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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by NERC Open Research Archive Article (refereed) - postprint Odee, D.W.; Telford, A.; Wilson, J.; Gaye, A.; Cavers, S. 2012 Plio- Pleistocene history and phylogeography of Acacia senegal in dry woodlands and savannahs of sub-Saharan tropical Africa: evidence of early colonisation and recent range expansion. Heredity, 109 (6). 372-382. 10.1038/hdy.2012.52 Copyright © 2012 Macmillan Publishers Limited This version available http://nora.nerc.ac.uk/18782 / NERC has developed NORA to enable users to access research outputs wholly or partially funded by NERC. Copyright and other rights for material on this site are retained by the rights owners. Users should read the terms and conditions of use of this material at http://nora.nerc.ac.uk/policies.html#access This document is the author’s final manuscript version of the journal article following the peer review process. Some differences between this and the publisher’s version may remain. You are advised to consult the publisher’s version if you wish to cite from this article. www.nature.com/ Contact CEH NORA team at [email protected] The NERC and CEH trademarks and logos (‘the Trademarks’) are registered trademarks of NERC in the UK and other countries, and may not be used without the prior written consent of the Trademark owner. 1 Plio-Pleistocene history and phylogeography of Acacia senegal in dry 2 woodlands and savannahs of sub-Saharan tropical Africa: evidence of early 3 colonisation and recent range expansion 4 5 DW Odee1,2*, A Telford1, J Wilson1, A Gaye3 and S Cavers1 6 7 8 1 Centre for Ecology & Hydrology, Bush Estate, Penicuik, Midlothian EH26 0QB, Scotland, 9 UK 10 2 Kenya Forestry Research Institute, P.O Box 20412-00200, Nairobi, Kenya 11 3 Institut Sénégalais de Recherches Agricoles (ISRA), B.P. 3120, Dakar, Senegal 12 13 14 Address for correspondence: *Centre for Ecology & Hydrology, Bush Estate, Penicuik, 15 Midlothian EH26 0QB, Scotland, UK 16 Tel. 0131 445 4343, Fax. 0131 445 3943 17 * Email [email protected] 18 19 Running head: Phylogeography of Acacia senegal 20 Total word count: 6 485 21 1 22 Abstract 23 The gum arabic tree (Acacia senegal) is an arid-adapted, morphologically diverse species 24 (varieties senegal, kerensis, rostrata and leiorhachis) widespread in the extensive but 25 relatively little-studied dry woodland and savannah biomes of sub-Saharan tropical Africa. 26 We used variation in nuclear ribosomal DNA (nrDNA) internal transcribed spacer (ITS) 27 sequences and chloroplast DNA markers (polymerase chain reaction-restriction fragment 28 length polymorphism [PCR-RFLP] and chloroplast microsatellites [cpSSR]) to study the 29 phylogeography of the species with 293 individuals from 66 populations sampled across its 30 natural range. The predominant pattern was a phylogeographic distinction between West and 31 Central African, and East and Southern African haplotypes. Phylogenetic analysis of ITS data 32 indicated a more recent origin for the clade including West and Central African haplotypes, 33 suggesting range expansion in the Sudano-Sahelian region, probably as recently as the 34 Holocene humid period. Variety leiorhachis formed a single clade while the other three were 35 mixed and some evidence for hybridization between A. senegal and other Acacia species was 36 present. Chloroplast DNA data showed high regional and rangewide haplotypic diversity 37 (hT(cpSSR) = 0.903 - 0.948) and population differentiation (GST(RFLP) = 0.700 - 0.782) with a 38 phylogeographic pattern that indicated extensive historical gene flow via seed dispersal. 39 Haplotypes were not restricted to any of the four varieties, but showed a significant 40 geographic structuring of genetic variation (GST(cpSSR) = 0.392; RST = 0.673; RST > RST 41 (permuted)), with the major division separating East and Southern Africa populations from 42 those in West and Central Africa. In conjunction with paleobotanical evidence, our data 43 suggests dispersal to West Africa, and across to the Arabian Peninsula and Indian 44 subcontinent from source populations located in the East African region during climate 45 oscillations of the Plio-Pleistocene. 2 46 47 Keywords: Aridity, gum arabic, hybridization, long-distance dispersal, phylogeny, refugia 48 49 3 50 Introduction 51 Modern dry woodland and savannah biomes, dominated by grasses and woody species, are 52 key ecosystems in sub-Saharan tropical Africa (Plana, 2004). With a species composition and 53 diversity that is driven by low rainfall and pronounced dry seasons (Jacobs, 2004), they 54 evolved during the Miocene (23-5 Mya), a period associated with drastic lowering of global 55 temperatures and increasing aridity that saw the replacement of once expansive extensive 56 lowland rainforests with savannah woodland (Plana, 2004). From the Plio-Pleistocene 57 onwards (from ~ 5 Mya), the species that occupy these biomes have experienced cyclical 58 range expansions and contractions due to climatic oscillations (Maley, 2001; Plana, 2004), 59 restricted by aridification on one hand and moist forest expansion on the other. Thus the 60 genetic structure of widely distributed dryland tree species is likely to reflect the influence of 61 these processes. 62 63 The interplay of major geomorphological features with climate oscillations has also 64 played a key role in shaping the genetic patterns and phylogeography of flora and fauna since 65 the end of the Pliocene (~ 3.5 Mya, deMenocal, 1995). For example, contraction and 66 expansion of the Sahara desert in Central and West Africa, and interaction of climate with the 67 Great Rift Valley and the elevated topographies of East and Southern Africa produced wide 68 altitudinal ranges forming a complex mosaic of landscapes and localised climate regimes that 69 functioned as refugia during extreme climate conditions (Plana, 2004; Lorenzen et al., 2010). 70 71 Previous phylogeographic studies of tropical African tree species have largely 72 focussed on moist forests (montane, lowland or rainforests) and have typically interpreted 73 results with respect to Pleistocene refugia (e.g. Hagenia abyssinica, Ayele et al., 2009; 4 74 Milicia excelsa, Daïnou et al., 2010; Irvingia gabonensis, Lowe et al., 2010). It has been 75 suggested that previously continuous rainforests fragmented into refugia within mountainous 76 areas and became separated by the expansion of savannah vegetation during glacial maxima 77 associated with cooler and drier conditions (Plana, 2004). Dry woodlands and savannahs are 78 likely to have experienced the same processes in reverse, and fragmented dryland habitats 79 may have acted as refugia for arid-adapted species during warmer and wetter periods (Plana, 80 2004). Relics of xeric vegetation or savannah enclaves persisting today in the Central and 81 West African rain forest since the last glacial maximum (LGM) may represent such refuges 82 (Maley, 2001). 83 84 A few savannah-type or dry woodland tree species have been studied, mainly in the 85 Brazilian cerrado (e.g. Caryocar brasilensis, Collevatti et al., 2003; Hymenaea stigonocarpa, 86 Ramos et al., 2007; Astronium urundeuva, Caetano et al., 2008) and others in the seasonally 87 dry tropical forests (SDTFs, Pennington et al., 2004; Pennington et al., 2009). Species in the 88 latter show patterns of diversity, endemism and phylogeny that indicate historically stable and 89 dispersal-limited systems, caused partly by the widespread patchy distribution of this biome 90 and its persistence over evolutionary timescales regarded as Pleistocene refugia (Pennington 91 et al., 2004; Collevatti et al., 2003; Caetano et al., 2008;). Although SDTFs share some of the 92 ecological characteristics of dry woodlands and savannahs of sub-Saharan Africa (Pennington 93 et al., 2009; Lock, 2006), direct comparisons are limited by phytogeographical differences. In 94 Africa, there have been three major phylogeographic studies of African tree species found in 95 these biomes. A study of Acacia nilotica populations showed genetic differences that broadly 96 matched subspecific designations and a phylogeographic separation of North and West Africa 97 from East and Southern Africa (Wardill et al., 2005). The other two studies, of the baobab 5 98 tree (Adansonia digitata L., Malvaceae; Pock Tsy et al., 2009) and the shea tree (Vitellaria 99 paradoxa C.F.Gaertn, Sapotaceae; Allal et al., 2011) showed strong phylogeographic 100 structure, distinguishing Eastern and Western populations within the Sudano-Sahelian region. 101 However, the ecological distribution of the baobab tree only partially matches that of the dry 102 woodlands and savannahs, and the shea tree has a limited distribution in the Sudano-Sahelian 103 zone. In contrast to plants, there are numerous studies of vertebrates that show development 104 of intraspecific differentiation that coincides with formation of the woodland and savannah 105 biomes in Africa (Jacobs, 2004), e.g. plains zebra, Equus quagga (Lorenzen et al., 2008) and 106 common eland antelope, Taurotragus oryx (Lorenzen et al., 2010). 107 108 Here, we study the phylogenetics and phylogeography of Acacia senegal (L.) Willd. 109 (Leguminosae, Mimosoideae) commonly known as the ‘gum arabic’ tree. Although renowned 110 for its commercial gum, which has been traded for centuries (Fagg and Allison 2004), Acacia 111 senegal also provides other key ecosystem services such as sand stabilization, shade, fodder 112 and forage for livestock and wildlife