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Rodentia, Gerbilliscus) Illuminates the History of the Somali-Masai Savanna Tatiana AghovA1,2* , Radim Sumbera3, LubomIr PiAlek3, OndRej Mikula1,4, Molly M

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Rodentia, Gerbilliscus) Illuminates the History of the Somali-Masai Savanna Tatiana Aghov�A1,2* , Radim �Sumbera3, Lubom�Ir Pi�Alek3, Ond�Rej Mikula1,4, Molly M Journal of Biogeography (J. Biogeogr.) (2017) ORIGINAL Multilocus phylogeny of East African ARTICLE gerbils (Rodentia, Gerbilliscus) illuminates the history of the Somali-Masai savanna Tatiana Aghova1,2* , Radim Sumbera3, Lubomır Pialek3, Ondrej Mikula1,4, Molly M. McDonough5,6, Leonid A. Lavrenchenko7, Yonas Meheretu8, Judith S. Mbau9 and Josef Bryja1,2 1Institute of Vertebrate Biology of the Czech ABSTRACT Academy of Sciences, 603 65 Brno, Czech Aim The rodent genus Gerbilliscus is widespread in savannas throughout sub- Republic, 2Department of Botany and Saharan Africa. The eastern clade comprises four species with distributions cen- Zoology, Faculty of Science, Masaryk University, 602 00 Brno, Czech Republic, tred in the Somali-Masai biogeographical region of East Africa. We investigated 3Department of Zoology, Faculty of Science, the genetic diversity of the group with a view to illuminating the historical University of South Bohemia, 370 05 Cesk e (Plio-Pleistocene) processes that formed contemporary biota of the understud- Budejovice, Czech Republic, 4Institute of ied Somali-Masai region. Animal Physiology and Genetics of the Czech Location Somali-Masai savanna, East Africa. Academy of Sciences, 602 00 Brno, Czech Republic, 5Center for Conservation Genomics, Methods We performed multilocus genetic analyses of 240 samples from 112 Smithsonian Conservation Biology Institute, localities, combining genotyping of recently collected samples (N = 145), 454- National Zoo, Washington, DC 20008, USA, pyrosequencing of museum material (N = 34) and published sequences 6Department of Vertebrate Zoology, National (N = 61). We used Bayesian and maximum likelihood approaches for phyloge- Museum of Natural History, Smithsonian netic reconstructions, and coalescent-based methods to delimit species. We also Institution, Washington, DC 20560-0108, estimated divergence times and modelled recent and past distributions to 7 USA, A.N. Severtsov Institute of Ecology and reconstruct the major evolutionary influences in the Somali-Masai region dur- Evolution RAS, 119081 Moscow, Russia, ing the Plio-Pleistocene. 8Department of Biology, College of Natural and Computational Sciences, Mekelle Results Genetic analyses provided evidence for six lineages, possibly corre- University, Mekelle, Tigray, Ethiopia, sponding to distinct species. The two main species groups (with two and four 9Department of Land Resource Management putative species, respectively) have overlapping distributions, but species within and Agricultural Technology, College of each group are distributed parapatrically. The origin of the eastern clade dates Agriculture and Veterinary Sciences, back to the Pliocene, while individual species diverged in the Pleistocene. The University of Nairobi, Nairobi, Kenya distribution of genetic diversity and ecological niche modelling point to the importance of the Rift Valley and the presence of unsuitable xeric habitats in the allopatric diversification of Gerbilliscus in the Somali-Masai savanna within *Correspondence: Tatiana Aghova, Institute of the last 5 Myr. Vertebrate Biology ASCR, Research Facility Studenec, 675 02 Studenec, Czech Republic. Conclusions This is the first detailed phylo(bio-)geographical study of ani- Current address: Department of Zoology, mals with predominant distribution in the Somali-Masai region. It revealed National Museum, 115 79 Prague, Czech Republic. currently underestimated diversity of eastern clade of Gerbilliscus and proposed E-mail: [email protected] a scenario of its evolution during Plio-Pleistocene. Conspicuous genetic struc- Dedication ture of these taxa can be now used to test detailed phylogeographical hypothe- We dedicate this paper to the late Bill Stanley ses related to Plio-Pleistocene history of gerbils and, to some extent, also biota who devoted much of his career to the study of Somali-Masai bioregion in general. of small mammals in East Africa. Bill facilitated acquiring numerous samples used in Keywords this study and the promise of future biogeography, Gerbillinae, historical DNA, murid rodents, phylogeography, collaborations was cut short as Bill passed Plio-Pleistocene climate change, pyrosequencing, Rift Valley, species delimita- away unexpectedly during his field trip in Ethiopia in 6 October 2015. tion, tropical Africa ª 2017 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 1 doi:10.1111/jbi.13017 T. Aghova et al. savanna (Fig. 1). The major geomorphological feature here is INTRODUCTION the East African Rift system which has had a long-term Tropical grasslands, savannas and shrublands are the most influence on the climatic regime in Africa (Sepulchre et al., widespread terrestrial habitats in sub-Saharan Africa (Sayre 2006). While this region has relatively low floristic and fau- et al., 2013). These ecosystems, hosting some of the most nistic species diversity, a high level of endemism exists for abundant and diverse mammalian communities on Earth, plants (Thulin, 1993), reptiles (Burgess et al., 2007) and are threatened by increased human activities (Craigie et al., rodents (Varshavsky et al., 2007). This region is home to the 2010). Within the continent they can be divided into four Horn of Africa biodiversity hotspot, which ranks among the main bioregions (sensu Linder et al., 2012): South African, oldest and most stable arid regions of Africa (Kingdon, Zambezian, Sudanian and Somali-Masai, with the last one 1990). In addition, it is one of the least known African corresponding to the ‘Somalia-Masai’ region, originally pro- bioregions and possibly also one of the most threatened due posed by White (1983) as a distinct dry phytochorion, to the rapid increase in human populations and climatic extending from Eritrea to Tanzania (Fig. 1). International changes (Geist & Lambin, 2004). Vegetation Classification (IVC; naturserve.org; Faber-Langen- Despite the biogeographical uniqueness of the Somali- doen et al., 2014) identifies this division as Eastern Africa Masai region, genetic data on organisms living here are Xeric Scrub and Grassland with four ecoregions: (1) Somali, scarce and fragmentary – usually included as part of large- (2) Southern, (3) Northern Acacia-Commiphora bushlands scale phylogenetic reconstructions with under-representative and thickets and (4) Masai xeric grasslands and shrublands geographical sampling. Previous studies found that taxa from (Dixon et al., 2014), referred to herein as Somali-Masai this region are phylogenetically distinct, thereby providing Figure 1 Distribution of species and intraspecific haplogroups of Gerbilliscus in East Africa. Species of the eastern clade are represented with different colours and intraspecific haplogroups are indicated by different symbol shapes. Empty squares represent genetically confirmed records of Gerbilliscus species from the western clade, empty circles those from the southern clade (sensu Granjon et al., 2012), and black crosses indicate localities where Gerbilliscus was not captured during our recent field trappings. The map is based on data from Colangelo et al. (2007, 2010), McDonough et al. (2015), this study and our unpublished data of DNA-barcoded specimens from western and southern clades. Orange background indicates the extent of Somali-Masai savanna, i.e. the distribution of Somali, Northern and Southern Acacia-Commiphora bushlands and thickets (based on WWF records http://www.eoearth.org/). 2 Journal of Biogeography ª 2017 John Wiley & Sons Ltd Phylogeny of Somali-Masai gerbils evidence that the Somali-Masai biota evolved in isolation for been studied in detail. Previously published genetic data an extended period of time (e.g. Smıd et al., 2013; Mikula have been limited to a few specimens genotyped at one et al., 2016). Noteworthy examples include the plant Wajira mitochondrial and one nuclear marker with low variability (Thulin et al., 2004), Grevy’s zebra (Kebede et al., 2016) and (Colangelo et al., 2007) and morphological analyses were warthogs (Randi et al., 2002). However, detailed phylogeo- geographically biased towards Tanzanian localities (Colan- graphical studies of the structure and evolutionary history of gelo et al., 2010). genetic lineages living predominantly in the Somali-Masai Species distributions based on morphological identifica- bioregion are lacking. tions (Monadjem et al., 2015) indicate that the eastern clade Eastern Africa experienced a turbulent climatic and geo- occurs within the borders of the Somali-Masai region and its morphological history during the Plio-Pleistocene. The evolu- genetic analysis may provide insights into the evolutionary tion of its biota was influenced by several major clima- processes that formed the contemporary biota of this region. tic transitions (Maslin & Christensen, 2007), including the We analysed how gerbil divergence dates reflect the geomor- intensification of the Northern Hemisphere glaciation (3.2– phology and climate of the area. More specifically, we tested 2.5 Ma), the development of the Walker circulation if (1) local geomorphological features such as mountain (2.0–1.7 Ma), and the early-middle Pleistocene transition ranges and the Great Rift Valley with its amplifier lakes and (1.2–0.8 Ma) (Maslin & Christensen, 2007; Trauth et al., (2) periods of pronounced climatic variation in the Plio- 2009). In particular, the tropical oscillations between warm Pleistocene influenced genetic structure and divergence and relatively wet pluvials and cooler and drier interpluvials within the eastern clade of Gerbilliscus. during the Pleistocene
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