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Phylogeography of the World's Tallest Angiosperm, Eucalyptus Regnans

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Phylogeography of the World's Tallest Angiosperm, Eucalyptus Regnans Journal of Biogeography (J. Biogeogr.) (2010) 37, 179–192 ORIGINAL Phylogeography of the world’s tallest ARTICLE angiosperm, Eucalyptus regnans: evidence for multiple isolated Quaternary refugia Paul G. Nevill1,2,3*, Gerd Bossinger1 and Peter K. Ades4 1School of Forest and Ecosystem Science, ABSTRACT University of Melbourne and Cooperative Aim There is a need for more Southern Hemisphere phylogeography studies, Research Centre for Forestry, Creswick, Australia, 2Botanic Gardens and Parks particularly in Australia, where, unlike much of Europe and North America, ice Authority, Kings Park and Botanic Gardens, sheet cover was not extensive during the Last Glacial Maximum (LGM). This West Perth, Australia, 3School of Plant Biology, study examines the phylogeography of the south-east Australian montane tree The University of Western Australia, Nedlands, species Eucalyptus regnans. The work aimed to identify any major evolutionary Australia and 4School of Forest and Ecosystem divergences or disjunctions across the species’ range and to examine genetic Science, University of Melbourne and signatures of past range contraction and expansion events. Cooperative Research Centre for Forestry, Location South-eastern mainland Australia and the large island of Tasmania. Parkville, Australia Methods We determined the chloroplast DNA haplotypes of 410 E. regnans individuals (41 locations) based on five chloroplast microsatellites. Genetic structure was examined using analysis of molecular variance (AMOVA), and a statistical parsimony tree was constructed showing the number of nucleotide differences between haplotypes. Geographic structure in population genetic diversity was examined with the calculation of diversity parameters for the mainland and Tasmania, and for 10 regions. Regional analysis was conducted to test hypotheses that some areas within the species’ current distribution were refugia during the LGM and that other areas have been recolonized by E. regnans since the LGM. Results Among the 410 E. regnans individuals analysed, 31 haplotypes were identified. The statistical parsimony tree shows that haplotypes divided into two distinct groups corresponding to mainland Australia and Tasmania. The distribution of haplotypes across the range of E. regnans shows strong geographic patterns, with many populations and even certain regions in which a particular haplotype is fixed. Many locations had unique haplotypes, particularly those in East Gippsland in south-eastern mainland Australia, north-eastern Tasmania and south-eastern Tasmania. Higher haplotype diversity was found in putative refugia, and lower haplotype diversity in areas likely to have been recolonized since the LGM. Main conclusions The data are consistent with the long-term persistence of E. regnans in many regions and the recent recolonization of other regions, such as the Central Highlands of south-eastern mainland Australia. This suggests that, in spite of the narrow ecological tolerances of the species and the harsh environmental conditions during the LGM, E. regnans was able to persist locally or contracted to many near-coastal refugia, maintaining a diverse genetic *Correspondence: Paul G. Nevill, Botanic structure. Gardens and Parks Authority, Kings Park and Keywords Botanic Garden, West Perth, WA 6005, Australia. Chloroplast microsatellite, climate change, Eucalyptus, phylogeography, Pleis- E-mail: [email protected] tocene refugia, south-eastern Australia, Tasmania. ª 2009 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi 179 doi:10.1111/j.1365-2699.2009.02193.x P. G. Nevill et al. INTRODUCTION Climatic oscillations during the Quaternary have had a strong influence on species distributions and evolution (Hewitt, 1996). In south-eastern Australia, the Pleistocene climate fluctuated between cool-dry (glacial) and warm-wet (intergla- cial) weather conditions (Bowler, 1982; Frakes et al., 1987; Markgraf et al., 1995), with the Last Glacial Maximum (LGM) (maximum extent of ice sheets during the last glaciation) occurring between 23 and 16 ka (Barrows et al., 2004). Temperatures during glacial maxima were up to 6–6.5°C cooler than those experienced today (Colhoun et al., 1996), and rainfall, particularly in summer, was reduced (Hubbard, 1995). In contrast to the case in central and northern Europe and much of North America, glaciation in south-eastern Australia was not extensive, being confined to small areas in the Snowy Mountains region of continental Australia (Barrows et al., 2001) and to the Central Plateau of Tasmania (Colhoun et al., 1996; Duller & Augustinus, 1997), and, as a result, there was not the removal of all vegetation from large areas. In south-eastern Australia, the combination of aridity and lower temperatures had a much more important effect on species distributions than did glaciation (Kershaw & Nanson, 1993). Tree species are thought to have responded to changing climate by contracting to suitable refugia during the LGM and Figure 1 Current natural range of Eucalyptus regnans (indicated then re-colonizing the landscape when conditions became by grey shading) in south-eastern Australia and Tasmania and more favourable. Lowland species are thought to have the location of the 10 geographic regions used in the analyses contracted to coastal refugia or onto the exposed continental (Otway Ranges, Central Highlands, south Central Highlands, shelf, whereas montane species made elevational migrations or South Gippsland, East Gippsland, northern Tasmania, north- survived in suitable microsites (McKinnon et al., 2004). These eastern Tasmania, eastern Tasmania, south-eastern Tasmania and range contractions and recolonization events should have left central Tasmania) (map source Boland et al., 2006). genetic signatures in the genomes of these species. For example, the low genetic diversity found in tree species in areas of northern Europe recolonized since the LGM is thought Tasmania is similar and shows clear links. Natural vegeta- to have arisen from a series of bottlenecks associated with tion in low- to moderate-rainfall areas is typically eucalypt founder events (Hewitt, 1996), which results in only a subset of forest or woodland (10–30 m tall). In higher-rainfall areas and the diversity present in refugia being found in recolonized protected microsites in low- to moderate-rainfall areas, tall areas (Petit et al., 2003). It is generally thought that refugia are eucalypt forest (30–80 m), and, to a very limited extent, cool- indicated by the present-day derived populations containing temperate rain forest can be found. Alpine vegetation exists in high levels of diversity or low levels of diversity but unique south-eastern mainland Australia above 1800 m a.s.l., whereas divergent haplotypes. By studying these genetic signatures it in Tasmania it is above 1100 m a.s.l., owing to its more will be possible to gain a better understanding of how eucalypt southerly position and thus cooler climate. species survived and then flourished following such severe During the LGM, Tasmania and south-eastern mainland climatic changes. Australia were colder and generally more arid than at present. The area in this study is situated in south-eastern mainland On the mainland, pollen and charcoal records suggest that Australia and on the large island of Tasmania (320 km · much of the Victorian Central Highlands were treeless and 320 km) between the latitudes 37° and 43°38¢ S (Fig. 1). dominated by alpine vegetation. Eucalypts are thought to have Tasmania and the mainland are separated by the Bass Strait, persisted at low elevations in the south of the region, near sea which is currently 250 km wide but generally less than 100 m level (McKenzie, 1997, 2002). In the Otway Ranges region, deep. Since the early Miocene, Tasmania and the mainland fossil pollen records indicate that eucalypts persisted along have been repeatedly separated and linked by changes in sea with rain forest taxa (McKenzie & Kershaw, 1997, 2000, 2004). level (Baillie, 1989). A land-bridge joining South Gippsland, Pleistocene vegetation history in East Gippsland is less well Flinders Island and north-east Tasmania in the east and the known; however, a recently published study from the west of Otway Ranges, King Island and north-west Tasmania in the that region indicates that, as in the south Central Highlands, west existed as recently as 7 ka (Jackson, 1999). Consequently, eucalypts survived but were restricted to small areas of suitable the vegetation of south-eastern mainland Australia and habitat and were not widespread (Kershaw et al., 2007). 180 Journal of Biogeography 37, 179–192 ª 2009 Blackwell Publishing Ltd Phylogeography of Eucalyptus regnans Forests in south-eastern mainland Australia are thought to In this study we examine in detail the phylogeography of the have expanded from southern, near-sea-level refugia, with the montane Australian tree species Eucalyptus regnans F. Muell. major phase of expansion between 7 and 5 ka (McKenzie & Eucalyptus regnans is endemic to mountainous regions of Kershaw, 2000). In Tasmania, glaciation was extensive on the south-eastern Australia (Fig. 1) and is discontinuously dis- central plateau and the tree line was close to current sea level tributed in south-eastern, mainland Australia at elevations (Kirkpatrick & Fowler, 1998). Pollen records indicate that the between 200 and 1100 m a.s.l. on and south of the Great midlands were treeless, and, like the Central Highlands on the Dividing Range in the east and in the Otway Ranges in the mainland, dominated
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