northern banded newt, Ommatotriton ophryticus (Berthold, 1846) (Caudata: Salamandridae) in Uludağ (Bursa, Turkey). Herpetol Notes 4:161–165
Crawford-Cabral J (1998) The Angolan rodents of the superfamily Muroidea: an account of their distribution. Instituto de Investigação Científica Tropical. Estud Ensaios Doc 161:1–223
Cvijanović M, Üzüm N, Ivanović A, Avci A, Özcan ÇG, Olgun K (2017) Variation in skull size and shape in a newt species with male-biased sexual dimorphism. Herpetol J 27:41–46
Dai J, Min J, Xiao Y, Lei X, Shen W, Wei H (2005) The absence of mitochondrial DNA diversity among common laboratory inbred mouse strains. J Exp Biol 208:4445–4450. https://doi.org/10.1242/jeb.01920
Dieterlen F (1991) Lemniscomys hoogstraali, a new murid species from Sudan. Bonn Zool Beitr 42:11–15
Ducroz J, Volobouev V, Granjon L (2001) An assessment of the systematics of Arvicanthine rodents using mitochondrial DNA sequences: evolutionary and biogeographical implications. J Mamm Evol 8:173–206. https://doi.org/10.1023/A:1012277012303
Eisentraut M (1968) Das Gaumenfaltenmuster bei westafrikanischen Muriden. Zool Jb Syst 96:478–490
Fadda C, Corti M, Verheyen E (2001) Molecular phylogeny of Myomys / Stenocephalemys complex and its relationships with related African genera. Biochem Syst Ecol 29:585–596. https://doi.org/10.1016/S0305-1978(00)00087-9
Hall T (2011) BioEdit: an important software for molecular biology. GERF Bull Biosci 2(1):60–61
Hammer Ø, Harper DAT, Ryan PD (2001) PAST version 2.17: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9
Happold DCD (2013) Mammals of Africa. Volume III: rodents, hares and rabbits. Bloomsbury Publishing, London
Heuglin THV (1864) Beiträge zur Zoologie Central-Afrika’s. Leopoldina 31, Abhandlungen 7:1–15
Hotelling H (1936) Relations between two sets of variates. Biometrika 28:321–377
Illiger JKW (1811) Prodromus systematis mammalium et avium additis terminis zoographicis utriusque classis, eorumque versione germanica. Berlin. https://doi.org/10.5962/bhl.title.106965
Kennerley R, Van der Straeten E (2016) Lemniscomys roseveari. (errata version published in 2017) The IUCN Red List of Threatened Species 2016. https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T11494A22439460.en. Accessed 21 July 2017
Kumar S, Stecher G, Tamura K (2016) MEGA: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Linnaeus C (1758) Systema Naturae per regna tria naturae, secundum classis, ordines, genera, species cum characteribus, differentiis, synonymis, locis. Tenth edition. Volume I. Laurentii Salvii, Stockholm
Linnaeus C (1766) Systema naturae per regna tria naturae, secundum classis, ordines, genera, species cum characteribus, differentiis, synonymis, locis. Twelfth edition. Volume I. Regnum animale, part I. Laurentii Salvii, Stockholm
Monadjem A, Perrin MR (1997) Population dynamics of Lemniscomys rosalia Muridae: Rodentia in a Swaziland grassland: effects of food and fire. S Afr J Zool 32:129–135. https://doi.org/10.1080/02541858.1997.11448444
Monadjem A, Taylor PJ, Denys C, Cotteril F (2015) Rodent of sub-Saharan Africa. A biogeographic and taxonomic synthesis. Walter de Gruyter, Berlin
Nowak RM (1999) Walker's mammals of the world. Two volumes 6th edition. Johns Hopkins University Press, Baltimore
Palumbi S, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fools guide to PCR, version II. University of Hawaii, Honolulu
Petter F (1961) Répartition géographique et écologique des rongeurs désertiques de la région paléarctique. PhD Thesis. University of Paris, France
Scherrer B (1984) Biostatistiques. Morin G (ed) University of Québec, Montréal
Schlick N, Jensen-Seaman M, Orlebeke K, Kwitek A, Jacob H, Lazar J (2006) Sequence analysis of the complete mitochondrial DNA in 10 commonly used inbred rat strains. Am J Physiol-Cell Physiol 291:C1183–C1192. https://doi.org/10.1152/ajpcell.00234.2006
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal omega. Mol Syst Biol 7:539. https://doi.org/10.1038/msb.2011.75
Sokal R, Michener C (1958) A statistical method for evaluating systematic relationships. Univ Kansas Sci Bull 38:1409–1438
Thomas O (1904) On mammals from northern Angola collected by Dr. WJ Ansorge. Ann Mag Nat Hist Ser 7(13):405–421
Thomas O (1910) Notes on African rodents. Ann Mag Nat Hist Ser 8(6):221–226
Thomas O, Wroughton RC (1910) Zoological results of the Ruwenzori expedition. Mammalia. Trans Zool Soc London 19:481–518
Trouessart EL (1881) Catalogue des mamifères vivants et fossiles: Rodentia. Bull Soc d'Études Sci d'Angers 10(2):124
Van der Straeten E (1975) Lemniscomys bellieri, a new species of Muridae from the Ivory Coast (Mammalia, Muridae). Rev Zool Afr 89:906–908
Van der Straeten E (1980) A new species of Lemniscomys (Muridae) from Zambia: Lemniscomys roseveari. Ann Cape Prov Mus Nat Hist 13:55–62
Van der Straeten E (2016) Lemniscomys hoogstraali. (errata version published in 2017) The IUCN Red List of Threatened Species 2016. https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T11490A22438904.en. Accessed 21 July 2017
Van der Straeten E, Verheyen WN (1979) Note sur la position systematique de Lemniscomys macculus (Thomas et Wroughton, 1910) (Mammalia, Muridae). Mammalia 43:377–389
Van der Straeten E, Verheyen WN (1980) Relations biometriques dans le groupe specifique Lemniscomys striatus (Mammalia, Muridae). Mammalia 44:73–82
Wilson DE, Reeder DM (2005) Mammal species of the world. A taxonomic and geographic reference, 3rd edn. Johns Hopkins University Press, Baltimore
Acknowledgments
The present study has been carried out in the Research Unit Biodiversity and Population Biology at the Faculty of Sciences of Tunis (FST). It would not have been possible without the collaboration of many people we want to thank. We express our gratitude to Mr. George Lenglet curator at “Institut Royal des Sciences Naturelles de Belgique” (IRSNB) and Mr. Wim Wendelen curator at “Musée Royal d’Afrique Centrale” (MRAC) and also to Mr. Maher Gtari professor at the “Faculty of Sciences of Tunis”.
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Ben Salem, I., Ben Ibrahim, A., Chetoui, M. et al. Contribution to the study of the genus Lemniscomys (Rodentia: Muridae). Morphometric and molecular approaches. Biologia 73, 339–349 (2018). https://doi.org/10.2478/s11756-018-0044-3
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DOI: https://doi.org/10.2478/s11756-018-0044-3