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Population Isolation Results in Unexpectedly High Differentiation in Carolina Hemlock (Tsuga Caroliniana), an Imperiled Southern Appalachian Endemic Conifer

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Population Isolation Results in Unexpectedly High Differentiation in Carolina Hemlock (Tsuga Caroliniana), an Imperiled Southern Appalachian Endemic Conifer Tree Genetics & Genomes (2017) 13:105 DOI 10.1007/s11295-017-1189-x ORIGINAL ARTICLE Population isolation results in unexpectedly high differentiation in Carolina hemlock (Tsuga caroliniana), an imperiled southern Appalachian endemic conifer Kevin M. Potter1 & Angelia Rose Campbell2 & Sedley A. Josserand3 & C. Dana Nelson3,4 & Robert M. Jetton5 Received: 16 December 2016 /Revised: 14 August 2017 /Accepted: 10 September 2017 # US Government (outside the USA) 2017 Abstract Carolina hemlock (Tsuga caroliniana Engelm.) is a range-wide sampling of the species. Data from 12 polymor- rare conifer species that exists in small, isolated populations phic nuclear microsatellite loci were collected and analyzed within a limited area of the Southern Appalachian Mountains for these samples. The results show that populations of of the USA. As such, it represents an opportunity to assess Carolina hemlock are extremely inbred (FIS =0.713)andsur- whether population size and isolation can affect the genetic prisingly highly differentiated from each other (FST =0.473) diversity and differentiation of a species capable of long- with little gene flow (Nm = 0.740). Additionally, most popu- distance gene flow via wind-dispersed pollen and seed. This lations contained at least one unique allele. This level of dif- information is particularly important in a gene conservation ferentiation is unprecedented for a North American conifer context, given that Carolina hemlock is experiencing mortality species. Numerous genetic clusters were inferred using two throughout its range as a result of infestation by hemlock different clustering approaches. The results clearly demon- wooly adelgid (Adelges tsugae Annand), an exotic insect. In strate that, existing as a limited number of small and isolated this study, 439 Carolina hemlock trees from 29 areas (ana- populations, Carolina hemlock has insufficient gene flow to lyzed as populations) were sampled, representing an extensive avoid widespread genetic drift and inbreeding, despite having the capacity to disperse pollen and seed relatively long dis- Communicated by S. C. González-Martínez tances by wind. These results have important conservation Electronic supplementary material The online version of this article implications for this imperiled species. (https://doi.org/10.1007/s11295-017-1189-x) contains supplementary material, which is available to authorized users. Keywords Disjunct populations . Gene conservation . Inbreeding . Microsatellite . Population isolation . Rare * Kevin M. Potter species [email protected] 1 Department of Forestry and Environmental Resources, North Introduction Carolina State University, 3041 Cornwallis Road, Research Triangle Park, Raleigh, NC 27709, USA Carolina hemlock (Tsuga caroliniana Engelm.) is a rare coni- 2 Department of Forestry and Environmental Resources, North fer with a limited geographic range within the Appalachian Carolina State University, Campus Box 8008, Raleigh, NC 27695-8008, USA mountains of the USA. It occurs in an area of approximately 465 km by 165 km in North Carolina, South Carolina, 3 Southern Institute of Forest Genetics, USDA Forest Service, Southern Research Station, 23332 Success Road, Tennessee, Virginia, and Georgia. Carolina hemlock stands Saucier, MS 39574, USA tend to be small (area and numbers of trees) and isolated 4 Forest Health Research and Education Center, University of (separated by 2 to 20 km), often occurring on exposed rocky Kentucky, Lexington, KY 40546, USA outcrops at elevations between 600 and 1500 m (Jetton et al. 5 Camcore, Department of Forestry and Environmental Resources, 2008a; Humphrey 1989). This is true even in the core of the North Carolina State University, Campus Box 8008, range (Fig. 1), where populations are small and discrete rather Raleigh, NC 27695-8008, USA than continuously distributed across the landscape, as well as 105 Page 2 of 20 Tree Genetics & Genomes (2017) 13:105 Fig. 1 Sampled populations of Carolina hemlock (Tsuga caroliniana). See Table 1 for population information. Blue populations (squares) are those for which collections of seed for gene conservation have been conducted. Seed had not been collected from red populations (circles) as of summer 2015 in a handful of more isolated populations that are peripheral to genetic variability within species and populations (Hamrick the center of the species distribution. et al. 1992; Hamrick and Godt 1996), but low differentiation Because Carolina hemlock clearly exists as a set of popu- among populations. Wind, in particular, is expected to be an lations that are both isolated and limited in size, we might effective pollen dispersal mechanism (Govindaraju 1988). For expect that the species would bear the signature of small- example, another conifer endemic to the Southern population processes such as inbreeding and genetic drift Appalachian region, Fraser fir (Abies fraseri (Pursh.) Poir), (Young et al. 1996), including low within-population genetic also exists in a limited number of isolated populations but variation and high between-population differentiation (Willi has been found to have relatively little differentiation among et al. 2006). This pattern might be particularly evident in pop- populations, possibly as a result of frequent long-distance pol- ulations that are peripheral to the core of the species distribu- len dispersal (Potter et al. 2008). tion, where neutral marker studies have, on average, found a Patterns of genetic variation, and their causes, have impor- decline in diversity and an increase in differentiation in plants tant implications for the genetic conservation of Carolina (Eckert et al. 2008). In fact, genetic diversity analyses of tree hemlock, which is a slow-growing, stress-tolerant, and late- species have found this to be the case across several continents successional species that often occurs in pure stands (Rentch (e.g., Kitamura et al. 2015; Mattioni et al. 2017;Pandeyand et al. 2000;Jettonetal.2008a). Like its eastern North America Rajora 2012). On the other hand, Carolina hemlock is a coni- congener, eastern hemlock (T. canadensis (L.) Carr.), it is fer with both pollen and seeds that are dispersed by wind under severe threat from the hemlock wooly adelgid (Godman and Lancaster 1990; Coladonato 1993). Species (Adelges tsugae Annand) (HWA), an invasive pest introduced with effective long-distance dispersal of pollen and seeds are from Japan. Once infested with HWA, which feed at the base able to achieve high gene flow and, as a result, often have high of hemlock needles regardless of a tree’s age and produce two Tree Genetics & Genomes (2017) 13:105 Page 3 of 20 105 clonally replicated generations per year, Carolina hemlocks isolated from each other, we hypothesize that little gene flow often die in as little as 4 years, though some trees have sur- occurs among them and, as a result, they are highly differen- vived infestation for more than 10 years (Havill et al. 2011). tiated, with levels of differentiation associated with distance Conditions that place stress on the trees, such as drought and among populations. We further hypothesize that populations extreme temperatures, can make them more vulnerable to disjunct from the core of the species range possess particularly HWA infestation and death (Quimby 1996), and it is possible low levels of genetic variation and high levels of differentia- that future climate changes may interact with and exacerbate tion compared to more centrally located populations. the impacts of HWA (Lemieux et al. 2011). Individual To test these hypotheses, we used highly polymorphic mi- Carolina hemlock trees may be less susceptible to HWA than crosatellite markers developed for Carolina hemlock the more widespread eastern hemlock (Jetton et al. 2008b), but (Josserand et al. 2008) to assess genetic variation and genetic the species as a whole may be at greater risk due to its rarity structure across the range of the species. Specifically, we used and limited range (Havill et al. 2011). In fact, Carolina hem- 12 nuclear microsatellite markers to genotype 439 trees from lock is ranked as Near Threatened on the IUCN Red List 29 populations of Carolina hemlock to (1) assess the relation- (Farjon 2013). The loss of both hemlock species is expected ship between population isolation and genetic diversity and to have numerous ecosystem impacts, including potentially differentiation, (2) evaluate genetic variation in peripheral dis- drastic changes to forest community structure, understory junct versus core range populations; and (3) compare genetic composition, nutrient cycling, soil pH, hydrologic processes, variation between populations that have and have not yet been microclimate, and wildlife assemblages (Orwig and Foster the focus of gene conservation seed collections. 1998; Jenkins et al. 1999; Brooks 2001; Kizlinski et al. 2002; Ford and Vose 2007; Allen et al. 2009; Yorks et al. 2000;Quimby1996). Materials and methods As a result of these concerns, ex situ gene conservation of hemlock genetic resources has been the focus of a collabora- Sample collection and DNA extraction tive effort between the US Department of Agriculture (USDA) Forest Service and Camcore, an international tree breeding Twenty-nine populations of Carolina hemlock were sampled and conservation program in the Department of Forestry and throughout the geographic range of the species (Fig. 1 and Environmental Resources at North Carolina State University. Table 1). This included a population located at Ritchie This project
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