The impact of the Congo River and its tributaries on the rodent genus Praomys: Speciation origin or range expansion limit?

Zoological Journal of the Linnean Society

Volumn 163, Issue 3, 2011, Pages 983-1002

  Kennis, Jan ^a   Nicolas, Violaine ^b   Hulselmans, Jan ^a   Katuala, Pionus G B ^c   Wendelen, Wim ^d   Verheyen, Erik ^a,e   Dudu, Akaibe M ^c   Leirs, Herwig ^a,f  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c UNIVERSITY OF KISANGANI   (Congo)

^d ROYAL MUSEUM FOR CENTRAL AFRICA   (Belgium)

^e ROYAL BELGIAN INSTITUTE OF NATURAL SCIENCES   (Belgium)

^f Danish Pest Infestation Laboratory   (Denmark)

Author keywords

Craniometric analysis; Cytochrome b; Phylogeny; Praomys; River barrier; Speciation

Indexed keywords

EID: 84861463584     PISSN: 00244082     EISSN: 10963642     Source Type: Journal    
DOI: 10.1111/j.1096-3642.2011.00733.x     Document Type: Article

References (79)

1. Amundala D, Bapeamoni A, Iyongo W, Kennis J, Gambalemoke M, Kadange N, Katuala PGB, Dudu A. 2005. The population structure of four rodent species from a tropical region (Kisangani, D.R. Congo). Belgian Journal of Zoology 135 (supplement): 127-131.
2. Amundala DN, Kennis J, Leirs H, Dudu AM. 2008. Farmer survey in the hinterland of Kisangani (Democratic Republic of Congo) on rodent crop damage and rodent control techniques used. Mammalia 72: 192-197.
3. Anthony NM, Johnson-Bawe M, Jeffery K, Clifford SL, Abernethy KA, Tutin CE, Lahm SA, White L, Utley JF, Wickings EJ, Bruford MW. 2007. The role of Pleistocene refugia and rivers in shaping gorilla genetic diversity in central Africa. Proceedings of the National Academy of Sciences 104: 20432-20436.
4. Barome P-O, Volobouev V, Monnerot M, Kazgeba Mfune J, Chitaukali W, Gautun J-C, Denys C. 2001. Phylogeny of Acomys spinosissimus (Rodentia, Muridae) from north Malawi and Tanzania: evidence from morphological and molecular analysis. Biological Journal of the Linnean Society 73: 321-340.
5. Barrière P, Hutterer R, Nicolas V, Quérouil S, Colyn M. 2005. Investigating the role of natural gallery forests outside the Congolese rainforest as a refuge for African forest shrews. Belgian Journal of Zoology 135 (supplement): 21-29.
6. Benton MJ, Donoghue PCJ. 2007. Paleontological Evidence to Date the Tree of Life. Molecular Biology and Evolution 24: 26-53.
7. Brown JH. 1984. On the Relationship between Abundance and Distribution of Species. The American Naturalist 124: 255.
8. Colyn M. 1987. Les primates des forêts ombrophiles de la cuvette du Zaïre: interprétations zoogéographiques des modèles de distribution. Revue De Zoologie Africaine 101: 183-196.
9. Colyn M, Deleporte P. 2002. Biogeographic analysis of central African forest guenons. In: Glenn M, Cords M, eds. Multicolored monkeys: diversity and adaptation in the guenons of Africa. New York: Kluwer Academic/Plenum Publishers, 61-78.
10. Colyn M, Gautier Hion A, Verheyen W. 1991. A re-appraisal of palaeoenvironmental history in central Africa: evidence for a major fluvial refuge in the Zaïre Basin. Journal of Biogeography 18: 403-407.
11. Crauwels D. 2009. Pestsoorten in de tropische landbouw: voeding van een typisch pest-genus (Mus) vergelijken met andere genera. Unpublished Master thesis, Universiteit Antwerpen.
12. DeMenocal PB. 2004. African climate change and faunal evolution during the Pliocene-Pleistocene. Earth and Planetary Science Letters 220: 3-24.
13. Denys C, Lecompte E, Granjon L, Baylac M, Cordeiro P, Cornette R, Dobigny G, Fichet-Calvet E, Hugot J-P, Meslage C, Millien-Parra V, Petrillo P, Volobouev V, Welz M. 2003. Integrative systematics: the importance of combining techniques for increasing knowledge of African Murinae. In: Singleton GR, Hinds LA, Krebs C, Spratt DM, eds. Rats, mice and people: rodent biology and management. Canberra: ACIAR Monograph Series, 499-506.
14. DeWinton W. 1897. On a collection of small mammals from Uganda. Annals and Magazine of Natural History 6: 318.
15. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.
16. Dudu A. 1991. Etude du peuplement d'insectivores et de rongeurs de la forêt ombrophile de basse altitude de Zaïre (Kisangani, Masako). Unpublished Doctoraatsthesis, Universiteit Antwerpen.
17. Dudu A, Verhagen R, Gevaerts H, Verheyen W. 1997. Population structure and reproductive cycle of Praomys jacksoni (& e, 1897) and first data on the reproduction of P. misonnei Van der Straeten & Dieterlen, 1987 and P. mutoni Van der Straeten & Dudu 1990 (Muridae) from Masako Forest (Kisangani, Zaire). Belgian Journal of Zoology 127: 67-70.
18. Eriksson J, Hohmann G, Boesch C, Vigilant L. 2004. Rivers influence the population genetic structure of bonobos (Pan paniscus). Molecular Ecology 13: 3425-3435.
19. Gaubert P, Veron G, Tranier M. 2002. Genets and 'genetlike' taxa (Carnivora, Viverrinae): phylogenetic analysis, systematics and biogeographic implications. Zoological Journal of the Linnean Society 134: 317-334.
20. Gradstein FM, Ogg JG. 2004. Geological Time Scale 2004 - why, how, and where next! Lethaia 37: 175-181.
21. Gradstein FM, Ogg JG. 2009. International Stratigraphy Chart: International Commission on Stratigraphy. Available at http://www.stratigraphy.org.
22. Groves CP. 2007. The taxonomic diversity of the Colobinae of Africa. Journal of Anthropological Studies 85: 7-34.
23. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696-704.
24. Guindon S, Lethiec F, Duroux P, Gascuel O. 2005. PHYML Online - a web server for fast maximum likelihoodbased phylogenetic inference. Nucleic Acids Research 33: W557-W559.
25. Haffer J. 1997. Alternative models of vertebrate speciation in Amazonia: an overview. Biodiversity and Conservation 6: 451-476.
26. Halanych KM, Robinson TJ. 1999. Multiple Substitutions Affect the Phylogenetic Utility of Cytochrome b and 12S rDNA Data: examining a Rapid Radiation in Leporid (Lagomorpha) Evolution. Journal of Molecular Evolution 48: 369- 379.
27. Hatt RT. 1934. Fourteen hitherto unrecognized African rodents. American Museum Novitates 708: 1-15.
28. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
29. Jansa SA, Barker FK, Heaney LR. 2006. The Pattern and timing of diversification of philippine endemic rodents: evidence from mitochondrial and nuclear gene sequences. Systematic Biology 55: 73-88.
30. Katuala PGB, Hart JA, Hutterer R, Leirs H, Dudu A. 2005. Biodiversity and ecology of small mammals (Rodents and Shrews) of the 'Réserve de Faune à Okapis', Democratic Republic of the Congo. Belgian Journal of Zoology 135 (supplement): 191-196.
31. Katuala PGB, Kennis J, Nicolas V, Wendelen W, Hulselmans J, Verheyen E, Van Houtte N, Dierckx T, Dudu AM, Leirs H. 2008. The presence of Praomys, Lophuromys, and Deomys species (Muridae, Mammalia) in the forest blocks separated by the Congo River and its tributaries (Kisangani region, Democratic Republic of Congo). Mammalia 72: 223-228.
32. Kouassi K, Nicolas V, Aniskine V, Lalis A, Cruaud C, Couloux A, Colyn M, Dosso M, Koivogui L, Verheyen E, Akoua-Koffi C, Denys C. 2008. Taxonomy and biogeography of the African Pygmy mice, Subgenus Nannomys (Rodentia, Murinae, Mus) in Ivory Coast and Guinea (West Africa). Mammalia 72: 237-252.
33. Lecompte E, Aplin K, Denys C, Catzeflis FM, Chades M, 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: 199-220.
34. Lecompte E, Denys C, Granjon L. 2001. An identification key for species within the genus Praomys (Rodentia, Muridae). In: Denys C, Granjon L, Poulet A, eds. African small mammals. Paris: IRD Editions, 127-139.
35. Lecompte E, Granjon L, Denys C. 2002a. The phylogeny of the Praomys complex (Rodentia: Muridae) and its phylogeographic implications. Journal of Zoological Systematics and Evolutionary Research 40: 8-25.
36. Lecompte E, Granjon L, Kerbis-Peterhans J, Denys C. 2002b. Cytochrome b-based phylogeny of the Praomys group (Rodentia, Murinae): a new African radiation? Comptes Rendus De Biologies 325: 1-14.
37. Lecompte E, Denys C, Granjon L. 2005. Confrontation of morphological and molecular data: the Praomys group (Rodentia, Murinae) as a case of adaptive convergences and morphological stasis. Molecular Phylogenetics and Evolution 37: 899-919.
38. Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
39. Louette M. 1992. Barriers, contact zones and subspeciation in central equatorial Africa. Bulletin B.O.C. Centenary Suppl 112A: 209-216.
40. Michaux JR, Libois R, Filippucci M-G. 2005. So close and so different: comparative phylogeography of two small mammal species, the Yellow-necked fieldmous (Apodemus flavicollis) and the Woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Heredity 94: 52-63.
41. Miller GS. 1900. A collection of small mammals from Mount Coffee Liberia. Proceedings of the Washington Academy of Sciences 2: 631-649.
42. Moritz C, Patton JL, Schneider CJ, Smith TB. 2000. Diversification of rainforest faunas: an integrated molecular approach. Annual Review of Ecology, Evolution and Systematics 31: 533-563.
43. Mukinzi I, Katuala PGB, Kennis J, Gambalemoke M, Kadange N, Dudu A, Colyn M, Hutterer R. 2005. Preliminary data on the biodiversity of rodents and insectivores (Mammalia) in the periphery of Kisangani (D.R. Congo). Belgian Journal of Zoology 135 (supplement): 133-140.
44. Musser GG, Carleton MD. 2005. Superfamily muroidea. In: Wilson DE, Reeder DM, eds. Mammal species of the world: a taxonomic and geographic reference. Baltimore, MD: The Johns Hopkins University Press, 894-1531.
45. Nicolas V. 2003. Systematique et écologie des communautés afrotropicales de muridés (Mammalia: Rodentia) et de soricidés (Mammalia: Insectivora). Unpublished Docteur de l'Université de Rennes 1, Université de Rennes 1.
46. Nicolas V, Colyn M. 2006. Swimming Ability of 5 Species of African Rainforest Murid Rodents in Relation to Their Habitat Preferences. Zoological Studies 45: 264-268.
47. Nicolas V, Verheyen E, Verheyen W, Hulselmans J, Dillen M, Akpatou B, Dudu A, Wendelen W, Colyn M. 2005. Systematics of African lowland rainforest Praomys (Rodentia, Muridae). Zoological Journal of the Linnean Society 145: 539-553.
48. Nicolas V, Quérouil S, Verheyen E, Verheyen W, Mboumba JF, Dillen M, Colyn M. 2006. Mitochondrial phylogeny of African wood mice, genus Hylomyscus (Rodentia, Muridae): implications for their taxonomy and biogeography. Molecular Phylogenetics and Evolution 38: 779-793.
49. Nicolas V, Bryja J, Akpatou B, Konecny A, Lecompte E, Colyn M, Lalis A, Couloux A, Denys C, Granjon L. 2008a. Comparative phylogeography of two sibling species of forest-dwelling rodent (Praomys rostratus and P. tullbergi) in West Africa: different reactions to past forest fragmentation. Molecular Ecology 17: 5118-5134.
50. Nicolas V, Mboumba JF, Verheyen E, Denys C, Lecompte E, Olayemi A, Missoup AD, Katuala G-B CM. 2008b. Phylogeographic structure and regional history of Lemniscomys striatus (Rodentia: Muridae) in tropical Africa. Journal of Biogeography 35: 2074-2089.
51. Nicolas V, Akpatou B,Wendelen W, Kerbis Peterhans JC, Olayemi A, Decher J, Missoup AD, Denys C, Barrière P, Cruaud C, Colyn M. 2010. Molecular and morphometric variation in two sibling species of the genus Praomys (Rodentia: Muridae): implications for biogeography. Zoological Journal of the Linnean Society 160: 397-419.
52. Plana V. 2004. Mechanisms and tempo of evolution in the African Guineo-Congolian rainforest. Proceedings of the National Academy of Sciences 359: 1585-1594.
53. Posada D, Crandall KA. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818.
54. Quérouil S. 2001. Interets et limites de l'approche moleculaire pour aborder la biogéographie et la speciation: quelques examples chez les mammifères d'Afrique tropicale. Unpublished PhD, Université de Rennes 1.
55. Quérouil S, Verheyen E, Dillen M, Colyn M. 2003. Patterns of diversification in two African forest shrews: Sylvisorex johnstoni and Sylvisorex ollula (Soricidae, Insectivora) in relation to paleo-environmental changes. Molecular Phylogenetics and Evolution 28: 24-37.
56. Rambaut A, Drummond AJ. 2007. Tracer v1.4. Available at http://beast.bio.ed.ac.uk/Tracer.
57. Robbrecht E. 1996. Geography of African Rubiaceae with reference to glacial rain forest refuges. In: van der Maesen LJG, van der Burgt XM, van Medenbach de Rooy JM, eds. The biodiversity of African plants. Dordrecht: Kluwer, 564- 581.
58. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
59. Rozas J, Rozas R. 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15: 174-175.
60. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497.
61. Sabatier M. 1982. Les rongeurs du site Pliocène à Hominidés de Hadar (Ethiopie). Palaeovertebrata 12: 1-56.
62. Smith MF, Patton JL. 1999. Phylogenetic relationships and the radiation of sigmodontine rodents in South America: evidence from Cytochrome b. Journal of Mammalian Evolution 6: 89-128.
63. Smith TB, Wayne RK, Girman DJ, Bruford MW. 1997. A role for ecotones in generating rainforest biodiversity. Science 276: 1855-1856.
64. Statsoft I. 2003. Statistica 6.1. Data analysis, data mining, and quality control. Tulsa: Statsoft.
65. Sullivan J, Joyce P. 2005. Model selection in Phylogenetics. Annual Review of Ecology, Evolution and Systematics 36: 445-466.
66. Swofford D. 2002. PAUP: phylogenetic analysis using parsimony, Version 4b10. Washington, DC: Smithsonian Institution.
67. Thomas O. 1894. Note on Mus burtoni, Thos. The Annals and Magazine of Natural History 8: 204.
68. Thomas O. 1915. List of mammals collected on the upper Congo by Christy for the Congo Museum. Tervuren. The Annals and Magazine of Natural History 8: 465-481.
69. Trouessart EL. 1881. Catalogue des mammifères vivants et fossiles. Bulletin De La Société D'études Scientifiques d'Angers 10: 121.
70. Van der Straeten E. 2008. Notes on the Praomys of Angola with the description of a new species (Mammalia:Rodentia: Muridae). Stuttgarter Beiträge Zur Naturkunde A., Neue Serie 1: 123-131.
71. Van der Straeten E, Dieterlen F. 1987. Praomys misonnei, a new species of Muridae from Eastern Zaïre (Mammalia). Stuttgarter Beiträge Zur Naturkunde 402: 1-11.
72. Van der Straeten E, Dudu AM. 1990. Systematics and distribution of Praomys from the Masako Forest Reserve (Zaire) with the description of a new species. In: Peters G, Hutterer R, eds. Vertebrates in the tropics. Bonn: Alexander Koenig Zoological Research Institute and Zoological Museum, 73-84.
73. Van der Straeten E, Kerbis Peterhans JC. 1999. Praomys degraaffi, a new species of Muridae (Mammalia) from central Africa. South African Journal of Zoology 34: 80-90.
74. Verheyen W, Van der Straeten E. 1977. Description of Malacomys verschureni, a new Murid-species from Central Africa (Mammalia - Muridae). Revue De Zoologie Africaine 91: 737-744.
75. Verheyen W, Colyn M, Hulselmans J. 1996. Re-evaluation of the Lophuromys nudicautus Heller 1911 species complex, with a description of a new species from Zaire (Muridae, Rodentia). Bulletin Van Het Koninklijk Belgisch Instituut Voor Natuurwetenschappen, Biologie 66: 241-273.
76. Verheyen W, Dierckx T, Hulselmans J. 2000. The brushfurred rats of Angola and southern Congo: description of a new taxon of the Lophuromys sikapusi species complex. Bulletin Van Het Koninklijk Belgisch Instituut Voor Natuurwetenschappen, Biologie 70: 253-267.
77. Verheyen W, Hulselmans J, Dierckx T, Verheyen E. 2002. The Lophuromys flavopunctatus Thomas, 1888 s.l. complex: a craniometric study, with the description and genetic characterization of two new species (Rodentia, Muridae, Africa). Bulletin Van Het Koninklijk Belgisch Instituut Voor Natuurwetenschappen, Biologie 72: 103-144.
78. Wieringa JJ. 1999. Monopetalanthus exit. A systematic study of Aphanocalyx, Bikinia, Icuria, Michelsonia and Tetraberlinia (Leguminosae, Caesalpinioideae). Wageningen Agricultural University Paper 99 (4).
79. Winnepenninckx B, Backeljau T, De Wachter R. 1993. Extraction of high molecular weight DNA from molluscs. Trends in Genetics 9: 407.