Pan-African phylogeny of Mus (subgenus Nannomys) reveals one of the most successful mammal radiations in Africa
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
25496476
PubMed Central
PMC4280006
DOI
10.1186/s12862-014-0256-2
PII: s12862-014-0256-2
Knihovny.cz E-zdroje
- MeSH
- biologická evoluce MeSH
- fylogeneze * MeSH
- fylogeografie MeSH
- myši klasifikace genetika MeSH
- zvířata MeSH
- Check Tag
- myši klasifikace genetika MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- subsaharská Afrika MeSH
BACKGROUND: Rodents of the genus Mus represent one of the most valuable biological models for biomedical and evolutionary research. Out of the four currently recognized subgenera, Nannomys (African pygmy mice, including the smallest rodents in the world) comprises the only original African lineage. Species of this subgenus became important models for the study of sex determination in mammals and they are also hosts of potentially dangerous pathogens. Nannomys ancestors colonized Africa from Asia at the end of Miocene and Eastern Africa should be considered as the place of their first radiation. In sharp contrast with this fact and despite the biological importance of Nannomys, the specimens from Eastern Africa were obviously under-represented in previous studies and the phylogenetic and distributional patterns were thus incomplete. RESULTS: We performed comprehensive genetic analysis of 657 individuals of Nannomys collected at approximately 300 localities across the whole sub-Saharan Africa. Phylogenetic reconstructions based on mitochondrial (CYTB) and nuclear (IRBP) genes identified five species groups and three monotypic ancestral lineages. We provide evidence for important cryptic diversity and we defined and mapped the distribution of 27 molecular operational taxonomic units (MOTUs) that may correspond to presumable species. Biogeographical reconstructions based on data spanning all of Africa modified the previous evolutionary scenarios. First divergences occurred in Eastern African mountains soon after the colonization of the continent and the remnants of these old divergences still occur there, represented by long basal branches of M. (previously Muriculus) imberbis and two undescribed species from Ethiopia and Malawi. The radiation in drier lowland habitats associated with the decrease of body size is much younger, occurred mainly in a single lineage (called the minutoides group, and especially within the species M. minutoides), and was probably linked to aridification and climatic fluctuations in middle Pliocene/Pleistocene. CONCLUSIONS: We discovered very high cryptic diversity in African pygmy mice making the genus Mus one of the richest genera of African mammals. Our taxon sampling allowed reliable phylogenetic and biogeographic reconstructions that (together with detailed distributional data of individual MOTUs) provide a solid basis for further evolutionary, ecological and epidemiological studies of this important group of rodents.
A N Severtsov Institute of Ecology and Evolution RAS Moscow Russia
CNRS UMR 6552 53 Université de Rennes 1 Station Biologique Paimpont France
College of Agriculture and Veterinary Sciences University of Nairobi Nairobi Kenya
Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic
Department of Zoology Faculty of Science University of South Bohemia České Budějovice Czech Republic
Earth Watch Institute Nairobi Kenya
Evolutionary Ecology Group Biology Department University of Antwerp Antwerpen Belgium
Institute of Vertebrate Biology Academy of Sciences of the Czech Republic Brno Czech Republic
Zobrazit více v PubMed
Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B. How many species are there on earth and in the ocean? PLoS Biol. 2011;9(8):e1001127. doi: 10.1371/journal.pbio.1001127. PubMed DOI PMC
Zachos FE, Apollonio M, Bärmann EV, Festa-Bianchet M, Göhlich U, Habel JC, Haring E, Kruckenhauser L, Lovari S, McDevitt AD, Pertoldi C, Rössner GE, Sánchez-Villagra MR, Scandura M, Suchentrunk F. Species inflation and taxonomic artefacts - A critical comment on recent trends in mammalian classification. Mamm Biol. 2013;78:1–6.
Groves CP. The nature of species: A rejoinder to Zachos et al. Mamm Biol. 2013;78:7–9.
Krishna Krishnamurthy P, Francis RA. A critical review on the utility of DNA barcoding in biodiversity conservation. Biodivers Conserv. 2012;21:1907–1919. doi: 10.1007/s10531-012-0306-2. DOI
Hoffmann M, Grubb P, Groves CP, Hutterer R, Van der Straeten E, Simmons N, Bergmans W. A synthesis of African and western Indian Ocean Island mammal taxa (Class: Mammalia) described between 1988 and 2008: an update to Allen (1939) and Ansell (1989) Zootaxa. 2009;2205:1–36.
Macholán M, Baird SJE, Munclinger P, Piálek J. Evolution of the house mouse. New York: Cambridge University Press; 2012.
Chevret P, Veyrunes F, Britton-Davidian J. Molecular phylogeny of the genus Mus (Rodentia: Murinae) based on mitochondrial and nuclear data. Biol J Linnean Soc. 2005;84:417–427. doi: 10.1111/j.1095-8312.2005.00444.x. DOI
Meheretu Y, Šumbera R, Bryja J: Enigmatic Ethiopian endemic rodentMuriculus imberbis(Rüppell 1842) represents a separate lineage within genusMus.Mammalia 2014, in press (doi:10.1515/mammalia-2013-0119).
Britton-Davidian J, Robinson TJ, Veyrunes F. Systematics and evolution of the African pygmy mice, subgenus Nannomys: A review. Acta Oecol. 2012;2012(42):41–49. doi: 10.1016/j.actao.2012.01.001. DOI
Musser GG, Carleton MD. Superfamily Muroidea. In: Wilson DE, Reeder DM, editors. Mammal Species of the World: A Taxonomic and Geographic Reference. Baltimore: Johns Hopkins University Press; 2005. pp. 894–1531.
Veyrunes F, Britton-Davidian J, Robinson TJ, Calvet E, Denys C, Chevret P. Molecular phylogeny of the African pygmy mice, subgenus Nannomys (Rodentia, Murinae, Mus): implications for chromosomal evolution. Mol Phylogenet Evol. 2005;36:358–369. doi: 10.1016/j.ympev.2005.02.011. PubMed DOI
Kan Kouassi S, Nicolas V, Aniskine V, Lalis A, Cruaud C, Couloux A, Colyn M, Dosso M, Koivogui L, Verheyen E, Akoua-Koffi C, Denys C. Taxonomy and biogeography of the African Pygmy mice, Subgenus Nannomys (Rodentia, Murinae, Mus) in Ivory Coast and Guinea (West Africa) Mammalia. 2008;72:237–252.
Fichet-Calvet E, Audenaert L, Barrière P, Verheyen E. Diversity, dynamics and reproduction in a community of small mammals in Upper Guinea, with emphasis on pygmy mice ecology. Afr J Ecol. 2009;48:600–614.
Lamb J, Downs S, Eiseb S, Taylor PJ. Increased geographic sampling reveals considerable new genetic diversity in morphologically conservative African Pygmy Mice (Genus Mus; Subgenus Nannomys) Mamm Biol. 2014;79:24–35.
Matthey R. L'eventail robertsonien chez les Mus (Leggada) africains du groupe minutoides-musculoides. Rev Suisse Zool. 1970;77(3):625–629. PubMed
Jotterand M. Un nouveau système polymorphe chez une nouvelle espèce de Leggada (Mus goundae Petter) Experientia. 1970;26:1360–1361. doi: 10.1007/BF02113032. PubMed DOI
Veyrunes F, Catalan J, Sicard B, Robinson TJ, Duplantier JM, Granjon L, Dobigny G, Britton-Davidian J. Autosome and sex chromosome diversity among the African pygmy mice, subgenus Nannomys. Chromosome Res. 2004;12:369–382. doi: 10.1023/B:CHRO.0000034098.09885.e6. PubMed DOI
Veyrunes F, Watson J, Robinson TJ, Britton-Davidian J. Accumulation of rare sex chromosome rearrangements in the African pygmy mouse, Mus (Nannomys) minutoides: a whole-arm reciprocal translocation (WART) involving a X-autosome fusion. Chromosome Res. 2007;15:223–230. doi: 10.1007/s10577-006-1116-8. PubMed DOI
Veyrunes F, Chevret P, Catalan J, Castiglia R, Watson J, Dobigny G, Robinson TJ, Britton-Davidian J. A novel sex determination system in a close relative of the house mouse. Proc R Soc B. 2010;277:1049–1056. doi: 10.1098/rspb.2009.1925. PubMed DOI PMC
Lecompte E, ter Meulen J, Emonet S, Daffis S, Charrel RN. Genetic identification of Kodoko virus, a novel arenavirus of the African pigmy mouse (Mus Nannomys minutoides) in West Africa. Virology. 2007;364:178–183. doi: 10.1016/j.virol.2007.02.008. PubMed DOI
de Bellocq JG, Borremans B, Katakweba A, Makundi R, Baird SJE, Becker-Ziaja B, Günther S, Leirs L. Sympatric occurrence of 3 arenaviruses, Tanzania. Emerg Infect Dis. 2010;16(4):692–695. doi: 10.3201/eid1604.091721. PubMed DOI PMC
Coulibaly-N’Golo D, Allali B, Kan Kouassi S, Fichet-Calvet E, Becker-Ziaja B, Rieger T, Ölschläger S, Dosso H, Denys C, ter Meulen J, Akoua-Koffi C, Günther S. Novel arenavirus sequences in Hylomyscus sp. and Mus (Nannomys) setulosus from Cote d'Ivoire: Implications for evolution of arenaviruses in Africa. PLoS One. 2011;6:e20893. doi: 10.1371/journal.pone.0020893. PubMed DOI PMC
Kronmann KC, Nimo-Paintsil S, Guirguis F, Kronmann LC, Bonney K, Obiri-Danso K, Ampofo W, Fichet-Calvet E. Two novel arenaviruses detected in Pygmy mice, Ghana. Emerg Infect Dis. 2013;19(11):1832–1835. doi: 10.3201/eid1911.121491. PubMed DOI PMC
Winkler AJ. Neogene paleobiogeography and East African paleoenvironments: contributions from the Tugen Hills rodents and lagomorphs. J Hum Evol. 2002;42:237–256. doi: 10.1006/jhev.2001.0501. PubMed DOI
Lecompte E, Granjon L, Peterhans JK, Denys C. Cytochrome b-based phylogeny of the Praomys group (Rodentia, Murinae): a new African radiation? C R Biol. 2002;325(7):827–840. doi: 10.1016/S1631-0691(02)01488-9. PubMed DOI
Stanhope MJ, Czelusniak J, Si JS, Nickeson J, Goodman M. A molecular perspective on mammalian evolution from the gene encoding interphotoreceptor retinoid binding protein, with convincing evidence for bat monophyly. Mol Phylogenet Evol. 1992;1:148–160. doi: 10.1016/1055-7903(92)90026-D. PubMed DOI
Galan M, Pagès M, Cosson JF. Next-generation sequencing for rodent barcoding: species identification from fresh, degraded and environmental samples. PLoS One. 2012;7(11):e48374. doi: 10.1371/journal.pone.0048374. PubMed DOI PMC
Stamatakis A. RAxML Version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC
Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–1574. doi: 10.1093/bioinformatics/btg180. PubMed DOI
Rambaut A, Drummond AJ. Tracer v1.5. 2007.
Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–1452. doi: 10.1093/bioinformatics/btp187. PubMed DOI
Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol. 2006;55(4):595–609. doi: 10.1080/10635150600852011. PubMed DOI
Powel JR. Accounting for uncertainty in species delineation during the analysis of environmental DNA sequence data. Methods Ecol Evol. 2012;3:1–11. doi: 10.1111/j.2041-210X.2011.00122.x. DOI
Fujisawa T, Barraclough TG. Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: A revised method and evaluation on simulated data sets. Syst Biol. 2013;62(5):707–724. doi: 10.1093/sysbio/syt033. PubMed DOI PMC
Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:1969–1973. doi: 10.1093/molbev/mss075. PubMed DOI PMC
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–2739. doi: 10.1093/molbev/msr121. PubMed DOI PMC
Baker RJ, Bradley RD. Speciation in mammals and the Genetic Species Concept. J Mammal. 2006;87:643–662. doi: 10.1644/06-MAMM-F-038R2.1. PubMed DOI PMC
Lecompte E, Aplin K, Denys C, Catzeflis F, Chades M, Chevret P. Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences with a new tribal classification of the subfamily. BMC Evol Biol. 2008;8:e199. doi: 10.1186/1471-2148-8-199. PubMed DOI PMC
Schenk JJ, Rowe KC, Steppan SJ. Ecological opportunity and incumbency in the diversification of repeated continental colonizations by muroid rodents. Syst Biol. 2013;62:837–864. doi: 10.1093/sysbio/syt050. PubMed DOI
Jacobs LL, Flynn LJ. Of mice… again: the Siwalik rodent record, murine distribution, and molecular clocks. In: Lieberman D, Smith R, Kelley J, editors. Interpreting the past: essays on human, primate and mammal evolution. Leiden: Brill Academic Publishers; 2005. pp. 63–80.
Denys C. Deux nouvelles espèces d’Aethomys(Rodentia, Muridae) à Langebaanweg (Pliocène, Afrique du Sud): Implications phylogénétiques. Annales de Paléontologie. 1990;76:41–69.
Ambrose SH, Bell CJ, Bernor RL, Boisserie J-R, Darwent CM, Degusta D, Deino A, Garcia N, Haile-Selassie Y, Head JJ, Howell FC, Kyule MD, Manthi FK, Mathu EM, Nyamai CM, Saegusa H, Stidham TA, Williams MAJ, Hlusko LJ. The paleoecology and paleogeographic context of Lemudong'o locality 1, a Late Miocene terrestrial fossil site in southern Kenya. Kirtlandia. 2007;56:38–52.
Mein P, Pickford M, Senut B. Late Miocene micromammals from the Harasib karst deposits, Namibia: Part 2b. Cricetomyidae, Dendromuridae and Muridae, with an addendum on the Myocricetodontinae. Commun Geological Surv Namibia. 2004;13:43–61.
Fabre PH, Hautier L, Dimitrov D, Douzery EJP. A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evol Biol. 2012;12:e88. doi: 10.1186/1471-2148-12-88. PubMed DOI PMC
Lemey P, Rambaut A, Drummond AJ, Suchard MA. Bayesian phylogeography finds its roots. PLoS Comput Biol. 2009;5:e1000520. doi: 10.1371/journal.pcbi.1000520. PubMed DOI PMC
Ree RH, Smith SA. Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst Biol. 2008;57(1):4–14. doi: 10.1080/10635150701883881. PubMed DOI
Ree RH, Moore BR, Webb CO, Donoghue MJ. A likelihood framework for inferring the evolution of geographic range in phylogenetic trees. Evolution. 2005;59(11):2299–2311. doi: 10.1111/j.0014-3820.2005.tb00940.x. PubMed DOI
R Core Team . R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2013.
Galtier N, Gouy M, Gautier C. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci. 1996;12:543–548. PubMed
Yalden DW. Small mammals of the Bale Mountains, Ethiopia. Afr J Ecol. 1988;26:281–294. doi: 10.1111/j.1365-2028.1988.tb00980.x. DOI
Lavrenchenko LA. The mammals of the isolated Harenna Forest (southern Ethiopia): structure and history of the fauna. In: Rheinwald G, editor. Isolated Vertebrate Communities in the Tropics. 2000.
Aniskin VM, Lavrenchenko LA, Varshavskii AA, Milishnikov AN. Karyotypes and cytogenetic differentiation of two African mouse species of genus Mus (Rodentia, Muridae) Rus J Genet. 1998;34(1):80–85. PubMed
Yalden DW, Largen MJ, Kock D, Hillman JC. Catalogue of the mammals of Ethiopia and Eritrea. 7. Revised checklist, zoogeography and conservation. Trop Zool. 1996;9:73–164. doi: 10.1080/03946975.1996.10539304. DOI
Dieterlen F, Happold DCD. Mus triton Grey-bellied Pygmy Mouse. In: Happold DCD, editor. Mammals of Africa, Volume III Rodents, hares and rabbits. London and New York: Bloomsbury Publishing; 2013. pp. 497–499.
Yalden DW, Largen MJ. The endemic mammals of Ethiopia. Mamm Rev. 1992;22:115–150. doi: 10.1111/j.1365-2907.1992.tb00128.x. DOI
Vermeiren L, Verheyen WN. Notes sur les Leggada de Lamto, Cote d'Ivoire, avec la description de Leggada baoulei sp. n. (Mammalia, Muridae) Revue de Zoologie Africaine. 1980;94:570–590.
Petter F. Les souris africaines du groupe sorella (Rongeurs, Muridés) Mammalia. 1981;45(3):313–320. doi: 10.1515/mamm.1981.45.3.313. DOI
Mboumba JF, Deleporte P, Colyn M, Nicolas V. Phylogeography of Mus (Nannomys) minutoides (Rodentia, Muridae) in West Central African savannahs: singular vicariance in neighbouring populations. J Zool Syst Evol Res. 2011;49(1):77–85. doi: 10.1111/j.1439-0469.2010.00579.x. DOI
Brouat C, Tatard C, Bâ K, Cosson JF, Dobigny G, Fichet-Calvet E, Granjon L, Lecompte E, Loiseau A, Mouline K, Duplantier JM. Phylogeography of the Guinea Multimammate Mouse (Mastomys erythroleucus): a case study for Sahelian species in West Africa. J Biogeogr. 2009;36:2237–2250. doi: 10.1111/j.1365-2699.2009.02184.x. DOI
Bryja J, Patzenhauerová H, Granjon L, Dobigny G, Konečný A, Duplantier JM, Gauthier P, Colyn M, Durnez L, Lalis A, Nicolas V. Plio-Pleistocene history of West African Sudanian savanna and the phylogeography of the Praomys daltoni complex (Rodentia): the environment/geography/genetic interplay. Mol Ecol. 2010;19:4783–4799. doi: 10.1111/j.1365-294X.2010.04847.x. PubMed DOI
Dobigny G, Tatard C, Gauthier P, Ba K, Duplantier JM, Granjon L, Kergoat GJ. Mitochondrial and nuclear genes-based phylogeography of Arvicanthis niloticus (Murinae) and sub-Saharan open habitats Pleistocene history. PLoS One. 2013;8(11):e77815. doi: 10.1371/journal.pone.0077815. PubMed DOI PMC
Colangelo P, Corti M, Verheyen E, Annesi F, Oguge N, Makundi RH, Verheyen W. Mitochondrial phylogeny reveals differential modes of chromosomal evolution in the genus Tatera (Rodentia: Gerbillinae) in Africa. Mol Phylogenet Evol. 2005;35:556–568. doi: 10.1016/j.ympev.2005.02.012. PubMed DOI
McDonough MM, Sotero-Caio CG, Ferguson AW, Lewis PJ, Tswiio M, Thies ML. Mitochondrial DNA and karyotypic data confirm the presence of Mus indutus and Mus minutoides (Mammalia, Rodentia, Muridae, Nannomys) in Botswana. Zookeys. 2013;359:35–51. doi: 10.3897/zookeys.359.6247. PubMed DOI PMC
Chevret P, Robinson TJ, Perez J, Veyrunes F, Britton-Davidian J. A phylogeographic survey of the Pygmy mouse Mus minutoides in South Africa: Taxonomic and karyotypic inference from cytochrome b sequences of museum specimens. PLoS One. 2014;9(6):e98499. doi: 10.1371/journal.pone.0098499. PubMed DOI PMC
Dobigny G, Tatard C, Kane M, Gauthier P, Brouat C, Ba K, Duplantier JM. A cytotaxonomic and DNA-based survey of rodents from Northern Cameroon and Western Chad. Mammal Biol. 2011;76(4):417–427.
Winkler AJ, Denys C, Avery MD. Rodentia. In: Werdelin L, Sanders WJ, editors. Cenozoic Mammals of Africa. Berkeley: University of California Press; 2010. pp. 263–304.
Isaac JB, Mallet J, Mace GM. Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol Evol. 2004;19:464–469. doi: 10.1016/j.tree.2004.06.004. PubMed DOI
Lavrenchenko LA, Verheyen WN, Verheyen E, Hulselmans J, Leirs H. Morphometric and genetic study of Ethiopian Lophuromys flavopunctatus Thomas, 1888 species complex with description of three new 70-chromosomal species (Muridae, Rodentia) Bulletin de l’Insitut Royal des Sciences Naturelles de Belgique, Biologie. 2007;77:77–117.
Berger SA, Krompass D, Stamatakis A. Performance, accuracy, and web server for evolutionary placement of short sequence reads under maximum likelihood. Syst Biol. 2011;60:291–302. doi: 10.1093/sysbio/syr010. PubMed DOI PMC
Skinner JD, Chimimba CT. The Mammals of the Southern African Subregion. 3. Cambridge, UK: Cambridge University Press; 2005.
Monadjem A. Mus setzeri Setzer’s Pygmy Mouse. In: Happold DCD, editor. Mammals of Africa, Volume III Rodents, hares and rabbits. London and New York: Bloomsbury Publishing; 2013. pp. 493–494.
Vermeiren L, Verheyen WN. Additional data on Mus setzeri Petter (Mammalia, Muridae) Annales Musée Royal de l'Afrique Centrale, ser 8 (Sciences Zoologiques) 1983;237:137–141.
Missoup AD, Nicolas V, Wendelen W, Keming E, Bilong Bilong CF, Couloux A, Atanga E, Hutterer R, Denys C. Systematics and diversification of Praomys species (Rodentia: Muridae) endemic to the Cameroon Volcanic Line (West Central Africa) Zool Scr. 2012;41:327–345. doi: 10.1111/j.1463-6409.2012.00541.x. DOI
Demos TC, Agwanda B, Hickerson MJ. Integrative taxonomy within the Hylomyscus denniae complex (Rodentia: Muridae) and a new species from Kenya. J Mamm. 2014;95(1):1–15. doi: 10.1644/13-MAMM-A-268. DOI
Verheyen WN, Hulselmans JLJ, Dierckx T, Mulungu L, Verheyen E, Corti M, Kerbis JP, Leirs H. Craniometric,cytogenetic and genetic characterization of the Kilimanjaro Lophuromys aquilus True 1892 population, its implications for the taxonomy of the Lophuromys flavopunctatus species complex and description of five new taxa. (Rodentia-Muridae-Africa) Bulletin de l’Insitut Royal des Sciences Naturelles de Belgique, Biologie. 2007;77:23–75.
Colangelo P, Verheyen E, Leirs H, Tatard C, Denys C, Dobigny G, Duplantier JM, Brouat C, Granjon L, Lecompte E. A mitochondrial phylogeographic scenario for the most widespread African rodent, Mastomys natalensis. Biol J Linn Soc. 2013;108(4):901–916. doi: 10.1111/bij.12013. DOI
Potts R. Hominin evolution in settings of strong environmental variability. Quat Sci Rev. 2013;73:1–13. doi: 10.1016/j.quascirev.2013.04.003. DOI
Alvarado-Serrano DF, Knowles LL. Ecological niche models in phylogeographic studies: applications, advances and precautions. Mol Ecol Resour. 2014;14:233–248. doi: 10.1111/1755-0998.12184. PubMed DOI
Šmíd J, Carranza S, Kratochvíl L, Gvoždík V, Nasher AK, Moravec J. Out of Arabia: A complex biogeographic history of multiple vicariance and dispersal events in the gecko genus Hemidactylus (Reptilia: Gekkonidae) PLoS One. 2013;8(5):e64018. doi: 10.1371/journal.pone.0064018. PubMed DOI PMC
Portik DM, Papenfuss TJ. Monitors cross the Red Sea: The biogeographic history of Varanus yemenensis. Mol Phylogenet Evol. 2012;62:561–565. doi: 10.1016/j.ympev.2011.09.024. PubMed DOI
Winney BJ, Hammond RL, Macasero W, Flores B, Boug A, Biquand V, Biquand S, Bruford MW. Crossing the Red Sea: phylogeography of the hamadryas baboon, Papio hamadryas hamadryas. Mol Ecol. 2004;13:2819–2927. doi: 10.1111/j.1365-294X.2004.02288.x. PubMed DOI
Bosworth W, Huchon P, McClay K. The red sea and gulf of aden basins. J Afr Earth Sci. 2005;43:334–378. doi: 10.1016/j.jafrearsci.2005.07.020. DOI
Fernandes CA, Rohling EJ, Siddall M. Absence of post-Miocene Red Sea land bridges: biogeographic implications. J Biogeogr. 2006;33:961–966. doi: 10.1111/j.1365-2699.2006.01478.x. DOI
Catzeflis FM, Denys C. The African Nannomys (Muridae): an early offshoot from the Mus lineage - Evidence from scnDNA hybridization experiments and compared morphology. Isr J Zool. 1992;38:219–231.
Denys C. Of mice and men: Evolution in East and South Africa during Plio-Pleistocene times. In: Bromage TG, Schrenk F, editors. African Biogeography, Climate Change, and Human Evolution. Oxford: Oxford University Press; 1999. pp. 226–252.
Trauth MH, Maslin MA, Deino AL, Strecker MR, Bergner AGN, Dühnforth M. High- and low-latitude forcing of Plio-Pleistocene East African climate and human evolution. J Hum Evol. 2007;53:475–486. doi: 10.1016/j.jhevol.2006.12.009. PubMed DOI
de Menocal PB. African climate change and faunal evolution during the Pliocene-Pleistocene. Earth Planet Sc Lett. 2004;220:3–24. doi: 10.1016/S0012-821X(04)00003-2. DOI
Zachos J, Pagani M, Sloan L, Thomas E, Billups K. Trends, rhythms, and abberations in global climate 65 Ma to present. Science. 2001;292:686–693. doi: 10.1126/science.1059412. PubMed DOI
Schultz S, Maslin M. Early human speciation, brain expansion and dispersal influenced by African climate pulses. PLoS One. 2013;8(10):e76750. doi: 10.1371/journal.pone.0076750. PubMed DOI PMC
Veyrunes F, Catalan J, Tatard C, Cellier-Holzem E, Watson J, Chevret P, Robinson TJ, Britton-Davidian J. Mitochondrial and chromosomal insights into karyotypic evolution of the pygmy mouse, Mus minutoides, in South Africa. Chromosome Res. 2010;18:563–574. doi: 10.1007/s10577-010-9144-9. PubMed DOI
Veyrunes F, Perez J, Paintsil SNC, Fichet-Calvet E, Britton-Davidian J. Insights into the evolutionary history of the X-linked sex reversal mutation in Mus minutoides: clues from sequence analyses of the Y-linked Sry gene. Sex Dev. 2013;7(5):244–252. PubMed
Matthey R. Nouvelles contributions à la cytogénétique des Mus africaines du sous-genre Leggada. Experientia. 1966;22(6):400–401. doi: 10.1007/BF01901163. PubMed DOI
Nichol ST, Arikawa J, Kawaoka Y. Emerging viral diseases. Proc Natl Acad Sci U S A. 2000;2000(97):12411–12412. doi: 10.1073/pnas.210382297. PubMed DOI PMC
Günther S, Lenz O. Lassa virus. Crit Rev Clin Lab Sci. 2004;41:339–390. doi: 10.1080/10408360490497456. PubMed DOI
Hugot JP, Gonzales JP, Denys C. Evolution of the Old World Arenaviridae and their rodent hosts: generalized host-transfer or association by descent? Infect Genet Evol. 2001;1:13–20. doi: 10.1016/S1567-1348(01)00003-X. PubMed DOI