Environmental Requirements Trump Genetic Factors in Explaining Narrow Endemism in Two Imperiled Florida Sunflowers
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Conserv Genet (2015) 16:1277–1293 DOI 10.1007/s10592-015-0739-8 RESEARCH ARTICLE Environmental requirements trump genetic factors in explaining narrow endemism in two imperiled Florida sunflowers 1 1 1 2 Chase M. Mason • Caitlin D. A. Ishibashi • Ashley M. Rea • Jennifer R. Mandel • 1 1 John M. Burke • Lisa A. Donovan Received: 24 October 2014 / Accepted: 5 June 2015 / Published online: 10 June 2015 Ó Springer Science+Business Media Dordrecht 2015 Abstract The mechanisms generating narrow endemism Keywords Climate change Á Genetic diversity Á have long been of interest to biologists, with a variety of Helianthus Á Inbreeding Á Niche modeling Á Phoebanthus underlying causes proposed. This study investigates the origins of narrow endemism of two imperiled Florida endemics, Helianthus carnosus and Phoebanthus tenuifolius, in relation to Introduction a widespread sympatric close relative, Helianthus radula,as well as other members of the genus Helianthus.Usinga Narrow endemics are taxa restricted to small geographic combination of population genetics and environmental niche areas. These species are often of conservation interest due modeling, this study compares evidence in support of potential to their relative rarity in comparison to widespread species mechanisms underlying the origin of narrow endemism, and the inherent risk of extinction associated with occu- including environmental specialization versus inbreeding, loss pying only small geographic areas (Kruckeberg and Rabi- of diversity, or other predominantly genetic factors. The two nowitz 1985). The origins of narrow endemism are not well narrow endemics were found to be comparable in genetic understood, though several underlying causes have been diversity to H. radula as well as other widespread Helianthus proposed. These include range contractions in formerly species, with little to no evidence of inbreeding. Environmental widespread species, often due to habitat loss, as well as niche modeling indicates that distributions of both narrow speciation events into isolated or specialized habitats endemics are strongly related to temperature and precipitation (Kruckeberg and Rabinowitz 1985). These two opposing patterns, and that both endemics are threatened with severe origins are directly related to species’ environmental reductions in habitat suitability under projected climate change. requirements, with the latter likely resulting in more nar- Evidence indicates that genetic factors likely are not the cause row requirements than the former. Regardless of origins, of narrow endemism in these species, suggesting that these narrow endemics have often been hypothesized to be species are likely ecological specialists and thus historical genetically depauperate (Stebbins 1942; Hamrick and Godt narrow endemics. This makes both species vulnerable to cli- 1996), with such species having reduced genetic diversity mate change, and of immediate conservation concern. either as a result of adaptation to narrow ecological con- ditions or increased inbreeding of clustered populations in a small geographic area (Kruckeberg and Rabinowitz Electronic supplementary material The online version of this 1985). In this way, reduced genetic variation may represent article (doi:10.1007/s10592-015-0739-8) contains supplementary material, which is available to authorized users. either a contributing factor to narrow endemism or a con- sequence thereof. Understanding the relative importance of & Chase M. Mason narrow environmental requirements and genetic variation [email protected] in determining narrow endemic status is key to our 1 Department of Plant Biology, University of Georgia, 2502 understanding of this biological phenomenon and the Miller Plant Sciences, Athens, GA 30602, USA management of threatened species. 2 Department of Biological Sciences, University of Memphis, The southeastern United States is a hotspot of plant Memphis, TN 38152, USA endemism, with multiple geographic centers with high 123 1278 Conserv Genet (2015) 16:1277–1293 densities of narrowly endemic species (Estill and Cruzan networks from which it produces flowering stems with 2001; Sorrie and Weakley 2001). The southeast has been a narrow leaves (Fig. 1). P. tenuifolius is winter-deciduous, focal region for the study of the origins of narrow ende- senescing all aboveground tissues and re-sprouting in the mism, and in particular the potential role of glacial refugia spring, reaching a height of around 40–100 cm and flow- in generating the patterns of species distributions seen ering throughout the summer (Schilling 2006c). The today (Soltis et al. 2006; Avise 2000). In addition, the study majority of the range of P. tenuifolius is made up of various of endemics in relation to their widespread close relatives state and federal conservation lands, including the Apa- has been highlighted as the preferred method for under- lachicola National Forest, Tate’s Hell State Forest, St. standing differences between species due to range size, as Mark’s National Wildlife Refuge, and a variety of smaller opposed to broad comparisons of rare and widespread preserves, wildlife and water management areas, and con- species that confound a variety of factors (Gitzendanner servation easements. P. tenuifolius is a state-listed threat- and Soltis 2000). The detailed study of southeastern ened species (Florida Administrative Code, Rule 5B- endemic plant species in relation to widespread relatives is 40.0055). a valuable avenue to understanding the origins of narrow By contrast to these two narrow endemics, Helianthus endemism, and we explore this avenue here using three radula (Torr. & A. Gray) (the rayless sunflower) is a southeastern sunflower species. perennial basal rosette species that is both widespread in Helianthus carnosus (Small) (the lakeside sunflower) is distribution and common within its range, ranging from a perennial basal rosette species native to five counties in South Carolina to Louisiana and far south into peninsular northeastern peninsular Florida, with the majority of the Florida (Fig. 1). It is thought that H. radula has historically range located east of the St. Johns River (Fig. 1). This occupied this widespread distribution throughout the species occurs in open wet meadows and sandy wet flat- southeastern coastal plain (Heiser et al. 1969). Like H. woods, as well as sandy wet roadside ditches which pro- carnosus, this species forms near-succulent leaves from vide analogous conditions as availability of the former two crown buds, maintains an aboveground rosette year-round, habitats has declined under the expansion of agriculture and sends up erect nearly-leafless stems upon which soli- and development in the region over the past half-century. tary flower heads are borne (Schilling 2006b). H. radula This shift in habitat occupancy has resulted in H. carnosus differs markedly, however, in leaf morphology and floral populations being subjected to regular mowing as part of anatomy, with obtuse or orbicular leaves covered in rough roadside maintenance, which may act to reduce growth and trichomes and flower heads completely lacking ray florets seed set in an already slow-growing species. This species (Fig. 1; Heiser et al. 1969). H. radula occupies a variety of forms linear, glabrous, near-succulent leaves from crown habitats, including the longleaf pine savanna, sandhill, and buds, maintaining an aboveground rosette year-round coastal scrub habitats of P. tenuifolius as well as the wet (Heiser et al. 1969). During the growing season, H. car- flatwoods and open roadside habitats of H. carnosus.In nosus typically produces one to three erect nearly-leafless fact, H. radula occurs in sympatry with both endemic stems approximately 10–60 cm tall upon which solitary species, even co-occurring in intermixed populations, flower heads are borne (Fig. 1; Schilling 2006a). This though it tends to flower much later in autumn than the growth form makes H. carnosus particularly susceptible to other species (September–November), except perhaps for mowing, as removal of the tall flowering stems at any point mowing-induced late flowering populations of H. carnosus during the months-long period between their initial elon- (Heiser et al. 1969; Schilling 2006b). gation and final seed maturation will prevent seed set. These three species are closely related, with Helianthus While primarily flowering in late summer (June–Septem- and Phoebanthus well supported as sister genera (Schilling ber), there is evidence that the effect of mowing has 2001; Schilling and Panero 2002; Mandel et al. 2014), and resulted in shifts in flowering time much later in the year, recent phylogenetic data support H. carnosus and H. radula with populations now flowering over a broader period as likely sister species (Stephens et al. 2015). All three between June and December (Heiser et al. 1969; C. Mason, species are sporophytically self-incompatible, with gravity- personal observation). H. carnosus is a state-listed endan- dispersed seeds. This might make it potentially difficult for gered species (Florida Administrative Code, Rule 5B- these species to colonize new locations and expand their 40.0055). ranges. As H. carnosus and P. tenuifolius were not Phoebanthus tenuifolius (S.F. Blake) (the pineland false described until 1902 and 1916 (Schilling 2006a; Schilling sunflower) is an erect rhizomatous perennial species native 2006c), it is unknown whether they historically occupied to five counties in the Florida panhandle, in and around the larger ranges before widespread deforestation