Evidence of Population Bottleneck in Astragalus Michauxii (Fabaceae), a Narrow Endemic of the Southeastern United States

Conserv Genet DOI 10.1007/s10592-013-0527-2 RESEARCH ARTICLE Evidence of population bottleneck in Astragalus michauxii (Fabaceae), a narrow endemic of the southeastern United States Wade A. Wall • Norman A. Douglas • William A. Hoffmann • Thomas R. Wentworth • Janet B. Gray • Qiu-Yun Jenny Xiang • Brian K. Knaus • Matthew G. Hohmann Received: 7 January 2013 / Accepted: 26 August 2013 Ó Springer Science+Business Media Dordrecht (outside the USA) 2013 Abstract Genetic factors such as decreased genetic microsatellites and genotyped 355 individuals from 24 diversity and increased homozygosity can have detrimental populations. We characterized the population genetic effects on rare species, and may ultimately limit potential diversity and structure, tested for evidence of past bottle- adaptation and exacerbate population declines. The Gulf necks, and identified evidence of contemporary gene flow and Atlantic Coastal Plain physiographic region has the between populations. The mean ratios of the number of second highest level of endemism in the continental USA, alleles to the allelic range (M ratio) across loci for A. but habitat fragmentation and land use changes have michauxii populations were well below the threshold of resulted in catastrophic population declines for many spe- 0.68 identified as indicative of a past genetic bottleneck. cies. Astragalus michauxii (Fabaceae) is an herbaceous Genetic diversity estimates were similar across regions and plant endemic to the region that is considered vulnerable to populations, and comparable to other long-lived perennial extinction, with populations generally consisting of fewer species. Within-population genetic variation accounted for than 20 individuals. We developed eight polymorphic 92 % of the total genetic variation found in the species. Finally, there is evidence for contemporary gene flow among the populations in North Carolina. Although genetic Electronic supplementary material The online version of this factors can threaten rare species, maintaining habitats article (doi:10.1007/s10592-013-0527-2) contains supplementary through prescribed burning, in concert with other inter- material, which is available to authorized users. ventions such as population augmentation or (re)introduc- W. A. Wall (&) Á N. A. Douglas Á W. A. Hoffmann Á tion, are likely most critical to the long term survival of A. T. R. Wentworth Á Q.-Y. J. Xiang michauxii. Department of Plant Biology, North Carolina State University, Box 7612, Raleigh, NC 27695, USA Keywords Astragalus Á Bottleneck Á Endemism Á e-mail: [email protected] Genetic diversity Á Microsatellites Á Pinus palustris W. A. Wall Á M. G. Hohmann US Army Corps of Engineers, Engineer Research and Development Center, P. O. Box 9005, Champaign, IL 61826, Introduction USA N. A. Douglas Land use changes over the last 500 years have led to Department of Biology, Oberlin College & Conservatory, habitat loss and population isolation for many species, Science Center K107, 119 Woodland St., Oberlin, OH 44074- leading to a greater concern about the loss of biodiversity 1097, USA and its effects on the biosphere (Balmford and Bond 2005). J. B. Gray In the southeastern United States, many terrestrial and Endangered Species Branch, Fort Bragg, NC 28310, USA aquatic species are threatened with extinction (Dobson et al. 1997). Many of the rare plant species of the coastal B. K. Knaus Department of Botany and Plant Pathology, Oregon State plain are part of the longleaf pine (Pinus palustris Mill.) University, 2082 Cordley Hall, Corvallis, OR 97331, USA ecosystem, an assemblage of fire-dependent communities 123 Conserv Genet dominated by temperate savanna that covered roughly 37 may be relicts from past vegetation assemblages of Plio- million hectares from east Texas to Florida to southeastern cene or Pleistocene origin (Noss 2013). In South Carolina Virginia (Frost 1993). The longleaf pine ecosystem and Georgia, all known populations of A. michauxii exist in depends on frequent fires to maintain an open understory a highly fragmented landscape and are separated from the and facilitate longleaf pine seedling recruitment. Urbani- North Carolina populations by over 200 km. The average zation, fire suppression, and conversion to agriculture have population size is less than 20 individuals (Wall et al. fragmented the original longleaf pine ecosystem and 2012) and there is substantial risk that these small, isolated reduced it to 2 % of its former area (Frost 2006), resulting populations may be subject to reduced genetic diversity in population declines for many endemic species (Van Lear and the negative effects that ensue. et al. 2005). In this study, we investigated genetic diversity and Anthropogenic habitat fragmentation in the southeastern structure of A. michauxii populations across the range of United States has occurred against a background of past, the species using eight microsatellite loci. We estimated highly dynamic, climatically driven vegetation change the level of genetic variation within and among populations during the transition from the Pleistocene to the Holocene and identified the most likely number of genetic clusters (Webb III 1987; Williams et al. 2004). Thus, possible within A. michauxii. In addition, we searched for evidence explanations for the current habitat fragmentation of some of past genetic bottlenecks and contemporary gene flow. southeastern plant populations include, in the short term, We hypothesized that the small, isolated populations would changes in land use following European settlement and, in exhibit strong genetic differentiation between populations the long term, climatic changes that have occurred in the and low genetic diversity within populations, as well as past 20,000 years. Habitat fragmentation results in evidence of genetic bottlenecks because of recent land use increased genetic isolation and smaller plant populations changes following European settlement. By examining the (Young et al. 1996), and with increasing time since frag- genetic variation of A. michauxii within the context of past mentation, genetic differentiation between populations climatic change and land use history, this study provides generally increases and genetic diversity within popula- useful information for any future conservation or restora- tions decreases (Young et al. 1996). If populations have tion efforts of this species and other rare plants of the Fall- been isolated since the early Holocene, it is assumed that line Sandhills. genetic differentiation between populations would be greater relative to that due to population isolation since European settlement. Methods Extreme reductions in population size can lead to genetic bottlenecks, which are of conservation concern Species because of the increased risk of extinction (Frankham 2005). Across taxa, it has been observed that genetic Astragalus michauxii is an herbaceous, long-lived legume diversity is lower in threatened species (Spielman et al. that is generally found in upland longleaf pine habitat in 2004) and in species with restricted ranges (Hamrick and what has been characterized as the pine/scrub oak sand- Godt 1989) relative to common, widespread species. This hill community (Schafale and Weakley 1990). The larg- suggests that genetic factors increase the likelihood of est extant populations are found in the loamy soil variant extinction of species by reducing fitness of individuals of this community type that generally have higher pH within small populations (Leimu et al. 2006) and restrict and more nutrients. These areas are known locally as evolutionary potential (Franklin 1980). Thus, assessing and ‘‘pea swales’’ or ‘‘bean dips’’ because of their high maintaining the genetic variation found within rare species diversity of Fabaceae species (James 2000). The species is of concern for both their short- and long-term viability is largely restricted to the Fall-line Sandhills of North and is one of the cornerstones of conservation genetics Carolina, South Carolina, Georgia, and Alabama (USA) (Frankham et al. 2010). (Sorrie and Weakley 2001; Peet 2006; NatureServe Astragalus michauxii (Kuntze) F.J. Herm. is a rare 2012), an extensive ancient dune system located at the legume endemic to the Fall-line Sandhills region of North boundary between the Coastal Plain and the Piedmont Carolina, South Carolina, and Georgia (USA). Only a few physiographic regions that is characterized by a rolling species of Astragalus are represented east of the Missis- topography with excessively-well drained, sandy soils in sippi. Most members of this genus occur in Asia, western the interfluvial areas. North America, and South America, with the North Astragalus michauxii is one of the earliest flowering American species belonging to the aneuploid Neo-Astrag- legumes in the Fall-line Sandhills, flowering in early May alus clade, which began to diversify 4.4 Ma (Scherson and producing mature fruits by early July (Radford et al. et al. 2008). The disjunct species in eastern North America 1968). The species is most likely an obligate outcrosser, 123 Conserv Genet and flowers are pollinated by a variety of flying insects. 1000 spectrophotometer (Thermo Scientific, Wilmington, Fruit set is commonly quite low relative to the number of DE, USA). Libraries were then pooled and paired-end flowers; however the reasons for this have not been iden- sequenced on one lane of an Illumina Genome Analyzer II. tified (e.g. an overabundance of self pollen, pollinator The resulting microreads were then sorted by the 4

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