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Recent Vicariance and the Origin of the Rare

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Recent Vicariance and the Origin of the Rare Molecular Ecology (2011) 20, 2901–2915 doi: 10.1111/j.1365-294X.2011.05151.x Recent vicariance and the origin of the rare, edaphically specialized Sandhills lily, Lilium pyrophilum (Liliaceae): evidence from phylogenetic and coalescent analyses NORMAN A. DOUGLAS,* WADE A. WALL,* QIU-YUN (JENNY) XIANG,* WILLIAM A. HOFFMANN,* THOMAS R. WENTWORTH,* JANET B. GRAY† and MATTHEW G. HOHMANN‡ *Department of Plant Biology, PO Box 7612, North Carolina State University, Raleigh, NC 27695, USA, †Directorate of Public Works, Endangered Species Branch, United States Army, Fort Bragg, NC 28310, USA, ‡US Army Corps of Engineers, Engineer Research and Development Center, PO Box 9005, Champaign, IL 618262, USA Abstract Establishing the phylogenetic and demographic history of rare plants improves our understanding of mechanisms that have led to their origin and can lead to valuable insights that inform conservation decisions. The Atlantic coastal plain of eastern North America harbours many rare and endemic species, yet their evolution is poorly understood. We investigate the rare Sandhills lily (Lilium pyrophilum), which is endemic to seepage slopes in a restricted area of the Atlantic coastal plain of eastern North America. Using phylogenetic evidence from chloroplast, nuclear internal transcribed spacer and two low-copy nuclear genes, we establish a close relationship between L. pyrophilum and the widespread Turk’s cap lily, L. superbum. Isolation-with-migration and coalescent simulation analyses suggest that (i) the divergence between these two species falls in the late Pleistocene or Holocene and almost certainly post-dates the establishment of the edaphic conditions to which L. pyrophilum is presently restricted, (ii) vicariance is responsible for the present range disjunction between the two species, and that subsequent gene flow has been asymmetrical and (iii) L. pyrophilum harbours substantial genetic diversity in spite of its present rarity. This system provides an example of the role of edaphic specialization and climate change in promoting diversification in the Atlantic coastal plain. Keywords: coalescence, divergence, edaphic, Lilium, Pleistocene, rarity Received 18 November 2010; revision received 28 April 2011; accepted 5 May 2011 species (Knowles 2009), have only rarely been applied Introduction to investigate the history of rare species (Raduski et al. Molecular studies of rare plant taxa usually aim to 2010; Whittall et al. 2010). quantify the level and patterns of genetic diversity in a Of the ‘seven forms of rarity’ (Rabinowitz 1981), the particular species (Karron 1987; Hamrick & Godt 1990; most extreme describes taxa that have a narrow geo- Ellstrand & Elam 1993; Gitzendanner & Soltis 2000). graphic range, require specific habitats and maintain Phylogeographic studies, on the other hand, often focus only small local populations. Many edaphic endemics on widespread species and try to discern continental- (plants restricted to soils with unusual physical or scale patterns (Taberlet et al. 1998; Brunsfeld et al. 2001; chemical properties) belong to this category. While the Soltis et al. 2006). However, the tools of phylogeogra- textbook examples of edaphic endemic plants are phy, particularly coalescent-based analyses that provide restricted to serpentine, various substrates support information about the age and historical demography of edaphic endemics, including guano, alkali, salt, and gypsum deposits, limestone, chalk, and granite out- Correspondence: Norman A. Douglas, Fax: (919) 515 3436; crops, oligotrophic bogs and deep porous sands (Orn- E-mail: [email protected] duff 1965; Axelrod 1972; Parsons 1976; Kruckeberg & Ó 2011 Blackwell Publishing Ltd 2902 N. A. DOUGLAS ET AL. Rabinowitz 1985; Kruckeberg 1986; Williamson & Baz- throughout the region) lies the Cretaceous Middendorf eer 1997). Many aspects of the origin of edaphic ende- formation, which is of deltaic origin and thus has more mic species are poorly understood (Rajakaruna 2004). abundant clays (Sohl & Owens 1991). At the interface For instance, such species often occur in close geo- between these (and similar formations in the Carolinas graphic proximity to their progenitor lineages (e.g. and southeastern Virginia) occur Sandhills seep and Baldwin 2005), yet it is not usually known whether or streamhead pocosin ecotone communities. When kept how strongly gene flow is interrupted. While taxa dis- open by frequent fires encroaching from the surround- playing edaphic endemic syndromes often show ing xeric pine savannas, these wetlands can support reduced genetic diversity compared with their close rel- extremely high local species richness, among the high- atives (Godt & Hamrick 1993; Baskauf et al. 1994; Ayres est values ever recorded in North America (>102 spe- & Ryan 1999; but see Raduski et al. 2010), this may cies per 1 ⁄ 100 ha, Schafale & Weakley 1990). The age of reflect genetic drift due to lower population sizes or the the formations implies that endemic species have poten- effects of selection. Strong selection imposed by edaphi- tially had a very long time to adapt to the unusual cally challenging soils could be sufficient to foster pop- edaphic conditions. ulation divergence (Nosil et al. 2009; Freeland et al. In this study, we consider the Sandhills lily, Lilium 2010). Some edaphic endemics may represent vicariant pyrophilum (Liliaceae), a striking endemic of the Sand- populations isolated in narrow parts of formerly wider hills in the Carolinas and southeastern Virginia. For- ranges and niches of their progenitors (e.g. Crawford mally described only recently (Skinner & Sorrie 2002), et al. 1985), which may themselves be able to grow on specimens of this species were previously identified in the unusual substrate without being restricted to it. herbaria as any of three similar species in the region Edaphic specialists (especially in bog and sand habi- (L. superbum, L. michauxii or L. iridollae) that share the tats, Sorrie & Weakley 2001) are an important compo- distinctive ‘Turk’s cap’ morphology, in which flowers nent of the endemic-rich flora of the coastal plain of are pendent with the tepals reflexed upward. Skinner & eastern North America. Few coastal plain endemics Sorrie (2002) identified three specific plant communities have been the subject of molecular analyses. Sand dune (Schafale & Weakley 1990; Sorrie et al. 2006) that sup- habitats in Florida apparently served as Pleistocene port L. pyrophilum, including Sandhills seep and refugia for the genera Dicerandra and Conradina streamhead pocosin ecotones. The third, small stream (Edwards et al. 2006; Oliveira et al. 2007), and in gen- swamps are affected by frequent flooding events in eral, Florida has been proposed as a major Pleistocene addition to seepage and rarely support L. pyrophilum refugium for many taxa in eastern North America (Sol- (Sorrie et al. 2006). tis et al. 2006). Yet, recent phylogeographic work indi- Lilium pyrophilum is a very rare species. There are cates that some coastal plain endemic species likely fewer than 75 historical and extant locations in North persisted in northerly latitudes throughout the Pleisto- and South Carolina, and Virginia (North Carolina Natu- cene. For instance, the Atlantic coastal plain endemic ral Heritage Program 2007), and between 2007 and Pyxie Moss, Pyxidanthera (Diapensiaceae), shows long- 2009, a survey of all known populations located term range stasis (Wall et al. 2010). <500 stems across 35 populations (W. Wall, unpub- The Fall-Line Sandhills of North and South Carolina lished data). Approximately half of the extant popula- (which occur at the western boundary of the coastal tions and a quarter of the individuals occur on Fort plain) provide one of the clearest examples of the Bragg Military Reservation in North Carolina, where edaphic contribution to the botanical diversity of the prescribed and ordnance-ignited fires maintain appro- Atlantic coastal plain. This region is comprised of roll- priate habitat. ing hills of open, fire-maintained longleaf pine (Pinus In describing L. pyrophilum (Skinner & Sorrie 2002), palustris) savanna dissected by numerous blackwater the authors outlined three phylogenetic hypotheses con- streams and wetlands, providing a diverse matrix of cerning the origin of the species. First, they speculated habitats that support at least eight endemic plants (and that L. pyrophilum may represent a peripheral isolate of numerous near-endemics, Sorrie & Weakley 2001). In the Turk’s cap lily, L. superbum, which it most resem- the core of the Sandhills region in southern North Caro- bles morphologically (albeit with significant differences, lina, the uppermost deposit is the Pinehurst formation, Skinner & Sorrie 2002). Lilium superbum is distributed which is characterized by loose coarse-grained sands throughout much of eastern North America (Fig. 1), found along ridgetops. This formation was deposited in and in contrast to the edaphically specialized L. pyro- a tidal environment (J. Nickerson, North Carolina Geo- philum, it is a generalist, occurring in rich woods and logical Survey, personal communication) and may date oligotrophic wetlands from high elevation to sea level. to the Eocene (Cabe et al. 1992). Below the Pinehurst Especially in northern parts of its range (e.g. the Pine formation (and exposed along drainages and slopes Barrens of New Jersey), it can be found in saturated Ó 2011 Blackwell Publishing Ltd ORIGIN OF LILIUM PYROPHILUM 2903 Fort Bragg Military Reservation 0 20 40 km L. iridollae L. michauxii 0
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