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Conservation Genetics

, Volume 19, Issue 2, pp 365–381 | Cite as

Genetic differentiation and diversity of two sympatric subspecies of Castilleja affinis; a comparison between the endangered serpentine endemic (spp. neglecta) and its widespread congener (ssp. affinis)

  • Laney Widener
  • Jeremie B. Fant
Research Article

Abstract

Edaphic endemic species are considered high conservation priority, as they are a unique and critical component of the ecosystems and are often restricted to small fragmented habitats. Castilleja affinis ssp. neglecta is a serpentine endemic species, known from six sites within the San Francisco Bay Area and is the focus of active restoration efforts. It grows sympatrically with the subspecies, C. affinis ssp. affinis, which is more widespread but differs in floral color and soil preference. In this study, we used morphometric measurements (three bract, ten floral, and two leaf measurements) and microsatellite markers to determine (1) how the two subspecies differ, (2) if there is evidence of hybridization and (3) quantify the genetic structure of known populations of C. affinis ssp. neglecta. We found that all 15 morphological measurements differed significantly between the subspecies and neutral genetic markers show strong genetic differentiation. Overall we found C. affinis ssp. neglecta populations had similar levels of genetic diversity and genetic differentiation between populations but higher inbreeding than compared to its more common congener. Two populations of C. affinis ssp. neglecta showed lower genetic differentiation from the C. affinis ssp. affinis populations, with some individuals showing considerable overlap in genotypic diversity, hence we cannot rule out historic or low levels hybridization in those populations. Castilleja affinis ssp. neglecta is a federally endangered species that would benefit from restoration efforts that aims to maintain genetic diversity while minimizing inbreeding in reintroduction efforts.

Keywords

Castilleja affinis California Endangered Serpentine Endemic Congener 

Notes

Acknowledgements

This study would not be possible without the support from the Creekside Science, who provided the grounds for the study, financial support for the lab work, and hours organizing and collecting data in the field for the endangered C. affinis ssp. neglecta with us. We thank the California Native Plant Society for providing additional funding, knowledge, encouragement, and support of the project from inception to completion. For reviewing and providing suggestions for improving this manuscript, we want to thank the two anonymous reviewers, members of the Skogen-Fant lab and Andrea Kramer. We also are indebted to two very knowledgeable scientists who work with Castilleja for their time and energy: Mark Egger [UTW], who verified all of the field vouchers, and David Tank [U. Idaho], for advice on the study. We thank the Shaw family for their generous donation and continued support for Northwestern’s Plant Biology and Conservation Graduate Program.

Supplementary material

10592_2017_1009_MOESM1_ESM.xlsx (26 kb)
Supplementary material 1 (XLSX 25 KB)

References

  1. Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17(24):5177–5188PubMedCrossRefGoogle Scholar
  2. Alvarez N, Thiel-Egenter C, Tribsch A, Holderegger R, Manel S, Schönswetter P et al (2009) History or ecology? Substrate type as a major driver of spatial genetic structure in Alpine plants. Ecol Lett 12(7):632–640. doi: 10.1111/j.1461-0248.2009.01312.x PubMedCrossRefGoogle Scholar
  3. Amos W, Balmford A (2001) When does conservation genetics matter? Heredity 87:257–265PubMedCrossRefGoogle Scholar
  4. Anacker BL, Strauss SY (2014) The geography and ecology of plant speciation: range overlap and niche divergence in sister species. Proc R Soc B 281:20132980PubMedPubMedCentralCrossRefGoogle Scholar
  5. Anacker BL, Whittall JB, Goldberb EE, Harrison SP (2011) Origins and consequences of serpentine endemism in the California flora. Evolution 63:365–276. doi: 10.1111/j.1558-5646.2010.01114.x CrossRefGoogle Scholar
  6. Azalea Society of America, Inc (2007) http://azaleas.org/index.pl/rhsmacfan1.html
  7. Beardsley PM, Yen A, Olmstead RG (2003) AFLP phylogeny of Mimulus section Erythranthe and the evolution of hummingbird pollination. Evol Int J Org Evol 57(6):1397–1410CrossRefGoogle Scholar
  8. Breed MF, Ottewell KM, Gardner MG, Marklund MHK, Dormontt EE, Lowe AJ (2013) Mating patterns and pollinator mobility are critical traits in forest fragmentation genetics. Heredity 115:108–114PubMedPubMedCentralCrossRefGoogle Scholar
  9. Brooks TM, Mittermeier RA, Mittermeier CG, Da Fonseca GAB, Rylands AB, Konstant WR, Pilgrim P, Flick J, Oldfield S, Magin G, Hilton-Taylor C (2002) Habitat loss and extinction in the hotspots of biodiversity. Conserv Biol 16(4) 909–923CrossRefGoogle Scholar
  10. Brown AHD, Briggs JD (1991) Sampling strategies for genetic variation in ex situ collections of endangered plant species. In: Falk DA, Holsinger KE (eds) Genetics and coservation of rare plants. Oxford University Press, New York, pp 99–122Google Scholar
  11. Burlakova LE, Karatayev AY, Karatayev VA, May ME, Bennett DL, Cook MJ (2011) Endemic species: contribution to community uniqueness, effect of habitat alteration, and conservation priorities. Biol Conserv 144(1):155–165CrossRefGoogle Scholar
  12. Byers DL, Meagher TR (1997) A comparison of demographic characteristics in a rare and a common species of Eupatorium. Ecol Appl 7(2):519–530CrossRefGoogle Scholar
  13. Cacho NI, Strauss SY (2014) Occupation of bare habitats, an evolutionary precursor to soil speciation in plants. Proc Natl Acad Sci. 111(42):15132–15137PubMedPubMedCentralCrossRefGoogle Scholar
  14. California Natural Diversity Database (CNDDB) (2011) California Department of Fish and WildlifeGoogle Scholar
  15. Campbell DR, Bischoff M, Lord JM, Robertson AW (2010) Flower color influences insect visitation in alpine New Zealand. Ecology 91(9):2638–2649PubMedCrossRefGoogle Scholar
  16. Caplow F (2004) Reintroduction plan for golden paintbrush (Castilleja levisecta). In: Prepared for the US Fish and Wildlife Service Western Washington Fish and Wildlife Office. Washington Natural Heritage ProgramGoogle Scholar
  17. Chittka L, Waser NM (1997) Why red flowers are not invisible to bees. Israel J Plant Sci. doi: 10.1080/07929978.1997.10676682 Google Scholar
  18. Chuang T, Heckard L (1992) Nomenclatural changes of some Californian Castilleja (Scrophulariaceae). Novon 2:185–189CrossRefGoogle Scholar
  19. Clark LV, Jasieniuk M (2011) POLYSAT: an R package for polyploidy microsatellite analysis. Mol Ecol Resour 11:562–566PubMedCrossRefGoogle Scholar
  20. Clegg MT (1980) Measuring plant mating system. Bioscience 30(12):814–818CrossRefGoogle Scholar
  21. Crandall K, Bininda-Emonds OR, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15(7):290–295PubMedCrossRefGoogle Scholar
  22. Crawford KM, Whitney KD (2010) Population genetic diversity influences colonization success. Mol Ecol 19(6):1253–1263PubMedCrossRefGoogle Scholar
  23. Cronk Q, Ojeda I (2008) Bird-pollinated flowers in an evolutionary and molecular context. J Exp Bot 59(4):715–727PubMedCrossRefGoogle Scholar
  24. Crosswhite FS, Crosswhite CD (1970) Pollination of Castilleja sessiliflora in Southern Wisconsin. Bull Torrey Bot Club 97(2):100–105CrossRefGoogle Scholar
  25. Damschen EI, Harrison S, Going BM, Anacker BL (2011) Climate change and plant communities on unusual soils. In: Harrison SP, Rajakaruna N (eds) Serpentine: the evolution and ecology of a model system 359–381. University of California Press, BerkeleyGoogle Scholar
  26. De Mendiburu F (2009) Una herramienta de analisis estadistico para la investigacion agricola. Tesis. Universidad Nacional de Ingenieria (UNI-PERU)Google Scholar
  27. Dobson AP, Bradshaw AD, Baker AJM (1997) Hopes for the future: restoration ecology and conservation biology. Science 277(5325):515–522CrossRefGoogle Scholar
  28. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  29. Duffield WJ (1972) Pollination ecology of Castilleja in Mount Rainier National Park. Ohio J Sci 72(2):110–114Google Scholar
  30. Dufresne F, Stift M, Vergilino R, Mable BK (2014) Recent progress and challenges in population genetics of polyploid organisms: an overview of current state-of-the-art molecular and statistical tools. Mol Ecol 23(1):40–69PubMedCrossRefGoogle Scholar
  31. Duminil J, Fineschi, Silvia, Hampe, Arndt, Jordano, Pedro, Daniela, Vendramin S, Giovanni G, Petit, Rémy J (2007) Can population genetic structure be predicted from life-history traits? Am Nat 169:662–672PubMedGoogle Scholar
  32. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361. doi: 10.1007/s12686-011-9548-7 CrossRefGoogle Scholar
  33. Egger M (1994) New natural hybrid combinations and comments on the interpretation of hybrid populations in Castilleja (Scrophulariaceae). Phytologia 77(5):381–389Google Scholar
  34. Elam DR, David H, Wright, Goettle B (1998) Recovery plan for serpentine soil species of the San Francisco Bay area. US Fish and Wildlife reportGoogle Scholar
  35. Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242CrossRefGoogle Scholar
  36. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620PubMedCrossRefGoogle Scholar
  37. Fant JB, Weinberg-Wolf H, Tank DC, Skogen KA (2013a) Characterization of microsatellite loci in Castilleja sessiliflora and transferability to 24 Castilleja species. Appl Plant Sci 1(6):1200564CrossRefGoogle Scholar
  38. Fant JB, Kramer A, Sirkin E, Havens K (2013b) Genetics of reintroduced populations of the narrowly endemic thistle, Cirsium pitcheri (Asteraceae). Botany 91:301–308CrossRefGoogle Scholar
  39. Fant JB, Havens K, Keller JM, Radosavljevic A, Yates ED (2014) The influence of contemporary and historic landscape features on the genetic structure of the sand dune endemic, Cirsium pitcheri (Asteraceae). Heredity (Edinb) 112:519–530CrossRefGoogle Scholar
  40. Fenster CB, Dudash MR (1994) Genetic considerations in plant population conservation and restoration”. In: Bowles ML, Whelan C (eds) Restoration of endangered species: conceptual issues, planning and implementation. Cambridge University Press, Cambridge, pp 34–62CrossRefGoogle Scholar
  41. Fiedler PL (1987) Life history and population dynamics of rare and common mariposa lilies (Calochortus Pursh: Liliaceae). J Ecol 75(4):977–995CrossRefGoogle Scholar
  42. Frankham R (1998) Inbreeding and extinction_ island populations (PDF download available).pdf. Conserv Biol 12(3):665–675CrossRefGoogle Scholar
  43. Frankham R (2005) Genetics and extinction. Biol Conserv 126(2):131–140CrossRefGoogle Scholar
  44. Frankham R, Ballou JD, Elderidge M.D.B., Lacy RC, Ralls K, Dudash MR, Fenster CB (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475PubMedCrossRefGoogle Scholar
  45. Fréville H, Colas B, Ronfort J, Riba M, Oliyieri I (1998) Predicting endemism from population structure of a widespread species: case study in Centaurea maculosa Lam. (Asteraceae). Conserv Biol 12(6):1269–1278CrossRefGoogle Scholar
  46. Gibson N, Yates C, Byrne M, Langley M, Thavornkanlapachai R (2012) The importance of recruitment patterns versus reproductive output in the persistence of a short range endemic shrub in a highly fragmented landscape of south western Australia. Aust J Bot 60:643–649CrossRefGoogle Scholar
  47. Gitzendanner MA, Soltis P (2000) Patterns of generic variation in rare and widespread plant congeners. Am J Bot 87(6):783–792PubMedCrossRefGoogle Scholar
  48. Godt MJW, Caplow F, Hamrick JL. 2005. Allozyme diversity in the federally threatened golden paintbrush, Castilleja levisecta (Scrophulariaceae). Conserv Genet 6:87–99CrossRefGoogle Scholar
  49. Grant KA (1966) A hypothesis concerning the prevalence of red coloration in California hummingbird flowers. Am Nat 100(911):85–97CrossRefGoogle Scholar
  50. Grant V (1994) Historical development of ornithophily in the western North America flora. Proc Natl Acad Sci 901:10407–10411CrossRefGoogle Scholar
  51. Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc London 351:1291–1298. Retrieved from http://classic.rstb.royalsocietypublishing.org/content/351/1345/1291.short
  52. Hamrick JL, Linhart YB, Mitton JB (1979) Relationship between life history characteristics and electrophoretically detectable genetic variation in plants. Annu Rev Ecol Syst 10:173–200CrossRefGoogle Scholar
  53. Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  54. Harris JA, Hobbs RJ, Higgs E, Aronson J (2006) Ecological restoration and global climate change. Restor Ecol 14(2):170–176CrossRefGoogle Scholar
  55. Havens K, Vitt P, Still S, Kramer AT, Fant JB, Schatz K (2015) Seed sourcing for restoration in an era of climate change seed. Natural Areas Journal 35(1):122–133. doi: 10.3375/043.035.0116 CrossRefGoogle Scholar
  56. Heckard L (1968) Chromosome numbers and polyploidy in Castilleja (Scrophulariaceae). Brittonia 20:212–226CrossRefGoogle Scholar
  57. Helenurm K, West R, Burckhalter SJ (2005) Allozyme variation in the endangered insular endemic Castilleja grisea. Ann Bot (Lond) 95:1221–1227CrossRefGoogle Scholar
  58. Hersch EI, Roy BA (2007) Context-dependent pollinator behavior: An explanation for patterns of hybridization among three species of Indian paintbrush. Evol Int J Org Evol 91:111–124CrossRefGoogle Scholar
  59. Hersch-Green EI (2012) Polyploidy in Indian paintbrush (Castilleja; Orobanchaceae) species shapes but does not prevent gene flow across species boundaries. Am J Bot 99:1680–1690PubMedCrossRefGoogle Scholar
  60. Hersch-Green EI, Cronn R (2009) Tangled trios?: characterizing a hybrid zone in Castilleja (Orobanchaceae). Am J Bot 96:1519–1531PubMedCrossRefGoogle Scholar
  61. Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405(6789):907–913PubMedCrossRefGoogle Scholar
  62. Hickman JC (ed) (1992) The jepson manual. University of California Press, Berkeley, CAGoogle Scholar
  63. Holtsford TP, Ellstrand NC (1992) Genetic and environmental variation in floral traits affecting outcrossing rate in clarkia. Evol Int J Org Evol 46(1):216–225CrossRefGoogle Scholar
  64. Hu FS, Hampe A, Petit RJ (2009) Paleoecology meets genetics: deciphering past vegetational dynamics. Front Ecol Environ 7(7):371–379CrossRefGoogle Scholar
  65. Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18(3):147–155CrossRefGoogle Scholar
  66. Hufford KM, Krauss SL, Veneklaas EJ (2012) Inbreeding and outbreeding depression in Stylidium hispidum: implications for mixing seed sources for ecological restoration. Ecol Evol 2(9):2262–2273PubMedPubMedCentralCrossRefGoogle Scholar
  67. Hughes AR, Stachowicz JJ (2004) Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc Natl Acad Sci USA 101(24), 8998–9002PubMedPubMedCentralCrossRefGoogle Scholar
  68. Hughes M, Möller M, Bellstedt DU, Edwards TJ, Villiers M (2005) Refugia, dispersal, and divergence in a forest archipelago: a study of Streptocarpus in eastern South Africa. Mol Ecol 14:4415–4426PubMedCrossRefGoogle Scholar
  69. Ison JL, Wagenius S (2014) Both flowering time and spatial isolation affect reproduction in Echinacea angustifolia. J Ecol 102:920–929CrossRefGoogle Scholar
  70. Jepson Flora Project (eds) (2013) Jepson eFlora, http://ucjeps.berkeley.edu/IJM.html. Accessed on 13 Oct 2014
  71. Jiménez-Mejías P, Fernández-Mazuecos M, Amat ME, Vargas P (2015) Narrow endemics in European mountains: high genetic diversity within the monospecific genus Pseudomisopates (Plantaginaceae) despite isolation since the late Pleistocene. J Biogeogr 42:1455–1468CrossRefGoogle Scholar
  72. Jogesh T, Overson RP, Raguso RA, Krissa A (2017) Herbivory as an important selective force in the evolution of floral traits and pollinator shifts. AoB Plants ​9(1):plw088Google Scholar
  73. Karron JD (1987) A comparison of levels of genetic polymorphism and self-incompatibility in geographically restricted and widespread plant congeners. Evol Ecol 1: 47–58CrossRefGoogle Scholar
  74. Kay KM, Sargent RD (2009) The role of animal pollination in plant speciation: integrating ecology, geography, and genetics. Annu Rev Ecol Evol Syst 40(1):637–656CrossRefGoogle Scholar
  75. Kay KM, Ward KL, Watt LR, Schemske DW (2011) Plant speciation. In: Harrison SP, Rajakaruna N (eds) Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley, pp 71–95Google Scholar
  76. 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(1):109–121PubMedCrossRefGoogle Scholar
  77. Kruckeberg AR (1984) California serpentines: flora, vegetation, geology, soils, and management problems. University of California Press, Berkeley, p 180Google Scholar
  78. Laikre L, Allendorf FW, Aroner LC, Baker CS, Gregovich DP, Hansen MM et al (2010) Neglect of genetic diversity in implementation of the convention on biological diversity. Conserv Biol 24(1):86–88PubMedCrossRefGoogle Scholar
  79. Lavergne S, Thompson JD, Garnier E, Debussche M (2004) The biology and ecology of narrow endemic and widespread plants: a comparative study of trait variation in 20 congeneric pairs. Oikos 107(3):505–518CrossRefGoogle Scholar
  80. Lesica P, Yurkewycz R, Crone E (2006) Rare plants are common when you find them. Am J Bot 93:454–459PubMedCrossRefGoogle Scholar
  81. Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annu Rev Ecol Syst 15:65–95CrossRefGoogle Scholar
  82. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27(2):209–220PubMedGoogle Scholar
  83. Maschinski, Haskins KE (eds) (2012) Plant reintroduction in a changing climate: promises and perils. Island Press, Washington DCGoogle Scholar
  84. Maschinski J, Wright SJ, Koptur S, Pinto-Torres EC (2013) When is local the best paradigm? Breeding history influences conservation reintroduction survival and population trajectories in times of extreme climate events. Biol Conserv 159:277–284CrossRefGoogle Scholar
  85. Meirmans P (2013) GenoDive Version 2.0b23 Manual. Software for analysis of population genetic dataGoogle Scholar
  86. Meirmans PG, Hedrick PW (2011) Assessing population structure: F(ST) and related measures. Mol Ecol Resour 11(1):5–18PubMedCrossRefGoogle Scholar
  87. Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794CrossRefGoogle Scholar
  88. Meirmans PG, Van Tienderen PH (2012) The effects of inheritance in tetraploids on genetic diversity and population divergence. Heredity 110(2):131–137PubMedPubMedCentralCrossRefGoogle Scholar
  89. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858PubMedCrossRefGoogle Scholar
  90. Neale JR (2012) Genetic considerations in rare plant reintroduction: practical applications (or how are we doing?). In: Maschinksi J, Haskins KE (eds) Plant reintroduction in a changing climate. Island Press, Washington, pp 71–88CrossRefGoogle Scholar
  91. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  92. Niederer C, Weiss SB (2011) Research facilitating recovery of the endangered serpentine endemic Tiburon paintbrush (Castilleja affinis ssp. neglecta) at Coyote Ridge in southern Santa Clara County. Creekside Center for Earth Observation. Prepared for Central Valley Project Conservation ProgramGoogle Scholar
  93. Noss RF (1990) Indicators for monitoring biodiversity: a hierarchical approach. Conserv Biol 4(4):355–364CrossRefGoogle Scholar
  94. Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13(5):1143–1155PubMedCrossRefGoogle Scholar
  95. Oksanen FJ, Blanchet G, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2013) Vegan: community ecology package. R package version 2.0–10. http://CRAN.R-project.org/package=vegan
  96. Ownbey M (1959) Castilleja. In Hitchcock CL, Cronquist A, Ownbey M, Thompson J (eds) Vascular plants of the pacific northwest, vol 17, issue 4. University of Washington Press, Seattle, pp 295–326Google Scholar
  97. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539PubMedPubMedCentralCrossRefGoogle Scholar
  98. Pekkala N, Knott KE, Kotiaho JS, Nissinen K, Puurtinen M. 2012. The benefits of interpopulation hybridization diminish with increasing divergence of small populations. J Evol Biol. doi: 10.1111/j.1420-9101.2012.02594.x PubMedGoogle Scholar
  99. Pennell FW (1951) Scrophulariaceae. In: Abrams L (ed) Illustrated flora of the pacific states, vol 3. Stanford University Press, Stanford, pp 686–859Google Scholar
  100. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959PubMedPubMedCentralGoogle Scholar
  101. R Core Team (2014). R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, http://www.R-project.org/
  102. Rasband WS (2010) ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/, 1997–2012
  103. Raymond M, Rousset F (1995) An exact test for population differentiation. Evol Int J Org Evol 49(6):1280–1283CrossRefGoogle Scholar
  104. Revelle W (in preparation) An introduction to psychometric theory with applications in R. Springer at http://personality-project.org/r/book/
  105. Rieseberg LH (1995) The role of hybridization in evolution: old wine in new skins. Am J Bot 82(7):944–953CrossRefGoogle Scholar
  106. Ronfort J, Jenczewski E, Bataillon T, Rousset F (1998) Analysis of population structure in autotetraploid species. Genetics 150:921–930PubMedPubMedCentralGoogle Scholar
  107. Rosas-Guerrero V, Aguilar R, Martén-Rodríguez S, Ashworth L, Lopezaraiza-Mikel M, Bastida JM, Quesada M (2014) A quantitative review of pollination syndromes: do floral traits predict effective pollinators? Ecol Lett 17(3):388–400PubMedCrossRefGoogle Scholar
  108. Sambatti JBM, Rice KJ (2006) Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis). Evolution 60(4):696–710PubMedCrossRefGoogle Scholar
  109. Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16(May):393–430CrossRefGoogle Scholar
  110. Stebbins GL (1980) Rarity of plant species: a synthetic viewpoint. Rhodora 82(829):77–86Google Scholar
  111. Stebbins GL, Major J (1965) Endemism and speciation in the California flora. Ecol Monogr 35:1–35. doi: 10.2307/1942216 CrossRefGoogle Scholar
  112. Tank DC, Olmstead RG (2008) From annuals to perennials: phylogeny of subtribe Castillejinae (Orobanchaceae). Am J Bot 95:608–625PubMedCrossRefGoogle Scholar
  113. Tapper S-L, Byrne M, Yates CJ, Keppel G, Hopper SD, Van Niel K, Schut AGT, Mucina L, Wardell-Johnson GW (2014) Isolated with persistence or dynamically connected? Genetic patterns in a common granite outcrop endemic. Divers Distrib 20(9):987–1001CrossRefGoogle Scholar
  114. The Royal Horticultural Society (2007) Fan 1: yellow, yellow-orange, orange, orange-red, red groups, 5th edn. The Royal Horticultural Society, LondonGoogle Scholar
  115. Thiel-Egenter C, Gugerli F, hamricez N, Brodbeck S, Cieślak E, Colli L, Holderegger R (2009) Effects of species traits on the genetic diversity of high-mountain plants: a multi-species study across the Alps and the Carpathians. Global Ecol Biogeogr 18(1):78–87CrossRefGoogle Scholar
  116. Thompson JD (1999) Population differentiation in Mediterranean plants: insights into colonization history and the evolution and conservation of endemic species. Heredity 82(September 1998):229–236PubMedCrossRefGoogle Scholar
  117. Toon A, Cook LG, Crisp MD (2014) Evolutionary consequences of shifts to bird-pollination in the Australian pea-flowered legumes (Mirbelieae and Bossiaeeae). BMC Evol Biol 14(1):43PubMedPubMedCentralCrossRefGoogle Scholar
  118. USFWS (1995) ETWP; proposed endangered status for ten plants threatened status for two plants from serpentine habitats in the San Francisco Bay Region of California. Fed Reg 60:6671–6685Google Scholar
  119. Van Oosterhout C, Van Heuven MK, Brakefield PM (2004) On the neutrality of molecular genetic markers: pedigree analysis of genetic variation in fragmented populations. Mol Ecol 13(5):1025–1034. doi: 10.1111/j.1365-294X.2004.02114.x PubMedCrossRefGoogle Scholar
  120. Vrancky G, Jacquemyn H, Muys B, Honnay O (2012) Meta-analysis of susceptibility of woody plants to loss of genetic diversity through habitat fragmentation. Conserv Biol 26(2):228–237CrossRefGoogle Scholar
  121. Weeks AR, Sgro CM, Young AG, Frankham R, Mitchell NJ, Miller KA, Byrne M, Coates DJ, Eldridge MDB, Sunnucks P, Breed MF, James EA, Hoffman AA (2011) Assessing the benefits and risks of translocations in changing environments: a genetic perspective. Evol Appl 4(6):709–725PubMedPubMedCentralCrossRefGoogle Scholar
  122. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol Int J Org Evol 38:1358–1370Google Scholar
  123. Whitlock MC (2011) G’ST and D do not replace FST. Mol Ecol 20(6):1083–1091PubMedCrossRefGoogle Scholar
  124. Wolf A (2001) Conservation of endemic plants in serpentine landscapes. Biol Conserv 100:35–44CrossRefGoogle Scholar
  125. Wolf AT, Thorp R (2011) Plant-pollinator interactions in naturally fragmented habitats. In: Harrison SP, Rajakaruna N (eds) Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley, pp 359–381Google Scholar
  126. Yost JM, Barry T, Kay KM, Rajakaruna N (2012) Edaphic adaptation maintains the coexistence of two cryptic species on serpentine soils. Am J Bot 99(5):890–897. doi: 10.3732/ajb.1100521 PubMedCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Plant Science and ConservationChicago Botanic GardenGlencoeUSA
  2. 2.Plant Biology and ConservationNorthwestern UniversityEvanstonUSA
  3. 3.New England Wild Flower SocietyFraminghamUSA

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