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Genetic Diversity and Biogeography of the Boab Adansonia Gregorii (Malvaceae: Bombacoideae)

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Genetic Diversity and Biogeography of the Boab Adansonia Gregorii (Malvaceae: Bombacoideae) CSIRO PUBLISHING Australian Journal of Botany, 2014, 62, 164–174 http://dx.doi.org/10.1071/BT13209 Genetic diversity and biogeography of the boab Adansonia gregorii (Malvaceae: Bombacoideae) Karen L. Bell A,B,E, Haripriya Rangan B, Rachael Fowler A,B, Christian A. Kull B, J. D. Pettigrew C, Claudia E. Vickers D and Daniel J. Murphy A ARoyal Botanic Gardens Melbourne, Birdwood Avenue, South Yarra, Vic. 3141, Australia. BSchool of Geography and Environmental Science, Monash University, Clayton, Vic. 3800, Australia. CQueensland Brain Institute, University of Queensland, St Lucia, Qld 4072, Australia. DAustralian Institute for Bioengineering and Nanotechnology, University of Queensland, St Lucia, Qld 4072, Australia. ECorresponding author. Email: [email protected] Abstract. The Kimberley region of Western Australia is recognised for its high biodiversity and many endemic species, including the charismatic boab tree, Adansonia gregorii F.Muell. (Malvaceae: Bombacoideae). In order to assess the effects of biogeographic barriers on A. gregorii, we examined the genetic diversity and population structure of the tree species across its range in the Kimberley and adjacent areas to the east. Genetic variation at six microsatellite loci in 220 individuals from the entire species range was examined. Five weakly divergent populations, separated by west–east and coast–inland divides, were distinguished using spatial principal components analysis. However, the predominant pattern was low geographic structure and high gene flow. Coalescent analysis detected a population bottleneck and significant gene flow across these inferred biogeographic divides. Climate cycles and coastline changes following the last glacial maximum are implicated in decreases in ancient A. gregorii population size. Of all the potential gene flow vectors, various macropod species and humans are the most likely. Additional keywords: Australian monsoon tropics, baobab, dispersal, gene flow, genetic admixture, Kimberley, microsatellite, phylogeography. Received 23 August 2013, accepted 12 April 2014, published online 22 May 2014 Introduction of populations (phylogeographic divergence), and adaptation The Kimberley region of north-west Australia has high to different habitat types (ecological divergence). Whereas biodiversity and many endemic species. It represents the these studies have provided insights into the distribution and westernmost region of the Australian monsoon tropics (AMT), divergence of some endemic Kimberley animal species, there characterised by highly seasonal rainfall and savanna vegetation. are no similar studies on intraspecific genetic variation of plants. The Kimberley Plateau is one of the three sandstone blocks in Under the same environmental influences, plant taxa would be the AMT, along with Arnhem Land and Cape York. It is separated expected to exhibit similar patterns of geographic variation to from the neighbouring Arnhem Land Plateau by the lowlands of those recorded for animals. This study examines the intraspecific a former Cretaceous sea floor (Bowman et al. 2010). The AMT genetic diversity and variation among populations of Adansonia biome is bounded to the south by arid habitats, which began gregorii F.Muell. (Malvaceae: Bombacoideae) in the Kimberley. developing in the Late Cenozoic and contain distinctly different These data are used to test the potential importance of previously biota (Byrne et al. 2008; Bowman et al. 2010). Several studies identified biogeographic barriers, and their influence on genetic have identified biogeographic barriers between the Kimberley divergence in this species. and Arnhem Land plateaus, including the ‘Bonaparte Gap’, the Adansonia gregorii (commonly called boab), was first ‘Ord Arid Intrusion’, the ‘Victoria River Drainage’, and the ‘Daly mentioned by Allan Cunningham, naturalist on the HMAS River Drainage’ (Eldridge et al. 2011). Within the Kimberley, Mermaid, who assigned it to the genus Capparis,asC. gibbosa a phylogeographic pattern comprising an ‘east–west Kimberley (Cunningham 1827). Later, Ferdinand von Mueller, on the divide’ (Eldridge et al. 2011), has been defined for multiple Gregory Expedition, recognised the affinity of this taxon with species (Hill and Johnson 1995; Oliver et al. 2010; Melville the genus Adansonia and named the species A. gregorii (von et al. 2011; Potter et al. 2012b). Heterogeneous environments Mueller 1857, 1858). In 2004, the Nomenclature Committee may have contributed to allopatric divergence through isolation for Spermatophyta ruled to conserve the name A. gregorii Journal compilation Ó CSIRO 2014 www.publish.csiro.au/journals/ajb Genetic diversity of Adansonia gregorii Australian Journal of Botany 165 (Brummitt 2002), and we use this name in the present paper. Following the Interim Biogeographical Regionalisation for A. gregorii is an ideal plant taxon for examining geographic Australia (Australian Government Department of Sustainability variation across the Kimberley, being a significant component 2012), A. gregorii is mainly confined to the Dampierland, Central of the vegetation and having a distribution that extends across Kimberley, Northern Kimberley and Victoria Bonaparte almost the entire Kimberley region and adjacent regions to subregions, with a minor extension eastward into the Ord the east in the Northern Territory (Baum 1995b, Baum et al. Victoria Plains (see Fig. 1). To the south, its distribution is 1998). bounded by the semiarid environments of the Great Sandy Adansonia gregorii is the sole member of the genus Desert and the Tanami Desert, which are too dry to support Adansonia occurring in Australia. Other Adansonia species the species (Wickens and Lowe 2008). The distribution of occur in Africa and Madagascar (Baum 1995b; Wickens and A. gregorii extends to the coastline which forms the northern Lowe 2008; Pettigrew et al. 2012). Earlier researchers thought bounds of the Kimberley (von Mueller 1893; Gillison 1983; the disjunct distributions of baobabs in Australia, Africa and Brock 1988; Baum and Handasyde 1990; Wickens and Lowe Madagascar were due to the break-up of Gondwana, although 2008). The distributional boundary to the east is less clear. the alternative hypothesis of more recent trans-oceanic dispersal Bowman (1997) questioned why A. gregorii is not distributed was proposed well before any attempts to date the divergences further east in the Gulf region of the Northern Territory where between species (Raven and Axelrod 1974; Armstrong 1979, the environmental conditions are similar to those of north- 1983). Molecular divergence dating suggests that A. gregorii western Australia. He suggested that its absence might be shared a common ancestor with other extant Adansonia species related to long-term fire history, and that changes in human in the Miocene, which is too late to be attributable to Gondwanan modification of the landscape in the past two centuries, fragmentation (Baum et al. 1998). including overgrazing and changes in fire frequency and Study samples Wickens & Lowe 2008 PCK0 1 Australian Virtual Herbarium IBRA subregions eg. DAL02 State border VIB02 DAB0 1 NOK 0 2 NOK 0 1 VIB03 VIB01 N OVP03 CEK0 1 OVP0 1 OVP02 CEK0 3 OVP04 CEK0 2 DAL 0 1 DAL 0 2 TAN01 GSD0 1 Fig. 1. Recorded distribution of Adansonia gregorii taken from the Australian Virtual Herbarium (http://avh.ala.org.au/, accessed 17 April 2014) (triangles) and from Wickens and Lowe (2008) (squares) and localities of samples of A. gregorii examined in the present study (circles). Details of these samples are given in Appendix 1 (available as Supplementary Material to this paper). The distribution is overlaid on the subregions of the Interim Biogeographic Regionalisation of Australia (IBRA) (Australian Government Department of Sustainability 2012). 166 Australian Journal of Botany K. L. Bell et al. intensity, may be altering the distribution of the species. Macrogen (Seoul, Korea) using Big-Dye terminator chemistry However, these hypotheses remain untested. (Applied Biosystems, Foster City, CA, USA), and read on a Adansonia gregorii occurs in a wide range of habitats 3730 sequencer (Applied Biosystems). Trace files were (Wickens and Lowe 2008). The trees are often concentrated imported into Geneious (Biomatters, Auckland, New Zealand), along seasonal waterways and flood plains, leading Wickens trimmed, and forward and reverse sequences assembled into and Lowe (2008) to suggest that the presence of groundwater consensus sequences. is an important factor controlling the species’ distribution. Microsatellites were used for population genetic analysis. However, it does not grow in forests bordering permanent Primers for 18 microsatellite loci were initially developed for rivers, possibly because of poor competitive ability (Bowman A. digitata, and 12 of the 18 were found to amplify in A. gregorii 1997; Wickens and Lowe 2008). The broad habitat range of (Larsen et al. 2009). We screened these 12 loci in a subset of A. gregorii may reflect ecotypes within the species (Beard seven A. gregorii samples and selected six loci (Ad06, Ad08, 1967). The western populations of A. gregorii are a significant Ad13, Ad14, Ad15, and Ad18) that were found to be routinely component of the savanna vegetation in the Fitzroy River amplifiable and polymorphic in A. gregorii. Amplified loci were Basin. The species also occurs in the more mountainous sequenced to test for homology with the microsatellites amplified central Kimberley on drainage lines and in areas with more in A. digitata. Forward primers for the six microsatellite
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