Cryptic speciation in the southern African vlei rat Otomys irroratus complex: Evidence derived from mitochondrial cyt b and niche modelling

Biological Journal of the Linnean Society

Volumn 104, Issue 1, 2011, Pages 192-206

  Engelbrecht, Adriaan ^a   Taylor, Peter John ^b   Daniels, Savel Regan ^a   Rambau, Ramugondo Victor ^a  

^a STELLENBOSCH UNIVERSITY   (South Africa)

^b UNIVERSITY OF VENDA   (South Africa)

Author keywords

Contact zone; MtDNA; Nested clade analysis; Phylogeography

Indexed keywords

BAYESIAN ANALYSIS; BIOCLIMATOLOGY; CLADISTICS; CONTACT ZONE; CRYPSIS; CYTOCHROME; DATA SET; DIVERGENCE; ECOLOGICAL MODELING; GEOGRAPHICAL DISTRIBUTION; MITOCHONDRIAL DNA; NICHE; PARSIMONY ANALYSIS; PHYLOGEOGRAPHY; PLEISTOCENE; PRECIPITATION (CLIMATOLOGY); RODENT; SEASONALITY; SPECIATION (BIOLOGY); TAXONOMY; ZOOGEOGRAPHY;

SOUTHERN AFRICA;

OTOMYS IRRORATUS; RATTUS; RODENTIA;

EID: 84860393837     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2011.01696.x     Document Type: Article

References (91)

1. Akaike H. 1973. Information theory as an extension of maximum likelihood principle. In: Petrov BN, Csake F, eds. Second International Symposium on Information Theory. Budapest: Akademiai Kaido, 267-281.
2. Avery DM. 1991. Late Quaternary incidence of some micro mammalian species in Natal. Durban Museum Novitates 16: 1-11.
3. Avise JC. 1998. The history and purview of phylogeography: a personal reflection. Molecular Ecology 7: 371-379.
4. Avise JC. 2000. Phylogeography: the history and formation of species. Cambridge, MA: Harvard University Press.
5. Baker RJ, Bradley RD. 2006. Speciation in mammals and the genetic species concept. Journal of Mammalogy 87: 643-662.
6. Bond JE, Sierwald P. 2002. Eurhinocricus rosenbergi, a new species of rhinocricid from the Caribbean island of Jamaica (Spirobolida: Rhinocricidae). Proceedings of the Biological Society of Washington 155: 670-675.
7. Bond J, Stockman A. 2008. An integrative method for delimiting cohesion species: finding the population-species interface in a group of Californian trapdoor spiders with extreme genetic divergence and geographic structuring. Systematic Biology 57: 628-646.
8. Bradley RD, Baker RJ. 2001. A test of genetic species concept: cytochrome b sequences and mammals. Journal of Mammalogy 82: 960-973.
9. Britton-Davidian J, Catalan J, Granjon L, Duplantier J-M. 1995. Chromosomal phylogeny and evolution in the genus Mastomys (Mammalia, Rodentia). Journal of Mammalogy 76: 248-262.
10. Clement MD, Posada D, Crandall KA. 2001. TCS. A computer program to estimate gene genealogies. Molecular Ecology 9: 1657-1660.
11. Contrafatto G, Meester JA, Bronner G, Taylor PJ, Willan K. 1992b. Genetic variation in the African rodent subfamily Otomyinae (Muridae). IV. Chromosome G banding analysis of Otomys irroratus and O.angoniensis. Israel Journal of Zoology 38: 277-291.
12. Contrafatto G, Meester JA, Willan K, Taylor PJ, Roberts MA, Baker CM. 1992c. Genetic variation in the African rodent subfamily Otomyinae (Muridae). II. Chromosomal changes in some populations of Otomys irroratus. Cytogenetics and Cell Genetics 59: 293-299.
13. Contrafatto G, Van Der Berg JR, Grace JH. 1997. Genetic variation in the African rodent subfamily Otomyinae (Muridae): immuno-electron transfer of liver proteins of some of Otomys irroratus (Brants, 1827) populations. Tropical Zoology 10: 157-171.
14. Cracraft J. 1989. Speciation and its ontology: the empirical consequences of alternative species concepts for understanding the pattern and process of differentiation. In: Ottc D, Endler JA, eds. Speciation and its consequences. Sunderland, MA: Sinauer, 28-59.
15. Cracraft J. 1992. The species of the birds-of-paradise (Paradisaeidae): applying the phylogenetic species concept to a complex pattern of diversification. Cladistics 8: 1-43.
16. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK. 2000. Considering evolutionary process in conservation biology. Tree 15: 290-295.
17. Crochet PA. 2000. Genetic structure of avian populations allozymes revisited. Molecular Ecology 9: 1463-1469.
18. Daniels SR, Hofmeyer MD, Henen BT, Crandall AK. 2007. Living with the genetic signature of Miocene induced change: evidence from the phylogeographic structure of the endemic angulate tortoise Chersina angulata. Molecular Phylogenetics and Evolution 45: 915-926.
19. Daniels SR, Heideman NJ, Hendricks MGJ. 2009. Examination of evolutionary relationships in a cape fossorial skink species complex (Acontiinae: Acontias meleagris meleagris) reveals the presence of five cryptic lineages. Zoologica Scripta 38: 449-463.
20. Denys C. 2003. Evolution du genre Otomys (Rodentia: Muridae) au Plio-Pléistocène d'Afrique orientale et australe. In: Radulescu C, Petculecus PMS, eds. Advances in paleontology 'Henth to Pantha'. Memorial Volume, 75-84.
21. Denys C, Jeager J-J. 1986. A biostratigraphic problem: the case of the East-African Plio-Pleistocene rodent faunas. Modern Geology 10: 215-233.
22. Drummond AJ, Rambaut A. 2006. BEAST v. 1.4. Bayesian evolutionary analysis sampling trees. Available at
23. Eeley HAC, Lawes MJ, Piper SE. 1999. The influence of climate change on the distribution of indigenous forest in KwaZulu-Natal, South Africa. Journal of Biogeography 26: 595-617.
24. Elith J, Graham CH, Anderson RP, Dudi'k M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G, Moritz C, Nakamura M, Nakazawa Y, Mc Overton JC, Peterson AT, Phillips SJ, Richardson KS, Scachetti-Pereira R, Schapire RE, Soberón J, Williams S, Wisz MS, Zimmermann N. 2006. Novel methods improve prediction of species' distributions from occurrence data. Ecography 29: 129-151.
25. Ellery WN, Scholes RJ, Mentis MT. 1991. An initial approach to predicting the sensitivity of the grassland biome to climate change. South African Journal of Science 87: 499-503.
26. Excoffier L, Smouse PE, Quattro JM. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetica 131: 479-491.
27. Excoffier L, Laval G, Schneider S. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evoutionary Bioinformaics Online 1: 47-50.
28. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
29. Frankham R, Ballou JD, Briscoe DA. 2003. Introduction to conservation genetics. Cambridge: Cambridge University Press.
30. Fu Y-X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915-925.
31. Goodman SM, Raxworthy CJ, Maminirnua CP, Olson LE. 2006. A new species of shrew tenrec (Microgale jobihely) from northern Madagascar. Journal of Zoology 270: 384-398.
32. Harpending HC. 1994. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology 66: 591-601.
33. Hasegawa M, Kishino H, Yano T. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160-174.
34. Hernandez PA, Graham CH, Master LL, Albert DL. 2006. The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecography 29: 773-785.
35. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965-1978.
36. Hopley PJ, Latham AJ, Marshall JD. 2006. Palaeoenvironments and palaeodiets of mid Pliocene micromammals from Makapansgat Limeworks, South Africa: a stable isotope and dental microwear approach. Palaeogeography, Palaeoclimatology, Palaeoecology 233: 235-251.
37. Huelsenbeck JP, Ronquist F. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinfomatics 17: 754-755.
38. Irwin DM, Kocher TD, Wilson AC. 1991. Evolution of cytochrome b gene of mammals. Journal of Molecular Evolution 32: 128-144.
39. 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.
40. Kocher TD, Thomas WK, Meyer A, Edwards SV, Paabo S, Villablancatt FX, Wilson AC. 1989. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proceedings of the National Academy of Science USA 86: 6196-6200.
41. Lawes MJ, Eeley HAC, Findlay NJ, Forbes D. 2007. Resilient forest faunal communities in South Africa: a legacy of palaeoclimatic change and extinction filtering? Journal of Biogeography 34: 1246-1264.
42. Lynch CD, Watson J. 1992. The distribution and ecology of Otomys sloggetti (Mammalia: Rodentia) with notes on its taxonomy. Navorsinge van die Nasionale Museum Bloemfontein 8: 141-158.
43. Matthews T, Denys C, Parkington JE. 2005. The palaeoecology of the micromammals from the late middle Pleistocene site of Hoedjiespunt 1 (Cape Province, South Africa). Journal of Human Evolution 49: 432-451.
44. Mayden RL. 1997. A hierarchy of species concepts: the denouement in the saga of the species problem. In: Claridge ME, Dawah HA, Wilson MR, eds. Species: the units of biodiversity. New York: Chapman and Hall, 381-424.
45. Mayr E. 1963. Animal species and evolution. Cambridge, MA: Harvard University Press.
46. Meester JAJ, Taylor PJ, Contrafatto G, Campbell GK, Willan K, Lamb JM, Pillay N. 1992. Chromosomal speciation in Southern African Otomyinae (Rodentia: Muridae): a review. Durban Museum Novitates 17: 58-63.
47. de Menocal P. 2004. African climate change and faunal evolution during the Pliocence-Pleistocene. Earth and Planetary Science Letters 220: 3-24.
48. Michaux JR, Libois R, Paradis E, Filippucci MG. 2004. Phylogeographic history of the yellow-necked fieldmouse (Apodemus flavicollis) in Europe and in the near and middle east. Molecular Phylogenetics and Evolution 32: 788-798.
49. Mitsainas GP, Tryfonopoulos GA, Thanoub EG, Bisac R, Fraguedakis-Tsolisb SE, Chondropoulos BP. 2009. New data on the distribution of Mus spicilegus Petenyi, 1882 (Rodentia, Muridae) and a distinct mtDNA lineage in the southern Balkans. Mammalian Biology 74: 351-360.
50. Monaghan MT, Wild R, Elliot M, Fujisawa T, Balke M, Inward DJG, Lees DC, Ranaivosolo R, Eggleton P, Barraclough TG, Vogler AP. 2009. Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology 58: 298-311.
51. Moreau RE. 1962. Vicissitudes of the African biomes in the late Pleistocene. Proceedings of the Zoological Society London 141: 395-421.
52. Mucina L, Rutherford MC. 2006. The vegetation of South Africa, Lesotho and Swaziland. Strelitzia 19. Pretoria: South African National Biodiversity Institute.
53. Mullin SK, Pillay N, Taylor PJ. 2004. Cranial variation and geographic patterns within the Dasymys rufulus complex (Rodentia: Muridae). Journal of Mammalogy 85: 911-923.
54. Nylander JAA, Ronquist F, Heulsenbeck JP, Nieves-Alderey JL. 2004. Bayesian phylogenetic analysis of combined data. Systematic Biology 53: 47-67.
55. Pääbo S, Wilson AC. 1988. Polymerase chain reaction reveals cloning artifacts. Nature 334: 387-388.
56. Palumbi SR, Martin AP, Romano S, McMillan WO, Stice L, Grabowski G. 1991. The simple fool's guide to PCR. Honolulu, HI: Department of Zoology Special Publication, University of Hawaii.
57. Petit E, Balloux F, Excoffier L. 2000. Mammalian population genetics: why not Y? Trends in Ecology and Evolution 17: 28-33.
58. Phillips SJ, Anderson RP, Schapire RE. 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190: 231-259.
59. Piel WH, Nutt KJ. 2000. One species or several? Discordant patterns of geographic variation between allozymes and mtDNA sequences among spiders in the genus Metepeira (Araneae: Araneidae). Molecular Phylogenetics and Evolution 15: 414-418.
60. Pillay N, Willan K, Meester J. 1992. Post-zygotic reproductive isolation in the African vlei rat Otomys irroratus (Muridae: Otomyinae). Israel Journal of Zoology 38: 307-313.
61. Pillay N, Willan K, Cooke J. 1995. Evidence of pre-mating reproductive isolation in two populations of the vlei rat Otomys irroratus: experiments of inta- and interpopulation male-female encounters. International Journal of Mammalian Biology 60: 352-360.
62. Pocock TN. 1976. Pliocene mammalian microfauna from Langebaanweg: a new fossil genus linking the Otomyinae with the Murinae. South African Journal of Science 72: 58-60.
63. Posada D, Crandall KA. 1998. Modeltest: testing the model of DNA substitution. Bioinfomatics 14: 817-818.
64. Posada D, Crandall KA, Templeton AL. 2000. GeoDIS. A program for nested cladistic analysis of the geographic distance of genetic haplotypes. Molecular Ecology 9: 487-488.
65. Rambau RV, Elder FFB, Robinson TJ. 2001. Chromosomal evolution in the vlei rat, Otomys irroratus (Muridae: Otomyinae): a compound chromosomal rearrangement separates two major cytogenetic groups. Cytogenetic and Cell Genetics 93: 253-257.
66. Rambau RV, Robinson TJ, Stanyon R. 2003. Molecular genetics of Rhabdomys pumilio subspecies boundaries: mtDNA phylogeography and karyotypic analysis by fluorescence in situ hybridization. Molecular Phylogenetics and Evolution 28: 564-575.
67. Roberts A. 1929. New forms of African mammals. Annals of the Transvaal Museum 13: 82-121.
68. Rogers AR, Harpending H. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9: 552-569.
69. Sénégas F. 2001. Interpretation of the dental pattern of the South African fossil Euryotomys (Rodentia, Murinae) and origin of otomyine dental morphology. In: Denys C, Granjon L, Poulet A, eds. African small mammals. Paris: IRD, 151-160.
70. Sénégas F, Avery M. 1998. New evidence for the murine origins of the Otomyinae (Mammalia, Rodentia) and the age of Bolt's Farm (South Africa). South African Journal of Science 94: 503-507.
71. Sites JW Jr, Marshall JC. 2003. Delimiting species: a Renaissance issue in systematic biology. Trends in Ecology and Evolution 18: 462-470.
72. Skinner JD, Chimimba CT. 2005. The mammals the Southern African Subregion, 3rd edn. Cambridge: Cambridge University Press, 174-175.
73. Smit HA, Robinson TJ, Jansen van Vuuren B. 2007. Coalescence methods reveal the impact of vicariance on the spatial genetic structure of Elephantulus edwardii (Afrotheria, Macroscelidea). Molecular Ecology 16: 2680-2692.
74. Stuart BL, Dugan KA, Allard MW, Kearney M. 2006. Extraction of nuclear DNA from bone of skeletonized and fluid-preserved museum specimens. Systematic Biology 4: 133-136.
75. Swart BL, Tolley KA, Matthee CA. 2009. Climate change drives speciation in the Southern rock Agama (Agama atra) in the Cape Floristic Region, South Africa. Journal of Biogeography 36: 78-87.
76. Swofford DL. 2002. PAUP phylogenetic analysis using parsimony (and other methods), version 4.10. Champaign, IL: Illinois Natural History Survey.
77. Taylor PJ, Campbell GK, Van Dyk D, Meester J, Willan K. 1992. Genetic variation in the African vlei rat Otomys irroratus. Israel Journal of Zoology 38: 293-305.
78. Taylor PJ, Contrafatto G, Willan K. 1994. Climatic correlates of chromosomal variation in the African vlei rat, Otomys irroratus. Mammalia 58: 623-634.
79. Taylor PJ, Rautenbach IL, Gordon DH, Sink K, Lotter P. 1995. Diagnostic morphometrics and southern African distribution of two sibling species of tree rat, Thallomys paedulcus and Thallomys nigricauda (Rodentia: Muridae). Durban Museum Novitates 20: 49-62.
80. Taylor PJ, Denys C, Mukerjee M. 2004. Phylogeny of the African murid tribe Otomyini (Rodentia), based on morphological and allozyme evidence. Zoologica Scripta 33: 389-402.
81. Taylor PJ, Maree S, van Sandwyk J, Kerbis Peterhans JC, Stanley WT, Verheyen E, Kaliba P, Verheyen W, Kaleme P, Bennett NC. 2009a. Speciation mirrors geomorphology and palaeoclimatic history in African laminate-toothed rats (Muridae: Otomyini) of the Otomys denti and O.lacustris species-complexes in the 'Montane Circle' of East Africa. Biological Journal of the Linnean Society 96: 913-941.
82. Taylor PJ, Maree S, van Sandwyk J, Baxter R, Rambau RV. 2009b. When is a species not a species? Uncoupled phenotypic, karyotypic and genotypic divergence in two species of South African laminate-toothed rats (Murinae: Otomyini). Journal of Zoology 277: 317-332.
83. Templeton AR. 1998. Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Molecular Ecology 7: 381-397.
84. Templeton AR. 2004. Statistical phylogeography: methods of evaluating and minimizing inference error. Molecular Ecology 13: 798-809.
85. Templeton AR, Crandall KA, Sing CF. 1992. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III Caladogram estimation. Genetics 132: 619-633.
86. Templeton AR, Routman E, Phillips CA. 1995. Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum. Genetics 140: 767-782.
87. Tolley KA, Chase BM, Forest F. 2008. Speciation and radiations track climate transitions since the Miocene Climatic Optimum: a case study of southern Africa chameleons. Journal of Biogeography 35: 1402-1414.
88. Tolley KA, Makokha JS, Houniet DT, Swart BL, Matthee CA. 2009. The potential for predicted climate shifts to impact genetic landscapes of lizards in the South African Cape Floristic Region. Molecular Phylogenetics and Evolution 51: 120-130.
89. Vega R, Vazquez-Domingueza E, Mejia-Puentea A, Cuaron AD. 2007. Unexpected high levels of genetic variability and the population structure of an island endemic rodent (Oryzomys couesi cozumelae). Biological Conservation 137: 210-222.
90. Willows-Munro S, Matthee CA. 2009. The evolution of the southern African members of the shrew genus Myosorex: understanding the origin and diversification of a morphologically cryptic group. Molecular Phylogenetics and Evolution 51: 394-398.
91. Yuasa T, Nagata J, Hamasaki S, Tsuruga H, Furubayashi K. 2007. The impact of habitat fragmentation on genetic structure of the Japanese sika deer (Cervus nippon) in southern Kantoh, revealed by mitochondrial d-loop sequences. Ecological Research 22: 97-106.