Conservation Genetics

, Volume 20, Issue 5, pp 1149–1161 | Cite as

Genetic diversity and population structure in Cary’s Beardtongue Penstemon caryi (Plantaginaceae), a rare plant endemic to the eastern Rocky Mountains of Wyoming and Montana

  • Benjamin W. StoneEmail author
  • Alexander Ward
  • Max Farenwald
  • Andrew W. Lutz
  • Andrea D. Wolfe
Research Article


Penstemon caryi is a narrow-range endemic angiosperm found primarily on sparsely vegetated limestone outcrops in the Bighorn and Pryor Mountains of north-central Wyoming and south-central Montana. A former candidate for listing under the Endangered Species Act, and currently a species of concern in these states, P. caryi is potentially threatened by habitat loss due to encroaching anthropogenic activities, such as limestone quarrying and road construction. In an effort to assess the capacity of P. caryi to withstand habitat loss and degradation, we used simple sequence repeats (SSRs) and amplified fragment length polymorphism (AFLP) markers to examine genetic diversity and differentiation of P. caryi populations from the Pryor Mountains of Montana and the southern Bighorn Mountains of Wyoming. Our analyses revealed overall moderate to high levels of genetic diversity in P. caryi, but with relatively lower levels of diversity in populations from the Pryor Mountains. There are fewer known individuals of Penstemon caryi in Montana, and because the examined populations from Montana exhibited less genetic diversity than those from Wyoming, populations from Montana may face an increased risk of population decline and extirpation. Both the AFLP and SSR data sets found population structure between different regions (Montana vs. Wyoming), while AFLP markers identified further subdivision between Wyoming populations. Despite moderate to high levels of genetic diversity, P. caryi is still a species at risk due to impending environmental stresses such as global climate change and human encroachment, which may be especially troublesome given its narrow distribution and the specificity of its habitat preferences.


SSR AFLP Penstemon Bighorn Mountains Rare angiosperm 



This research was funded by NSF DEB 1455399. We thank Laura Kubatko, Paul Blischak, Rosa Rodriguez-Peña, Megan Smith, Mary Sagatelova, Lydia Mihaly, and two anonymous reviewers for helpful comments on the manuscript. We thank Rosa Rodriguez-Peña, Emiko Waight, and Gabi Zacarías-Correa for assistance with specimen collections.

Supplementary material

10592_2019_1204_MOESM1_ESM.docx (12 kb)
Supplementary material 1 (DOCX 92 kb)
10592_2019_1204_MOESM2_ESM.docx (186 kb)
Supplementary material 2 (DOCX 182 kb)


  1. Alexander JM, Chalmandrer L, Lenoir J, Burgess TI, Essl F, Haider S, Kueffer C, McDougall K, Milbau A, Nuñez MA, Pauchard A, Rabitsch W, Rew LJ, Sanders NJ, Pellissier L (2018) Lags in the response of mountain plant communities to climate change. Glob Change Biol 24:563–579. CrossRefGoogle Scholar
  2. Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Biol Lett 15:365–377. CrossRefGoogle Scholar
  3. Boakes EH, Isaac NJB, Fuller RA, Mace GM, McGowan PJK (2019) Examining the relationship between local extinction risk and position in range. Conserv Biol 32:229–239. CrossRefGoogle Scholar
  4. Brown JL, Weber JJ, Alvarado-Serrano DF, Hickerson MJ, Franks SJ, Carnaval AC (2016) Predicting the genetic consequences of future climate change: the power of coupling spatial demography, the coalescent, and historical landscape changes. Am J Bot 103:153–163. CrossRefPubMedGoogle Scholar
  5. Brzyski JR, Cullet TM (2011) Genetic variation and clonal structure of the rare, riparian shrub Spiraea virginiana (Rosaceae). Conserv Genet 12:1323–1332. CrossRefGoogle Scholar
  6. Butcher PA, Bradbury D, Krauss SL (2011) Limited pollen-mediated dispersal and partial self-incompatibility in the rare ironstone endemic Tetratheca paynterae subsp. Paynterae increase the risks associated with habitat loss. Conserv Genet 12:1603–1618. CrossRefGoogle Scholar
  7. Campbell D, Duchesne P, Bernatchez L (2003) AFLP utility for population assignment studies: analytical investigation and empirical comparison with microsatellites. Mol Ecol 12:1979–1991. CrossRefPubMedGoogle Scholar
  8. Chakraborty R, Jin L (1992) Heterozygote deficiency, population substructure and their implications in DNA fingerprinting. Hum Genet 88:267–272CrossRefPubMedGoogle Scholar
  9. Chapuis M, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631. CrossRefPubMedGoogle Scholar
  10. Chybicki IJ, Burczyk J (2009) Simultaneous estimation of null alleles and inbreeding coefficients. J Hered 100:106–113. CrossRefPubMedGoogle Scholar
  11. Chybicki IJ, Burczyk J (2011) Increased inbreeding and strong kinship structure in Taxus baccata estimated from both AFLP and SSR data. Heredity 107:589–600. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedPubMedCentralGoogle Scholar
  13. Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc B 39:1–38Google Scholar
  14. Di Rienzo A, Peterson AC, Garzat JC et al (1994) Mutational processes of simple-sequence repeat loci in human populations. PNAS 91:3166–3170. CrossRefPubMedGoogle Scholar
  15. Dostálek T, Münzbergová Z, Plačková I (2014) High genetic diversity in isolated populations of Thesium ebracteatum at the edge of its distribution range. Conserv Genet 15:75–86. CrossRefGoogle Scholar
  16. Duggan JM, Eichelberger BA, Ma S, Lawler JJ, Ziv G (2015) Informing management of rare species with an approach combining scenario modeling and spatially explicit risk assessment. Ecosyst Health Sustain 1:22. CrossRefGoogle Scholar
  17. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. CrossRefGoogle Scholar
  18. Eckert CG, Samis KE, Lougheed C (2008) Genetic variation across species’ geographic ranges: the central-marginal hypothesis and beyond. Mol Ecol 17:1170–1188. CrossRefPubMedGoogle Scholar
  19. Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242CrossRefGoogle Scholar
  20. Elsen PR, Tingley MW (2015) Global mountain topography and the fate of montane species under climate change. Nat Clim Change 5:772–776. CrossRefGoogle Scholar
  21. Elsen PR, Monahan WB, Merenlender AM (2018) Global patterns of protection of elevational gradients in mountain ranges. PNAS 115:6004–6009. CrossRefPubMedGoogle Scholar
  22. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Fertig W (2002) Status of Cary beardtongue (Penstemon caryi) in Wyoming. Prepared for the Bureau of Land Management Wyoming State Office and Wyoming Natural Diversity DatabaseGoogle Scholar
  26. Forrest A, Escudero M, Heuertz M et al (2017) Testing the hypothesis of low genetic diversity and population structure in narrow endemic species: the endangered Antirrhinum charidemi (Plantaginaceae). Bot J Linn Soc 183:260–270CrossRefGoogle Scholar
  27. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140. CrossRefGoogle Scholar
  28. Frankham R (2010) Where are we in conservation genetics and where do we need to go? Conserv Genet 11:661–663. CrossRefGoogle Scholar
  29. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  30. Frei ES, Scheepens JF, Stöcklin J (2012) High genetic differentiation in populations of the rare alpine plant species Campanula thyrsoides on a small mountain. Alp Bot 122:23–34. CrossRefGoogle Scholar
  31. Gargano D, Pellegrino G, Bernardo L (2015) Genetic and fitness consequences of interpopulation mating in Dianthus guliae Janke: conservation implications for severely depleted and isolated plant populations. Conserv Genet 16:1127–1138. CrossRefGoogle Scholar
  32. Gathmann A, Tscharntke T (2002) Foraging ranges of solitary bees. J Anim Ecol 71:757–764. CrossRefGoogle Scholar
  33. Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178. CrossRefPubMedGoogle Scholar
  34. Gigant RL, De Bruyn AD, Church B, Humeau L, Gauvin-Bialecki A, Pailler T, Grisoni M, Besse P (2014) Active sexual reproduction but no sign of genetic diversity in range-edge populations of Vanilla roscheri Rchb. f. (Orchidaceae) in South Africa. Conserv Genet 15:1403–1415. CrossRefGoogle Scholar
  35. Gitzendanner MA, Soltis PS (2000) Patterns of genetic variation in rare and widespread plant congeners. Am J Bot 87:783–792. CrossRefPubMedGoogle Scholar
  36. Gong W, Lei Gu, Zhang D (2010) Low genetic diversity and high genetic divergence caused by inbreeding and geographical isolation in the populations of endangered species Loropetalum subcordatum (Hamamelidaceae) endemic to China. Conserv Genet 11:2281–2288. CrossRefGoogle Scholar
  37. Hamilton JA, Miller JM (2016) Adaptive introgression as a resource for management and genetic conservation in a changing climate. Conserv Biol 30:33–41. CrossRefPubMedGoogle Scholar
  38. Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467. CrossRefPubMedGoogle Scholar
  39. Hamrick JL (2004) Response of forest trees to global environmental changes. For Ecol Manag 197:323–335. CrossRefGoogle Scholar
  40. Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc Lond B 351:1291–1298CrossRefGoogle Scholar
  41. Hannah L, Flint L, Syphard AD, Moritz MA, Buckley LB, McCullough IM (2014) Fine-grain modeling of species’ response to climate change: holdouts, stepping-stones, and microrefugia. Trends Ecol Evol 29:390–397. CrossRefPubMedGoogle Scholar
  42. Harrison S, Damschen E, Going BM (2009) Climate gradients, climate change, and special edaphic floras. Northeast Nat 16:121–130. CrossRefGoogle Scholar
  43. Harrison S, Damschen E, Fernandez-Going B, Eskelinen A, Copeland S (2015) Plant communities on infertile soils are less sensitive to climate change. Ann Bot 116:1017–1022. CrossRefPubMedGoogle Scholar
  44. Hedrick P (1999) Highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318CrossRefPubMedGoogle Scholar
  45. Heidel B, Handley J (2004) Penstemon caryi Pennell (Cary’s beardtongue): a technical conservation assessment. Prepared for the USDA Forest Service, Rocky Mountain RegionGoogle Scholar
  46. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. CrossRefPubMedGoogle Scholar
  47. Jump AS, Peñuelas J (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett 8:1010–1020. CrossRefGoogle Scholar
  48. Kimura M, Ohta T (1978) Stepwise mutation model and distribution of allelic frequencies in a finite population. PNAS 75:2868–2872CrossRefPubMedGoogle Scholar
  49. Kitchen SG, Meyer SE (1991) Seed germination of intermountain Penstemons as influenced by stratification and GA3 treatments. J Environ Hortic 9:51–56Google Scholar
  50. Kothera L, Richards CM, Carney SE (2007) Genetic diversity and structure in the rare Colorado endemic plant Physaria bellii Mulligan (Brassicaceae). Conserv Genet 8:1043–1050. CrossRefGoogle Scholar
  51. Kramer AT, Fant JB (2007) Isolation and characterization of microsatellite loci in Penstemon rostriflorus (Plantaginaceae) and cross-species amplification. Mol Ecol Notes 7:998–1001. CrossRefGoogle Scholar
  52. Kramer AT, Fant JB, Ashley MV (2011) Influences of landscape and pollinators on population genetic structure: examples from three Penstemon (Plantaginaceae) species in the Great Basin. Am J Bot 98:109–121. CrossRefPubMedGoogle Scholar
  53. La Sorte FA, Jetz W (2010) Projected range contractions of montane biodiversity under global warming. Proc R Soc B 277:3401–3410. CrossRefPubMedGoogle Scholar
  54. Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952. CrossRefGoogle Scholar
  55. Lindgren DT, Schaaf DM (2004) Influence of seed stratification and seed age on emergence of Penstemon. HortScience 39:1385–1386CrossRefGoogle Scholar
  56. Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  57. Lutz AW (2001) Patterns in genetic diversity in Penstemon caryi Pennel. (Scrophulariaceae s.l.), an endemic to limestone substrates. M.Sc. thesis, Ohio State University, Columbus, USAGoogle Scholar
  58. Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622–629. CrossRefPubMedGoogle Scholar
  59. Mace GM, Collar NJ, Gaston KJ, Hilton-Taylor C, Akçakaya HR, Leader-Williams N, Milner-Guilland EJ, Stuart SN (2008) Quantification of extinction risk: IUCN’s system for classifying threatened species. Conserv Biol 22:1424–1442. CrossRefPubMedGoogle Scholar
  60. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  61. Maynard-Smith J, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genet Res 23:23–35. CrossRefGoogle Scholar
  62. McCain CM, Colwell RK (2011) Assessing the threat to montane biodiversity from discordant shifts in temperature and precipitation in a changing climate. Ecol Lett 14:1236–1245. CrossRefPubMedGoogle Scholar
  63. Meyer SE, Kitchen SG, Carlson SL (1995) Seed germination timing patterns in intermountain Penstemon (Scrophulariaceae). Am J Bot 82:377–389CrossRefGoogle Scholar
  64. NatureServe (2019) NatureServe Explorer: an online encyclopedia of life (web application). Version 7.1. NatureServe, Arlington, Virginia. Accessed 28 Jan 2019
  65. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefPubMedGoogle Scholar
  66. Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155. CrossRefPubMedGoogle Scholar
  67. Oleksa A, Chybicki IJ, Gawroński R, Svensson GP, Burczyk J (2013) Isolation by distance in saproxylic beetles may increase with niche specialization. J Insect Conserv 17:219–233. CrossRefGoogle Scholar
  68. Pacifici M et al (2015) Assessing species vulnerability to climate change. Nat Clim Change 5:215–225. CrossRefGoogle Scholar
  69. Pauls S, Nowak C, Bálint M, Pfenninger M (2013) The impact of global climate change on genetic diversity within populations and species. Mol Ecol 22:925–946. CrossRefPubMedGoogle Scholar
  70. Paun O, Schönswetter P (2012) Amplified fragment length polymorphism: an invaluable fingerprinting technique for genomic, transcriptomic, and epigenetic studies. Methods Mol Biol 862:75–87. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. CrossRefGoogle Scholar
  72. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  73. Prentice H, Malm JU, Mateu-Andrés I, Segarra-Moragues JG (2003) Allozyme and chloroplast DNA variation in island and mainland populations of the rare Spanish endemic, Silene hifacensis (Caryophyllaceae). Conserv Genet 4:543–555CrossRefGoogle Scholar
  74. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. CrossRefPubMedPubMedCentralGoogle Scholar
  75. Rau P (1929) The biology and behavior of mining bees, Anthophora abrupta and Entechnia taurea. Psyche 36:155–181CrossRefGoogle Scholar
  76. Reisch C, Bernhardt-Römermann M (2014) The impact of study design and life history traits on genetic variation of plants determined with AFLPs. Plant Ecol 215:1493–1511. CrossRefGoogle Scholar
  77. Rodríguez-Peña RA, Johnson RL, Johnson LA, Anderson CD, Ricks NJ, Farley KM, Robbins MD, Wolfe AD, Stevens MR (2018) Investigating the genetic diversity and differentiation patterns in the Penstemon scariosus species complex under different sample sizes using AFLPs and SSRs. Conserv Genet 19:1335–1348. CrossRefGoogle Scholar
  78. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. CrossRefGoogle Scholar
  79. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedPubMedCentralGoogle Scholar
  80. Severns PM, Liston A, Wilson MV (2011) Habitat fragmentation, genetic diversity, and inbreeding depression in a threatened grassland legume: is genetic rescue necessary? Conserv Genet 12:881–893. CrossRefGoogle Scholar
  81. Shapcott A, Hutton I, Baker WJ, Auld TD (2012) Conservation genetics and ecology of an endemic montane palm on Lord Howe Island and its potential for resilience. Conserv Genet 13:257–270. CrossRefGoogle Scholar
  82. Skrede I, Borgen L, Brochmann C (2009) Genetic structuring in three closely related circumpolar plant species: AFLP versus microsatellite markers and high-arctic versus arctic–alpine distributions. Heredity 102:293–302. CrossRefPubMedGoogle Scholar
  83. Song Z, Zhang M, Li F et al (2016) Genome scans for divergent selection in natural populations of the widespread hardwood species Eucalyptus grandis (Myrtaceae) using microsatellites. Sci Rep 6:34941. CrossRefPubMedPubMedCentralGoogle Scholar
  84. Stebbins GL (1942) The genetic approach to problems of rare and endemic species. Madroño 60:302–319CrossRefGoogle Scholar
  85. Stone JL, Crystal PA, Devlin EE, Downer RHL, Cameron DS (2012) Highest genetic diversity at the northern range limit of the rare orchid Isotria medeoloides. Heredity 109:215–221. CrossRefPubMedPubMedCentralGoogle Scholar
  86. Tepedino V, Griswold JE, Freilich JE, Shephard P (2011) Specialist and generalist bee visitors of an endemic beardtongue (Penstemon caryi: Plantaginaceae) of the Big Horn Mountains, Wyoming. West North Am Nat 71:523–528CrossRefGoogle Scholar
  87. Thomas CD, Cameron A, Green RE et al (2004) Extinction risk from climate change. Nature 427:145–148CrossRefPubMedPubMedCentralGoogle Scholar
  88. Trivedi M, Berry PM, Morecroft MD, Dawson TP (2008) Spatial scale affects bioclimate model projections of climate change impacts on mountain plants. Glob Change Biol 14:1089–1103. CrossRefGoogle Scholar
  89. USFWS (United States Fish and Wildlife Service) (1993) Endangered and threatened wildlife and plants; review of plant taxa for listing as endangered or threatened species. Fed Reg 58:51144–51180Google Scholar
  90. Van der Merwe M, Spain CS, Rossetto M (2010) Enhancing the survival and expansion potential of a founder population through clonality. New Phytol 188:868–878. CrossRefPubMedGoogle Scholar
  91. Vekemans X, Beauwens T, Lemaire M, Roldan-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151CrossRefPubMedGoogle Scholar
  92. von Kohn C, Conrad K, Kramer M, Pooler M (2018) Genetic diversity of Magnolia ashei characterized by SSR markers. Conserv Genet 19:923–936. CrossRefGoogle Scholar
  93. Wahlund S (1928) Zusammensetzung von Populationen und Korrelationserscheinungen vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas 11:65–106CrossRefGoogle Scholar
  94. Wall WA, Douglas NA, Hoffmann WA, Wentworth TR, Gray JB, Xiang QYJ, Knaus BK, Hohmann MG (2014) Evidence of population bottleneck in Astragalus michauxii (Fabaceae), a narrow endemic of the southeastern United States. Conserv Genet 15:153–164. CrossRefGoogle Scholar
  95. Wessinger CA, Freeman CC, Mort ME et al (2016) Multiplexed shotgun genotyping resolves species relationships within the North American genus. Am J Bot 103:912–922. CrossRefPubMedGoogle Scholar
  96. Wolfe AD (2005) ISSR techniques for evolutionary biology. Methods Enzymol 395:134–144. CrossRefPubMedGoogle Scholar
  97. Wolfe AD, Randle CP, Datwyler SL et al (2006) Phylogeny, taxonomic affinities, and biogeography of Penstemon (Plantaginaceae) based on ITS and cpDNA sequence data. Am J Bot 93:1699–1713CrossRefPubMedGoogle Scholar
  98. Wolfe AD, McMullen-Sibul A, Tepedino VJ et al (2014) Conservation genetics and breeding system of Penstemon debilis (Plantaginaceae), a rare beardtongue endemic to oil shale talus in western Colorado, USA. J Syst Evol 52:598–611. CrossRefGoogle Scholar
  99. Wolfe AD, Necamp T, Fassnacht S et al (2016) Population genetics of Penstemon albomarginatus (Plantaginaceae), a rare Mojave Desert species of conservation concern. Conserv Genet 17:1245–1255. CrossRefGoogle Scholar
  100. Zurbuchen A, Landert L, Klaiber J et al (2010) Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biol Conserv 143:669–676. CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Evolution, Ecology, and Organismal BiologyThe Ohio State UniversityColumbusUSA
  2. 2.School of MedicineWashington UniversitySt. LouisUSA

Personalised recommendations