Skip to main content

Advertisement

Log in

Habitat fragmentation, genetic diversity, and inbreeding depression in a threatened grassland legume: is genetic rescue necessary?

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Kincaid’s lupine (Lupinus oreganus), a threatened perennial legume of western Oregon grasslands, is composed of small, fragmented populations that have consistently low natural seed set, suggesting they may have accumulated high enough levels of genetic load to be candidates for genetic rescue. We used simple sequence repeat (SSR) loci, both nuclear DNA and chloroplast DNA, to screen populations throughout the species’ range for evidence of severe inbreeding and recent genetic bottlenecks due to habitat fragmentation. After genotyping about 40% of the known populations, only one of 24 populations had strong statistical evidence for a recent genetic bottleneck (H e > H eq). Both mean nSSR fixation coefficients and genetic diversity did not statistically differ between very small, small, medium, and large lupine population size classes. Within population chloroplast DNA haplotype number was high for an animal pollinated species, ≈4.2 haplotypes/population, and within population haplotype diversity was also relatively evenly distributed. Within population patterns of nSSR and cpSSR genetic diversity suggest that genetic diversity has not been lost over the last century of habitat fragmentation. With genet lifespan thought to exceed 100 years, overlap of several to many generations, and substantial reductions in seed set from inbreeding depression that shifts cohort composition towards those generated by outcrossing events, Kincaid’s lupine is likely maintain the currently high levels of within population genetic diversity. The case of Kincaid’s lupine provides an example of how the assumptions of severe inbreeding depression with small population size and habitat fragmentation can be inaccurate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ågren J (1996) Population size, pollinator limitation, and seed set in the self-incompatible herb Lythrum salicaria. Ecology 77:1779–1790

    Article  Google Scholar 

  • 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 17:5177–5188

    Article  PubMed  Google Scholar 

  • Arnaud-Haond S, Belkhir K (2007) GENCLONE 1.0: a new program to analyse genetics data on clonal organisms. Mol Ecol Notes 7:15–17

    Article  CAS  Google Scholar 

  • Arnaud-Haond S, Duarte CM, Alberto F, Serrão EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16:5115–5139

    Article  PubMed  CAS  Google Scholar 

  • Arnold MC, Hodges SA (1995) Are natural hybrids fit or unfit relative to their parents? Trends Ecol Evol 10:67–71

    Article  PubMed  CAS  Google Scholar 

  • Barrett SCH, Charlesworth D (1991) Effects of change in the level of inbreeding on the genetic load. Nature 352:522–524

    Article  PubMed  CAS  Google Scholar 

  • Broadhurst LM, Lowe A, Coates DJ, Cunningham SA, McDonald M, Vesk PA, Yates C (2008) Seed supply for broadscale restoration: maximizing evolutionary potential. Evol Appl 1:587–597

    Google Scholar 

  • Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography: effect of immigration and extinction. Ecology 58:445–449

    Article  Google Scholar 

  • Brown BJ, Mitchell RJ (2001) Competition for pollination: effects of pollen of an invasive plant on seed set of a native congener. Oecologia 129:43–49

    Article  Google Scholar 

  • Buza L, Young A, Thrall P (2000) Genetic erosion, inbreeding and reduced fitness in fragmented populations of the tetraploid pea Swainsona recta. Biol Conserv 93:177–186

    Article  Google Scholar 

  • Byrne M, MacDonald B, Coates D (1999) Divergence in the chloroplast genome and nuclear rDNA of the rare western Australian plant Lambertia orbifolia Gardner (Proteaceae). Mol Ecol 8:1789–1796

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth D (2003) Effects of inbreeding on the genetic diversity of populations. Philos Trans Biol Sci 358:1051–1070

    Article  CAS  Google Scholar 

  • Charlesworth B, Charlesworth D (1999) The genetic basis of inbreeding depression. Genet Res 74:329–340

    Article  PubMed  CAS  Google Scholar 

  • Citerne HL (2005) A primer set for specific amplification of two CYCLOIDEA-like genes in the genistoid clade of Leguminosae subfam. Papilionideae. Edingburgh J Bot 62:119–126

    Article  Google Scholar 

  • Citerne HL, Luo D, Pennington RT, Coen E, Cronk QCB (2003) A phylogenomic investigation of CYCLOIDEA like TCP genes in the Leguminosae. Plant Phys 131:1042–1053

    Article  CAS  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • Cozzolino S, Noce ME, Musacchio A, Widmer A (2003) Variation at a chloroplast minisatellite locus reveals the signature of habitat fragmentation and genetic bottlenecks in the rare orchid Anacamptis palustris (Orchidaceae). Am J Bot 90:1681–1687

    Article  PubMed  Google Scholar 

  • Drummond CS, Hamilton MB (2005) Isolation and characterization of nuclear microsatellite loci in Lupinus group Microcarpi (Leguminosae). Mol Ecol Notes 5:510–513

    Article  CAS  Google Scholar 

  • Ellis JR, Paghley CH, Burke JM, McCauley DE (2006) High genetic diversity in a rare and endangered sunflower as compared to a common congener. Mol Ecol 15:2345–2355

    Article  PubMed  CAS  Google Scholar 

  • Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242

    Article  Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci 97:7043–7050

    Article  PubMed  CAS  Google Scholar 

  • Field DL, Ayre DJ, Whelan RJ, Young AG (2008) Relative frequency of sympatric species influences rates of interspecific hybridization, seed production and seedling performance in the uncommon Eucalyptus aggregata. J Ecol 96:1198–1210

    Article  Google Scholar 

  • Fischer M, Matthies D (1997) Mating structure and inbreeding and outbreeding depression in the rare plant Gentianella germanica (Gentianaceae). Am J Bot 84:1685–1692

    Article  PubMed  CAS  Google Scholar 

  • Harder LD (1990) Behavioral responses by bumble bees to variation in pollen availability. Oecologia 85:41–47

    Article  Google Scholar 

  • Haynes J, Mesler M (1984) Pollen foraging by bumblebees: foraging patterns and efficiency on Lupinus polyphyllus. Oecologia 61:249–253

    Article  Google Scholar 

  • Hedrick PW (1994) Purging inbreeding depression and the probability of extinction: full sib mating. Heredity 73:363–372

    Article  PubMed  Google Scholar 

  • Hickman JC (ed) (1996) The Jepson manual: higher plants of California. University of California Press. Berkeley, California, USA

    Google Scholar 

  • Holmes GD, James EA, Hoffmann AA (2008) Limitations to reproductive output and genetic rescue in populations of the rare shrub Grevillea repens (Proteaceae). Ann Bot 102:1031–1041

    Article  PubMed  CAS  Google Scholar 

  • Honjo M, Ueno S, Tsumura Y, Washitani I, Ohsawa R (2004) Phylogeographic study based on intraspecific sequence variation of chloroplast DNA for the conservation of genetic diversity in the Japanese endangered species Primula sieboldii. Biol Conserv 120:211–220

    Article  Google Scholar 

  • Honnay O, Jacquemyn H (2007) Susceptibility of common and rare plant species to the genetic consequences of habitat fragmentation. Conserv Biol 21:823–831

    Article  PubMed  Google Scholar 

  • Hughes C, Eastwood R (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc Natl Acad Sci 103:10334–10339

    Article  PubMed  CAS  Google Scholar 

  • Husband BC, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70

    Article  Google Scholar 

  • Jaquiéry J, Guillaume F, Perrin N (2009) Predicting the deleterious effects of mutation load in fragmented populations. Conserv Biol 23:207–218

    Article  PubMed  Google Scholar 

  • Jennerston O (1988) Pollination in Dianthus deltoides (Caryophyllaceae): effects of habitat fragmentation on visitation and seed set. Conserv Biol 2:359–366

    Article  Google Scholar 

  • Juncosa AM, Webster BD (1989) Pollination in Lupinus nanus subsp. latifolius (Leguminosea). Am J Bot 76:59–66

    Article  Google Scholar 

  • Karoly K (1994) Inbreeding effects on mating system traits for two species of Lupinus (Leguminosae). Am J Bot 81:1538–1544

    Article  Google Scholar 

  • Kashi Y, King DG (2006) Simple sequence repeats as advantageous mutators in evolution. Trends Genet 22:253–259

    Article  PubMed  CAS  Google Scholar 

  • Kaye TN (1999) Obligate insect pollination of a rare plant: Lupinus sulphureus ssp. kincaidii. Northwest Sci 73:50–52

    Google Scholar 

  • Kaye TN, Kuykendall K (2001) Effects of scarification, cold stratification, and source population on germination of Lupinus sulphureus ssp. kincaidii. Seed Sci Technol 29:663–668

    Google Scholar 

  • Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112

    Article  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Keller M, Kollmann J, Edwards PJ (2000) Genetic introgression from distant provenances reduces fitness in local weed populations. J Appl Ecol 37:647–659

    Article  Google Scholar 

  • Kéry M, Matthies D, Spillmann HH (2000) Reduced fecundity and offspring performance in small populations of the declining grassland plants Primula veris and Gentiana lutea. J Ecol 88:17–30

    Article  Google Scholar 

  • Kittleson PM, Maron JL (2000) Outcrossing rates and inbreeding depression in the perennial yellow bush lupine, Lupinus arboreus (Fabaceae). Am J Bot 87:652–660

    Article  Google Scholar 

  • Lande R (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophies. Am Nat 142:911–927

    Article  Google Scholar 

  • Leimu R, Matikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952

    Article  Google Scholar 

  • Levin DA (2002) The role of chromosomal change in plant evolution. Oxford University Press, New York

    Google Scholar 

  • Lewis PO, Zaykin D (2002) Genetic Data Analysis: computer program for the analysis of allelic data, version 1.1

  • Lewis GM, Schrire B, Mackinder B, Lock M (2005) Legumes of the world. Royal Botanic Gardends, Kew, UK

    Google Scholar 

  • Li Y, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: a genomic distribution, putative function and mutational mechanisms: a review. Mol Ecol 11:2453–2465

    Article  PubMed  CAS  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Heredity 89:238–247

    Article  CAS  Google Scholar 

  • Lynch M, Conery J, Bürger R (1995) Mutation accumulation and the extinction of small populations. Am Nat 146:489–518

    Article  Google Scholar 

  • Melbourne BA, Hastings A (2008) Extinction risk depends strongly on factors contributing to stochasticity. Nature 454:100–103

    Article  PubMed  CAS  Google Scholar 

  • Michaels HJ, Shi XJ, Mitchell RJ (2008) Effects of population size on performance and inbreeding depression in Lupinus perennis. Oecologia 154:651–661

    Article  PubMed  CAS  Google Scholar 

  • Montalvo AM, Ellstrand NC (2001) Nonlocal transplantation and outbreeding depression in the subshrub Lotus scoparius (Fabaeceae). Am J Bot 88:258–269

    Article  PubMed  CAS  Google Scholar 

  • Newman D, Tallmon DA (2001) Experimental evidence for the beneficial fitness effects of gene flow in recently isolated populations. Conserv Biol 15:1054–1063

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Gilmore S, Keys W, Morgante M, Rafalski A (1998) Cross-species amplification of soybean (Glycine max) simple sequence repeats (SSRs) within the genus and other legume genera: implications for the transferability of SSRs in plants. Mol Biol Evol 15:1275–1287

    PubMed  CAS  Google Scholar 

  • Petit C, Bretagnolle F, Felber F (1999) Evolutionary consequences of diploid-polyploid hybrid zones in wild species. Trends Ecol Evol 14:306–311

    Article  PubMed  Google Scholar 

  • Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701

    Article  PubMed  CAS  Google Scholar 

  • Pickup M, Young AG (2008) Population size, self-incompatibility and genetic rescue in diploid and tetraploid races of Rutidosis leptorrhynchoides (Asteraceae). Heredity 100:268–274

    Article  PubMed  CAS  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Genetics 90:502–503

    Google Scholar 

  • Prentice HC, 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 hifarensis (Caryophyllaceae). Conserv Genet 4:543–555

    Article  CAS  Google Scholar 

  • Rasner CA, Yeh P, Essert LS, Hunt KE, Woodruff DS, Price TD (2004) Genetic and morphological evolution following a founder event in the dark-eyed junco, Junco hyemalis thurberi. Mol Ecol 13:671–681

    Article  PubMed  CAS  Google Scholar 

  • Ree RH, Citerne HL, Lavin M, Cronk QCB (2004) Heterogenous selection on LEGCYC paralogs in relation to flower morphology and phylogeny of Lupinus (Leguminosae). Mol Biol Evol 21:321–331

    Article  PubMed  CAS  Google Scholar 

  • Richards CM (2000) Inbreeding depression and genetic rescue in a plant metapopulation. Am Nat 155:383–394

    Article  PubMed  Google Scholar 

  • Schemske DW, Husband BC, Ruckelshaus MH, Goodwillie C, Parker IM, Bishop JG (1994) Evaluating approaches to the conservation of rare and endangered plants. Ecology 75:584–606

    Article  Google Scholar 

  • Schlötterer C (2004) The evolution of nuclear markers—just a matter of fashion? Nat Rev Genet 5:63–69

    Article  PubMed  Google Scholar 

  • Severns P (2003a) Inbreeding and small population size reduce seed set in a threatened and fragmented plant species, Lupinus sulphureus ssp. kincaidii (Fabaceae). Biol Conserv 110:221–229

    Article  Google Scholar 

  • Severns PM (2003b) Propagation of a long-lived and threatened prairie plant, Lupinus sulphureus ssp. kincaidii. Restor Ecol 11:334–342

    Article  Google Scholar 

  • Severns PM (2004) Creating bare ground increases presence of native pollinators in Kincaid’s lupine seeding plots. Ecol Restor 22:234–235

    Google Scholar 

  • Severns PM (2008) Seedling population size and microhabitat association in Lupinus oreganus A. Heller var. kincaidii C.P. Smith (Fabaceae), a threatened plant of western Oregon grasslands. Native Plants J 9:358–365

    Article  Google Scholar 

  • Severns PM (2009a) Conservation genetics of Kincaid’s lupine: a threatened plant of western Oregon and southwest Washington grasslands. PhD Thesis, Oregon State University, Corvallis, OR, USA

  • Severns PM (2009b) Patterns of genetic diversity in Douglas County populations of Kincaid’s lupine (Lupinus oreganus var kincaidii = Lupinus sulphureus ssp. kincaidii). Report to USDI Bureau of Land Management, Roseburg District, Oregon. 19 pp

  • Severns PM (2009c) Patterns of genetic diversity in Washington State populations of Kincaid’s lupine (Lupinus oreganus var kincaidii = Lupinus sulphureus ssp. kincaidii). Report submitted to USFWS, Lacey District, Washington. 15 pp

  • Severns PM, Lewis B (2007) Is it appropriate to rely on seed set to assess candidate plant populations for genetic rescue? A case study with a threatened species. Natural Areas J 27:313–319

    Article  Google Scholar 

  • Severns PM, Liston A (2008) Intraspecific chromosome number variation: a neglected threat to the conservation of rare plants. Conserv Biol 22:1641–1647

    Article  PubMed  Google Scholar 

  • Severns PM, Wilson MV (2011) Resolving conflicts between butterfly host resource abundance and genet population size estimates for a vegetatively spreading, threatened grassland legume. Biol Conserv. doi:10.1016/j.biocon.2010.12.035

  • Sheridan PM, Karrowe DN (2000) Inbreeding, outbreeding, and heterosis in the yellow pitcher plant, Sarracenia flava (Sarraceniaceae) in Virginia. Am J Bot 87:1628–1633

    Article  PubMed  CAS  Google Scholar 

  • Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci 101:15261–15264

    Article  PubMed  CAS  Google Scholar 

  • Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496

    Article  PubMed  Google Scholar 

  • Van Rossum F (2008) Conservation of long-lived perennial forest herbs in an urban context: Primula elatior as study case. Conserv Genet 9:119–128

    Article  Google Scholar 

  • Vergeer P, Rengelink R, Copal A, Ouborg NJ (2003) The interacting effects of genetic variation, habitat quality and population size on the performance of Succisa pratensis. J Ecol 91:18–26

    Article  CAS  Google Scholar 

  • Verstrepen KJ, Jansen A, Lewitter F, Fink GR (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37:986–990

    Article  PubMed  CAS  Google Scholar 

  • Waser NM, Price MV (1979) Pollen dispersal and optimal outcrossing in Delphinium nelsoni. Nature 277:294–297

    Article  Google Scholar 

  • Waser NM, Price MV (1989) Optimal outcrossing in Ipomopsis aggregata: seed set and offspring fitness. Evolution 43:1097–1109

    Article  Google Scholar 

  • Washitani I, Ishihama F, Matsumura C, Nagai M, Nishihito J, Nishihito MA (2005) Conservation ecology of Primula sieboldii: synthesis of information toward the prediction of the genetic/demographic fate of a population. Plant Species Biol 20:3–15

    Article  Google Scholar 

  • Weising K, Gardener RC (1999) A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genes of dicotyledonous angiosperms. Genome 42:9–19

    Article  PubMed  CAS  Google Scholar 

  • Welch ME, Rieseberg LH (2002) Habitat divergence between a homoploid hybrid sunflower species Helianthus paradoxus (Asteraceae), and its progenitors. Am J Bot 89:472–478

    Article  PubMed  Google Scholar 

  • Willi Y, Van Buskirk J, Fischer M (2005) A threefold genetic allee effect: population size affects cross-compatibility, inbreeding depression and drift load in the self-incompatible Ranunculus reptans. Genetics 169:2255–2266

    Article  PubMed  CAS  Google Scholar 

  • Wilson MV, Erhart T, Hammond PC, Kaye TN, Kuykendall K, Liston A, Robinson AF, Schultz CB, Severns PM (2003) Biology of Kincaid’s lupine (Lupinus sulphureus ssp. kincaidii [Smith] Phillips), a threatened species of western Oregon native prairies. Natural Areas J 23:72–83

    Google Scholar 

Download references

Acknowledgments

We thank Quentin Cronk (University of British Columbia) for primers to LEGCYCLOIDEA and Brian Knaus for sharing chloroplast SSR primers. K. Karoly and two anonymous reviewers made comments that helped improve this manuscript. P. M. Severns thanks Emma Bradford, Tri Tran, Mariah Parker-deFenix, and Stephanie McKnight for their help in the lab, the Kuhls, The Nature Conservancy (Jason Nuckols and Greg Fitzpatrick), Starker Forest, and the numerous other private landowners who wished to remain anonymous, for granting access to Kincaid’s and spurred lupine populations. Joe Arnett, Sam Friedman, and Steve Smith provided access to study sites and provided invaluable information on local populations. This research was funded by the Eugene District (Sally Villegas) and Roseburg District (Sam Friedman) Bureau of Land Management, U.S. Fish and Wildlife Service Portand District (Mikki Collins) and Lacey District (Ted Thomas) Offices, U.S. Army Corps of Engineers Fern Ridge Project (James Beal and Wes Messinger), Native Plant Society of Oregon, Bonnie Templeton Endowment Fund, Hardman Native Plant Research Endowment, Leslie and Vera Gottlieb Research Award in Plant Evolutionary Biology, and the Moldenke Plant Systematics Endowment.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul M. Severns.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Severns, P.M., Liston, A. & Wilson, M.V. Habitat fragmentation, genetic diversity, and inbreeding depression in a threatened grassland legume: is genetic rescue necessary?. Conserv Genet 12, 881–893 (2011). https://doi.org/10.1007/s10592-011-0191-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-011-0191-3

Keywords

Navigation