Comparative Phylogeography of Three Endemic Rodents from the Albertine Rift, East Central Africa

Molecular Ecology (2007) 16, 663–674 doi: 10.1111/j.1365-294X.2007.03153.x ComparativeBlackwell Publishing Ltd phylogeography of three endemic rodents from the Albertine Rift, east central Africa MICHAEL H. HUHNDORF,*† JULIAN C. KERBIS PETERHANS†‡ and SABINE S. LOEW*† *Department of Biological Sciences, Behaviour, Ecology, Evolution and Systematics Section, Illinois State University, Normal, Illinois 61790-4120, USA, †Department of Zoology, The Field Museum, Chicago, Illinois, 60605-2496, USA, ‡University College, Roosevelt University, Chicago, Illinois, 60605, USA Abstract The major aim of this study was to compare the phylogeographic patterns of codistributed rodents from the fragmented montane rainforests of the Albertine Rift region of east central Africa. We sampled individuals of three endemic rodent species, Hylomyscus denniae, Hybomys lunaris and Lophuromys woosnami from four localities in the Albertine Rift. We analysed mitochondrial DNA sequence variation from fragments of the cytochrome b and control region genes and found significant phylogeographic structuring for the three taxa examined. The recovered phylogenies suggest that climatic fluctuations and volcanic activity of the Virunga Volcanoes chain have caused the fragmentation of rainforest habitat during the past 2 million years. This fragmentation has played a major role in the diversification of the montane endemic rodents of the region. Estimation of the divergence times within each species suggests a separation of the major clades occurring during the mid to late Pleistocene. Keywords: Africa, Albertine Rift, control region, cytochrome b, phylogeography, rodent Received 26 May 2006; revision accepted 1 September 2006 The Albertine Rift is the western branch of the Great Rift Introduction Valley in central and east Africa. It lies in the eastern Different biogeographical processes than those of the Democratic Republic of Congo (DR Congo), western Uganda, Northern Hemisphere have shaped the evolutionary history Rwanda, Burundi and Tanzania. The Albertine Rift has of taxa of east central Africa. The advance and retreat been formed by uplifting of pre-Cambrian rock during the of glaciers during the Quaternary were a major force in Miocene and by volcanic activity that began during the shaping the biodiversity on the continents of the Northern Plio–Pleistocene and that continues to this day. The main Hemisphere. These glacial periods corresponded to cool feature of the Albertine Rift is a chain of mountains stretching and dry periods in tropical west and east Africa (deMenocal from Lake Albert in the north to the southern end of Lake 1995), which presumably led to the periodic fragmentation Tanganyika (Fig. 1). The ecoregion is dominated by montane of the lowland rainforest of west and central Africa. The rainforest [1500–3500 metres above sea level (m a.s.l.) ‘refuge theory’ (Haffer 1969) postulates that periods of altitude] but is bordered by a lowland forest/savanna mosaic climatic fluctuation caused rainforests to become frag- to the east and west down to altitudes of 500–800 m a.s.l. mented and isolated and then reconnected thus leading to Volcanic activity and rifting in combination with climatic the high species diversification seen in the lowland tropics. change during the mid- to late-Pleistocene created complex Climatic change during the Plio–Pleistocene has also been patterns of habitat fragmentation and expansion/contraction suggested as the major force driving diversification in cycles of montane vegetation in the Albertine Rift (Morrison east African montane rainforests (Fjeldsa & Lovett 1997; 1968; Morrison & Hamilton 1974; Hamilton 1982). These Roy 1997; Roy et al. 2001). Additionally, geologic activity, patterns are consistent with proposed hypotheses (Fjeldsa i.e. volcanic activity, during this time period may have & Lovett 1997; Roy et al. 2001) of diversification in montane played an equal role in shaping the diversification of the rainforests. At several historical stages volcanic activity Albertine Rift. reduced or eliminated the vegetation around the eight present volcanoes of the Virungas chain (Fig. 1). This may Correspondence: Michael H. Huhndorf, Fax: 309-438-3722; E-mail: have separated the Albertine Rift into northern and southern [email protected] biogeographical regions. Additionally, the volcanic activity © 2007 The Authors Journal compilation © 2007 Blackwell Publishing Ltd 664 M. H. HUHNDORF, J. C. KERBIS PETERHANS and S . S . LOEW Fig. 1 Montane regions (grey) of the Albertine Rift. Modified from Dieterlen (1976). Black circles with white dots indicate the four sampling locales included in this study (Appendix). RWE, Rwenzori Mountains National Park; BWI, Bwindi Impenetrable Forest National Park; MGA, Mgahinga Gorilla National Park; KIB, Kibira National Park. All three taxa are distributed across the montane forests of the Albertine Rift. in the Virungas altered the hydrology of the central Albertine the montane forest zone. These three taxa are codistributed Rift (Beadle 1981) which may have created potential in disjunct populations across the Albertine Rift but vary biogeographical barriers due to altered rivers and lakes slightly in their habitat preferences. Hylomyscus denniae, that isolated certain montane areas from one another. This climbing wood mouse, is restricted to mid to high-altitude complex geological history and high biodiversity make the montane forests and the afro-alpine zone (1900–4000 m Albertine Rift ideally suited to test specific hypotheses a.s.l.), it is strictly arboreal in the montane forest but is on the relationship between biogeography and species more terrestrial in the higher afro-alpine zone. diversification in east central Africa, nevertheless the Lophuromys woosnami, brush-furred mouse, is restricted comparative phylogeography of the montane dependent to mid to high-altitude montane forests (1900–3000 m a.s.l.), fauna of the Albertine Rift has received little attention and is mainly terrestrial and found in wetter areas of the forests. remains poorly understood. H. lunaris, Rwenzori striped mouse, is restricted to low Our study focuses on three rodent species endemic to to mid-elevation montane forests (1500–2700 m a.s.l.), is the Albertine Rift montane forest biotic region, Hylomyscus terrestrial and prefers areas near water. denniae, Hybomys lunaris and Lophuromys woosnami. The For all three taxa, we obtained DNA sequence data from complete limits of their distributions within the Albertine two mitochondrial DNA (mtDNA) markers, the cytochrome- Rift is unknown as some areas have never been surveyed; b gene and the noncoding control region to examine the however, it is presumed that they are found throughout evolutionary history of Albertine Rift fauna. Using the © 2007 The Authors Journal compilation © 2007 Blackwell Publishing Ltd PHYLOGEOGRAPHY OF ALBERTINE RIFT RODENTS 665 principles of vicariance biogeography (Rosen 1978; Nelson Appendix for details). Unique DNA sequences have been & Platnick 1981), we can use phylogenies of mtDNA submitted to GenBank under Accession nos DQ902717– lineages to develop hypotheses about levels of endemism DQ902827. and area-relationships among the montane forests of the Albertine Rift. Congruent patterns among codistributed DNA extraction and sequencing taxa are evidence that these taxa share a common history of response to vicariant events (Cracraft 1985). Using the Total genomic DNA was extracted from 0.25 g or less of general hypothesis that unique mtDNA lineages will liver, heart or muscle tissue using the commercially evolve in allopatry, we specifically addressed the follow- available DNeasy Tissue Kit (QIAGEN). For this study, ing three questions: (i) Are there distinct mtDNA lineages we compared sequences from fragments of two mtDNA within H. denniae, H. lunaris and L. woosnami? (ii) How genes, cytochrome b and the control region (D-loop). Primers are mtDNA lineages geographically distributed within the H14542 and L14115 (Smith & Patton 1991) were used to Albertine Rift? (iii) What is the degree of phylogeographic amplify a 426-bp segment of the mtDNA cytochrome b concordance of mtDNA lineages among the three taxa? On gene. Primer names correspond to the 3′ base of the primer the basis of the three species geographical distributions, in the complete mtDNA sequence of Mus (Bibb et al. 1981). the geological history and the current fragmentation seen Primers CBT and MR1 (Morzunov et al. 1998), corresponding among the montane rainforests we expect to see congruent to bases 15 393 and 15 777 of the mtDNA Mus sequence, phylogeographic patterns and make the following predic- were used to amplify a 427-bp segment of the mtDNA tions. First, since all three taxa are dependent upon montane D-loop. Fragments were amplified by polymerase chain rainforest and are codistributed, historic biogeographical reaction (PCR) using the following parameters for cytoch- barriers will have affected them similarly and they will rome b: denaturation at 93 °C for 30 s, annealing at 60 °C exhibit phylogenetic breaks in similar geographical locations. for 30 s and extension at 72 °C for 1 min for a total of 30 Second, we expect phylogenetic patterns to show a northern cycles. The parameters used for the D-loop amplification and southern region centred on the Virunga Volcanoes were: denaturation at 93 °C for 30 s, annealing at 48 °C for because the volcanic activity during the past 2 million 30 s and extension at 72 °C for 2 min for a total of 40 cycles. years has altered

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