The Ethiopian highlands represent a remarkable biodiversity 'hot spot' with a very high number of endemic species, even among vertebrates. Ethiopian representatives of a species complex of speckled brush-furred rats (Lophuromys flavopunctatus sensu lato) inhabit highland habitats ranging from low-elevation forests to Afroalpine grasslands. These may serve as a suitable model for understanding evolutionary processes leading to high genetic and ecological diversity in montane biodiversity hot spots. Here, we analyse the most comprehensive genetic data set of this group, comprising 315 specimens (all nine putative Ethiopian Lophuromys taxa sampled across most of their distribution ranges) genotyped at one mitochondrial and four nuclear markers, and thousands of SNPs from ddRAD sequencing. We performed phylogenetic analyses, delimited species and mapped their distribution and estimated divergence time between species (under the species-tree framework) and mitochondrial lineages. We found significant incongruence between mitochondrial and nuclear phylogenies, most probably caused by multiple interspecific introgression events. We discuss alternative scenarios of Ethiopian Lophuromys evolution, from retention of ancestral polymorphism to hybridization upon secondary contact of partially reproductively isolated lineages leading to reticulate evolution. Finally, we use the diversity of the speckled brush-furred rats for the description of the main biogeographic patterns in the fauna of the Ethiopian highlands.

A N Severtsov Institute of Ecology and Evolution Russian Academy of Sciences Moscow Russia

Department of Biology and Institute of Mountain Research and Development Mekelle University Mekelle Tigray Ethiopia

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

Institute of Vertebrate Biology Czech Academy of Sciences Brno Czech Republic

Zobrazit více v PubMed

Aghová, T., Kimura, Y., Bryja, J., Dobigny, G., Granjon, L., & Kergoat, G. J. (2018). Fossils know it best: Using a new set of fossil calibrations to improve the temporal phylogenetic framework of murid rodents (Rodentia: Muridae). Molecular Phylogenetics and Evolution, 128, 98-111. https://doi.org/10.1016/j.ympev.2018.07.017

Bayona-Vásquez, N. J., Glenn, T. C., Kieran, T. J., Pierson, T. W., Hoffberg, S. L., Scott, P. A., Bentley, K. E., Finger, J. W., Louha, S., Troendle, N., Diaz-Jaimes, P., Mauricio, R., & Faircloth, B. C. (2019). Adapterama III: Quadruple-indexed, double/triple-enzyme RADseq libraries (2RAD/3RAD). PeerJ, 7, e7724. https://doi.org/10.7717/peerj.7724

Belay, G., & Mori, A. (2006). Intraspecific phylogeographic mitochondrial DNA (D-loop) variation of Gelada baboon, Theropithecus gelada, Ethiopia. Biochemical Systematics and Ecology, 34(7), 554-561. https://doi.org/10.1016/j.bse.2006.01.004

Bell, M. A., & Lloyd, G. T. (2015). Strap: An R package for plotting phylogenies against stratigraphy and assessing their stratigraphic congruence. Palaeontology, 58(2), 379-389. https://doi.org/10.1111/pala.12142

Bonini, M., Corti, G., Innocenti, F., Manetti, P., Mazzarini, F., Abebe, T., & Pecskay, Z. (2005). Evolution of the Main Ethiopian Rift in the frame of Afar and Kenya rifts propagation. Tectonics, 24(1), 1-21. https://doi.org/10.1029/2004TC001680

Boratyński, Z., Melo-Ferreira, J., Alves, P. C., Berto, S., Koskela, E., Pentikäinen, O. T., Tarroso, P., Ylilauri, M., & Mappes, T. (2014). Molecular and ecological signs of mitochondrial adaptation: Consequences for introgression? Heredity, 113(4), 277-286. https://doi.org/10.1038/hdy.2014.28

Bouckaert, R. R. (2010). DensiTree: Making sense of sets of phylogenetic trees. Bioinformatics, 26, 1372-1373. https://doi.org/10.1093/bioinformatics/btq110

Bryja, J., Colangelo, P., Lavrenchenko, L. A., Meheretu, Y., Šumbera, R., Bryjová, A., & Castiglia, R. (2019). Diversity and evolution of African Grass Rats (Muridae: Arvicanthis) - From radiation in East Africa to repeated colonization of north-western and south-eastern savannas. Journal of Zoological Systematics and Evolutionary Research, 57, 970-988. https://doi.org/10.1111/jzs.12290

Bryja, J., Kostin, D., Meheretu, Y., Šumbera, R., Bryjová, A., Kasso, M., Mikula, O., & Lavrenchenko, L. A. (2018). Reticulate Pleistocene evolution of Ethiopian rodent genus along remarkable altitudinal gradient. Molecular Phylogenetics and Evolution, 118, 75-87. https://doi.org/10.1016/j.ympev.2017.09.020

Bryja, J., Meheretu, Y., Šumbera, R., & Lavrenchenko, L. A. (2019). Annotated checklist, taxonomy and distribution of rodents in Ethiopia. Folia Zoologica, 68(3), 117-213. https://doi.org/10.25225/fozo.030.2019

Burland, T. G. (2000). DNASTAR’s Lasergene sequence analysis software. Bioinformatics Methods and Protocols, 132, 71-91. https://doi.org/10.1385/1-59259-192-2:71

Chalk, T. B., Hain, M. P., Foster, G. L., Rohling, E. J., Sexton, P. F., Badger, M. P. S., Cherry, S. G., Hasenfratz, A. P., Haug, G. H., Jaccard, S. L., Martínez-García, A., Pälike, H., Pancost, R. D., & Wilson, P. A. (2017). Causes of ice age intensification across the Mid-Pleistocene Transition. Proceedings of the National Academy of Sciences of the United States of America, 114(50), 13114-13119. https://doi.org/10.1073/pnas.1702143114.

Craig, E. W., Stanley, W. T., Kerbis Peterhans, J. C., Bryja, J., & Meheretu, Y. (2020). Small terrestrial mammals of Simien Mountains National Park, Ethiopia: A reassessment of elevational distributions after nearly a century. Journal of Mammalogy, 101(3), 634-647. https://doi.org/10.1093/jmammal/gyaa040

Currat, M., Ruedi, M., Petit, R. J., & Excoffier, L. (2008). The hidden side of invasions: Massive introgression by local genes. Evolution, 62, 1908-1920. https://doi.org/10.1111/j.1558-5646.2008.00413.x

deMenocal, P. B. (2004). African climate change and faunal evolution during the Pliocene-Pleistocene. Earth and Planetary Science Letters, 220(1-2), 3-24. https://doi.org/10.1016/S0012-821X(04)00003-2

Drummond, A. J., & Bouckaert, R. R. (2015). Bayesian evolutionary analysis with BEAST. Cambridge University Press. https://doi.org/10.1017/CBO9781139095112

Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29(8), 1969-1973. https://doi.org/10.1093/molbev/mss075

Durand, E. Y., Patterson, N., Reich, D., & Slatkin, M. (2011). Testing for ancient admixture between closely related populations. Molecular Biology and Evolution, 28(8), 2239-2252. https://doi.org/10.1093/molbev/msr048

Eaton, D. A. R., & Overcast, I. (2020). ipyrad: Interactive assembly and analysis of RADseq datasets. Bioinformatics, 36(8), 2592-2594. https://doi.org/10.1093/bioinformatics/btz966

Evans, B. J., Bliss, S. M., Mendel, S. A., & Tinsley, R. C. (2011). The Rift Valley is a major barrier to dispersal of African clawed frogs (Xenopus) in Ethiopia. Molecular Ecology, 20(20), 4216-4230. https://doi.org/10.1111/j.1365-294X.2011.05262.x

Freilich, X., Anadón, J. D., Bukala, J., Calderon, O., Chakraborty, R., & Boissinot, S. (2016). Comparative Phylogeography of Ethiopian anurans: Impact of the Great Rift Valley and Pleistocene climate change. BMC Evolutionary Biology, 16(1), 206. https://doi.org/10.1186/s12862-016-0774-1

Freilich, X., Tollis, M., & Boissinot, S. (2014). Hiding in the highlands: Evolution of a frog species complex of the genus Ptychadena in the Ethiopian highlands. Molecular Phylogenetics and Evolution, 71(1), 157-169. https://doi.org/10.1016/j.ympev.2013.11.015

Frichot, E., & François, O. (2015). LEA: An R package for Landscape and Ecological Association studies. Methods in Ecology and Evolution, 6, 925-929.

Frichot, E., Mathieu, F., Trouillon, T., Bouchard, G., & François, O. (2014). Fast and efficient estimation of individual ancestry coeficients. Genetics, 196, 973-983.

Glenn, T. C., Nilsen, R. A., Kieran, T. J., Sanders, J. G., Bayona-Vásquez, N. J., Finger, J. W., & Garcia-De Leon, F. J. (2019). Adapterama I: Universal stubs and primers for 384 unique dual-indexed or 147,456 combinatorially-indexed Illumina libraries (iTru & iNext). PeerJ, 7, e7755. https://doi.org/10.7717/peerj.7755.

Gottelli, D., Marino, J., Sillero-Zubiri, C., & Funk, S. M. (2004). The effect of the last glacial age on speciation and population genetic structure of the endangered Ethiopian wolf (Canis simensis). Molecular Ecology, 13(8), 2275-2286. https://doi.org/10.1111/j.1365-294X.2004.02226.x

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic acids symposium series, 41(41),95-98.[London]: Information Retrieval Ltd., 1979-2000. https://doi.org/10.1021/bk-1999-0734.ch008

Hill, G. E. (2019). Mitonuclear Ecology. Oxford Series in Ecology and Evolution. Oxford University Press.

Jiang, H., Lei, R., Ding, S. W., & Zhu, S. (2014). Skewer: A fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics, 15(1), 182. https://doi.org/10.1186/1471-2105-15-182

Jones, G. (2017). Algorithmic improvements to species delimitation and phylogeny estimation under the multispecies coalescent. Journal of Mathematical Biology, 74(1-2), 447-467. https://doi.org/10.1007/s00285-016-1034-0

Jones, G., Aydin, Z., & Oxelman, B. (2015). DISSECT: An assignment-free Bayesian discovery method for species delimitation under the multispecies coalescent. Bioinformatics, 31(7), 991-998. https://doi.org/10.1093/bioinformatics/btu770

Kapli, P., Lutteropp, S., Zhang, J., Kobert, K., Pavlidis, P., Stamatakis, A., & Flouri, T. (2017). Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics, 33(11), 1630-1638. https://doi.org/10.1093/bioinformatics/btx025

Kebede, M., Ehrich, D., Taberlet, P., Nemomissa, S., & Brochmann, C. (2007). Phylogeography and conservation genetics of a giant lobelia (Lobelia giberroa) in Ethiopian and Tropical East African mountains. Molecular Ecology, 16(6), 1233-1243. https://doi.org/10.1111/j.1365-294X.2007.03232.x

Kostin, D. S., Kasso, M., Komarova, V. A., Martynov, A. A., Gromov, A. R., Alexandrov, D. Y., Bekele, A., Zewdie, C. H., Bryja, J., & Lavrenchenko, L. A. (2019). Taxonomic and genetic diversity of rodents from the Arsi Mountains (Ethiopia). Mammalia, 83(3), 237-247. https://doi.org/10.1515/mammalia-2017-0135

Kostin, D. S., Martynov, A. A., Komarova, V. A., Alexandrov, D. Y., Yihune, M., Kasso, M., Bryja, J., & Lavrenchenko, L. A. (2020). Rodents of Choke Mountain and surrounding areas (Ethiopia): The Blue Nile gorge as a strong biogeographic barrier. Journal of Vertebrate Biology, 69(2), 1. https://doi.org/10.25225/jvb.20016.

Krásová, J., Mikula, O., Mazoch, V., Bryja, J., Říčan, O., & Šumbera, R. (2019). Evolution of the Grey-bellied pygmy mouse group: Highly structured molecular diversity with predictable geographic ranges but morphological crypsis. Molecular Phylogenetics and Evolution, 130, 143-155. https://doi.org/10.1016/j.ympev.2018.10.016

Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7), 1870-1874. https://doi.org/10.1093/molbev/msw054

Lamboy, W. F. (1994). Computing genetic similarity coefficients from RAPD data: The effects of PCR artifacts. Genome Research, 4(1), 31-37. https://doi.org/10.1101/gr.4.1.31

Lanfear, R., Calcott, B., Ho, S. Y. W., & Guindon, S. (2012). PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695-1701. https://doi.org/10.1093/molbev/mss020

Lavrenchenko, L. A. (2011). Testing of alternative hypotheses for speciation: A case study on ground vertebrates in tropical mountains. Biology Bulletin, 38(6), 551-557. https://doi.org/10.1134/S1062359011060082

Lavrenchenko, L. A., & Bekele, A. (2017). Diversity and conservation of Ethiopian mammals: What have we learned in 30 years? Ethiopian Journal of Biological Sciences, 16(1), 1-20.

Lavrenchenko, L. A., Verheyen, E., Potapov, S. G., Lebedev, V. S., Bulatova, N. S., Aniskin, V. M., Verheyen, W. N., & Ryskov, A. P. (2004). Divergent and reticulate processes in evolution of Ethiopian Lophuromys flavopunctatus species complex: Evidence from mitochondrial and nuclear DNA differentiation patterns. Biological Journal of the Linnean Society, 83(3), 301-316. https://doi.org/10.1111/j.1095-8312.2004.00390.x

Lavrenchenko, L. A., Verheyen, W. N., & Hulselmans, J. (1998). Systematic and distributional notes on the Lophuromys flavopunctatus Thomas, 1888 species-complex in Ethiopia (Muridae-Rodentia). Bulletin De L’institut Royal Des Sciences Naturelles De Belgique, 68, 199-214.

Lavrenchenko, L. A., Verheyen, W. N., Verheyen, E. K., Hulselmans, J., & Leirs, H. (2007). 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’institut Royal Des Sciences Naturelles De Belgique, 77, 77-117.

Librado, P., & Rozas, J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25(11), 1451-1452. https://doi.org/10.1093/bioinformatics/btp187

Mairal, M., Sanmartín, I., Herrero, A., Pokorny, L., Vargas, P., Aldasoro, J. J., & Alarcón, M. (2017). Geographic barriers and Pleistocene climate change shaped patterns of genetic variation in the Eastern Afromontane biodiversity hotspot. Scientific Reports, 7(March), 45749. https://doi.org/10.1038/srep45749

Manthey, J. D., Reyes-Velasco, J., Freilich, X., & Boissinot, S. (2017). Diversification in a biodiversity hotspot: Genomic variation in the river frog Amietia nutti across the Ethiopian Highlands. Biological Journal of the Linnean Society, 122(4), 801-813. https://doi.org/10.1093/BIOLINNEAN/BLX106

Martin, S. H., Davey, J. W., & Jiggins, C. D. (2015). Evaluating the use of ABBA-BABA statistics to locate introgressed loci. Molecular Biology and Evolution, 32(1), 244-257. https://doi.org/10.1093/molbev/msu269

Martin, S. H., Davey, J. W., Salazar, C., & Jiggins, C. D. (2019). Recombination rate variation shapes barriers to introgression across butterfly genomes. PLOS Biology, 17(2), e2006288. https://doi.org/10.1371/journal.pbio.2006288

Melo-Ferreira, J., Vilela, J., Fonseca, M. M., da Fonseca, R. R., Boursot, P., & Alves, P. C. (2014). The elusive nature of adaptive mitochondrial DNA evolution of an arctic lineage prone to frequent introgression. Genome Biology and Evolution, 6(4), 886-896. https://doi.org/10.1093/gbe/evu059

Mikula, O. (2018). Cutting tree branches to pick OTUs: A novel method of provisional species delimitation for phylogenetic and ecological studies. BioRxiv, 419887, https://doi.org/10.1101/419887.

Miller, M. A., Pfeiffer, W., & Schwartz, T. (2012). The CIPRES science gateway: enabling high-impact science for phylogenetics researchers with limited resources. In Proceedings of the 1st Conference of the Extreme Science and Engineering Discovery Environment: Bridging from the eXtreme to the campus and beyond (p. 39). ACM. https://doi.org/10.1145/2335755.2335836

Mittermeier, R. A., Turner, W. R., Larsen, F. W., Brooks, T. M., & Gascon, C. (2011). Global biodiversity conservation: the critical role of hotspots. In: F. E. Zachos & J. C. Habel (Eds.), Biodiversity hotspots (pp. 3-22). Springer. https://doi.org/10.1007/978-3-642-20992-5_1

Mizerovská, D., Mikula, O., Meheretu, Y., Bartáková, V., Bryjová, A., Kostin, D. S., Šumbera, R., Lavrenchenko, L. A., & Bryja, J. (2020). Integrative taxonomic revision of the Ethiopian endemic rodent genus Stenocephalemys (Muridae: Murinae: Praomyini) with the description of two new species. Journal of Vertebrate Biology, 69, 20031. https://doi.org/10.25225/jvb.20031

Peterson, B. K., Weber, J. N., Kay, E. H., Fisher, H. S., & Hoekstra, H. E. (2012). Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One, 7(5), e37135. https://doi.org/10.1371/journal.pone.0037135

Puillandre, N., Lambert, A., Brouillet, S., & Achaz, G. (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21(8), 1864-1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x

QGIS Development Team (2016). QGIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org

A. Rambaut, A. J. Drummond, M. A. Suchard, & D. Xie (Eds.) (2014). Tracer v1. 6. Computer program and documentation distributed by the author.

Remington, C. L. (1968). Suture-zones of hybrid interaction between recently joined biotas. In (T. Dobzhansky, M. K. Hecht, & W. C. Steere, Eds) Evolutionary Biology (pp. 321-428). Springer. https://doi.org/10.1007/978-1-4684-8094-8_8

Reyes-Velasco, J., Manthey, J. D., Bourgeois, Y., Freilich, X., & Boissinot, S. (2018). Revisiting the phylogeography, demography and taxonomy of the frog genus Ptychadena in the Ethiopian highlands with the use of genome-wide SNP data. PLoS One, 13(2), 1-23. https://doi.org/10.1371/journal.pone.0190440.

Reyes-Velasco, J., Manthey, J. D., Freilich, X., & Boissinot, S. (2018). Diversification of African tree frogs (genus Leptopelis) in the highlands of Ethiopia. Molecular Ecology, 27(9), 2256-2270. https://doi.org/10.1111/mec.14573

Rieseberg, L. H. (1996). Homology among RAPD fragments in interspecific comparisons. Molecular Ecology, 5(1), 99-105. https://doi.org/10.1111/j.1365-294X.1996.tb00295.x

Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574. https://doi.org/10.1093/bioinformatics/btg180

Ropiquet, A., & Hassanin, A. (2006). Hybrid origin of the Pliocene ancestor of wild goats. Molecular Phylogenetics and Evolution, 41(2), 395-404. https://doi.org/10.1016/j.ympev.2006.05.033

Sloan, D. B., Havird, J. C., & Sharbrough, J. (2017). The on-again, off-again relationship between mitochondrial genomes and species boundaries. Molecular Ecology, 26(8), 2212-2236. https://doi.org/10.1111/mec.13959

Stamatakis, A. (2014). RAxML Version 8: A tool for phylogenetic analysis and postanalysis of large phylogenies. Bioinformatics, 30, 1312-1313. https://doi.org/10.1093/bioinformatics/btu033

Šumbera, R., Krásová, J., Lavrenchenko, L. A., Mengistu, S., Bekele, A., Mikula, O., & Bryja, J. (2018). Ethiopian highlands as a cradle of the African fossorial root-rats (genus Tachyoryctes), the genetic evidence. Molecular Phylogenetics and Evolution, 126, 105-115. https://doi.org/10.1016/j.ympev.2018.04.003

Taylor, P. J., Lavrenchenko, L. A., Carleton, M. D., Verheyen, E., Bennet, N. C., Oosthuizen, C. J., & Maree, S. (2011). Specific limits and emerging diversity patterns in East African populations of laminate- toothed rats, genus Otomys (Muridae: Otomyini): Revision of the Otomys typus complex. Zootaxa, 3024, 1-66. https://doi.org/10.11646/zootaxa.3024.1.1

Toews, D. P. L., & Brelsford, A. (2012). The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology, 21(16), 3907-3930. https://doi.org/10.1111/j.1365-294X.2012.05664.x

Vaidya, G., Lohman, D. J., & Meier, R. (2011). SequenceMatrix: Concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics, 27(2), 171-180. https://doi.org/10.1111/j.1096-0031.2010.00329.x

Verheyen, W. N., Hulselmans, J. L., Dierckx, T., Mulungu, L. S., Leirs, H., Corti, M., & Verheyen, E. (2007). The characterization of the Kilimanjaro Lophuromys aquilus True 1892 population and the description of five new Lophuromys species (Rodentia, Muridae). Bulletin De L'institut Royal Des Sciences Naturelles De Belgique: Biologie, 77, 23-75.

Yalden, D. W., & Largen, M. J. (1992). The endemic mammals of Ethiopia. Mammal Review, 22, 115-150. https://doi.org/10.1111/j.1365-2907.1992.tb00128

Yalden, D. W., Largen, M. J., & Kock, D. (1976). Catalogue of the mammals of Ethiopia: 2. Insectivora and Rodentia: pubblicazioni del centro di studio per la faunistica ed ecologia tropicali del cnr: cxi. Monitore Zoologico Italiano. 8(1), 1-118. https://doi.org/10.1080/03749444.1976.10736830

Yalden, D. W., Largen, M. J., Kock, D., & Hillman, J. C. (1996). Catalogue of the mammals of Ethiopia and Eritrea. 7. Revised checklist, zoogeography and conservation. Tropical Zoology, 9, 73-164. https://doi.org/10.1080/03946975.1996.10539304

Yang, Z. (2007). PAML 4: Phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24(8), 1586-1591. https://doi.org/10.1093/molbev/msm088

Yannic, G., Dubey, S., Hausser, J., & Basset, P. (2010). Additional data for nuclear DNA give new insights into the phylogenetic position of Sorex granarius within the Sorex araneus group. Molecular Phylogenetics and Evolution, 57(3), 1062-1071. https://doi.org/10.1016/j.ympev.2010.09.015

Zhang, J., Kobert, K., Flouri, T., & Stamatakis, A. (2014). PEAR: A fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics, 30(5), 614-620. https://doi.org/10.1093/bioinformatics/btt593

Historical biogeography, systematics, and integrative taxonomy of the non-Ethiopian speckled pelage brush-furred rats (Lophuromys flavopunctatus group)

Zobrazit více v PubMed

Dryad
10.5061/dryad.stqjq2c2r