Skip to main content
Log in

Genetic factors accelerate demographic decline in rare Asclepias species

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

Abstract

We investigated the role of genetic, reproductive and demographic factors in the decline of two co-occurring milkweeds, Asclepias lanuginosa and A. viridiflora, in fragmented populations in Illinois and Wisconsin. Asclepias lanuginosa flowers but does not set seed while seed set is regularly observed in A. viridiflora. We used microsatellite genotyping to determine the extent of clonal growth, genetic diversity, and genetic structure in nine populations of A. lanuginosa and five populations of A. viridiflora. Microsatellite genotyping revealed extremely high clonality in A. lanuginosa; only 32 multilocus genotypes occurred among more than 300 ramets, compared to 118 multilocus genotypes among 124 ramets for A. viridiflora. Four A. lanuginosa populations were monoclonal. While we found no evidence for inbreeding, A. lanuginosa had significantly lower expected heterozygosity and a lower mean number of effective alleles than A. viridiflora. Population viability analysis (PVA) conducted at one site indicated a high probability of persistence, although the population was comprised of only two clones. Because PVA does not distinguish between ramets and genets, results should be interpreted with caution when conducted on highly clonal species. A nearly complete shift in the mode of reproduction, from sexual to asexual, appears to be the most immediate threat to survival of A. lanuginosa in these fragmented prairie remnants. Conservation management strategies should include actions to increase clonal diversity in remnant populations.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Abraham ST, Zaya DN, Koenig WD, Ashley MV (2011) Interspecific and intraspecific pollination patterns of valley oak, Quercus lobata, in a mixed stand in coastal central California. Int J Plant Sci 172:691–699

    Article  Google Scholar 

  • Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980

    Article  PubMed  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, Alberto F, Teixeira S, Procaccini G, Serrao EA, Duarte CM (2005) Assessing genetic diversity in clonal organisms: low diversity or low resolution? Combining power and cost efficiency in selecting markers. J Hered 96:434–440

    Article  CAS  PubMed  Google Scholar 

  • Avise JC (1989) A role for molecular-genetics in the recognition and conservation of endangered species. Trends Ecol Evol 4:279–281

    Article  CAS  PubMed  Google Scholar 

  • Baty F, Ritz C, Charles S, Brutsche M, Flandrois JP, Delignette-Muller ML (2014) A toolbox for nonlinear regression in R: the package nlstools. J Stat Softw (under revision)

  • Betz RF (1989) Ecology of Mead’s milkweed (Asclepias meadii Torrey). In: Proceedings of the 11th North American Prairie Conference, p 187–192

  • Betz RF, Lamp HF (1990) Flower, pod, and seed production in eighteen species of milkweeds (Asclepias). In: Proceedings of the 12th North American Prairie Conference, p 25–30

  • Bruna EM (2002) Effects of forest fragmentation on Heliconia acuminata seedling recruitment in central Amazonia. Oecologia 132:235–243

    Article  Google Scholar 

  • Bruna EM, Kress WJ (2002) Habitat fragmentation and the demographic structure of an Amazonian understory herb (Heliconia acuminata). Conserv Biol 16:1256–1266

    Article  Google Scholar 

  • Brzosko E, Wroblewska A, Ratkiewicz M (2002) Spatial genetic structure and clonal diversity of island populations of lady’s slipper (Cypripedium calceolus) from the Biebrza National Park (northeast Poland). Mol Ecol 11:2499–2509

    Article  CAS  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach, 1st edn. Springer-Verlag, New York

    Book  Google Scholar 

  • Caro TM, Laurenson MK (1994) Ecological and genetic factors in conservation: a cautionary tale. Science 263:485–486

    Article  CAS  PubMed  Google Scholar 

  • Core Team R (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Cunningham SA (2000) Effects of habitat fragmentation on the reproductive ecology of four plant species in mallee woodland. Conserv Biol 14:758–768

    Article  Google Scholar 

  • DeMauro MM (1993) Relationship of breeding system to rarity in the lakeside daisy (Hymenoxys acaulis var. glabra). Conserv Biol 7:542–550

    Article  Google Scholar 

  • Dennis B, Munholland PL, Scott JM (1991) Estimation of growth and extinction parameters for endangered species. Ecol Monogr 61:115–143

    Article  Google Scholar 

  • Diggle PK, Lower S, Ranker TA (1998) Clonal diversity in alpine populations of Polygonum viviparum (Polygonaceae). Int J Plant Sci 159:606–615

    Article  Google Scholar 

  • Dorken ME, Eckert CG (2001) Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J Ecol 89:339–350

    Article  Google Scholar 

  • Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Google Scholar 

  • Ellegren H, Primmer CR, Sheldon BC (1995) Microsatellite ‘evolution’: directionality or bias? Nat Genet 11:360–362

    Article  CAS  PubMed  Google Scholar 

  • Ellstrand NC, Roose ML (1987) Patterns of genotypic diversity in clonal plant species. Am J Bot 74:123–131

    Article  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  • Fant JB, Holmstrom RM, Sirkin E, Etterson JR, Masi S (2008) Genetic structure of threatened native populations and propagules used for restoration in a clonal species, American beachgrass (Ammophila breviligulata Fern.). Restor Ecol 16:594–603

    Article  Google Scholar 

  • Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140

    Article  Google Scholar 

  • Galpern P, Manseau M, Hettinga P, Smith K, Wilson P (2012) Allelematch: an R package for identifying unique multilocus genotypes where genotyping error and missing data may be present. Mol Ecol Resour 12:771–778

    Article  PubMed  Google Scholar 

  • Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on G(ST) and D: forget G(ST) but not all of statistics! Mol Ecol 19:3845–3852

    Article  PubMed  Google Scholar 

  • Gitzendanner MA, Weekley CW, Germain-Aubrey CC, Soltis DE, Soltis PS (2012) Microsatellite evidence for high clonality and limited genetic diversity in Ziziphus celata (Rhamnaceae), an endangered, self-incompatible shrub endemic to the Lake Wales Ridge, Florida, USA. Conserv Genet 13:223–234

    Article  CAS  Google Scholar 

  • Glemin S, Petit C, Maurice S, Mignot A (2008) Consequences of low mate availability in the rare self-incompatible species Brassica insularis. Conserv Biol 22:216–221

    Article  PubMed  Google Scholar 

  • Gonzalez-Varo JP, Arroyo J, Aparicio A (2009) Effects of fragmentation on pollinator assemblage, pollen limitation and seed production of Mediterranean myrtle (Myrtus communis). Biol Conserv 142:1058–1065

    Article  Google Scholar 

  • Grixti JC, Wong LT, Cameron SA, Favret C (2009) Decline of bumble bees (Bombus) in the North American Midwest. Biol Conserv 142:75–84

    Article  Google Scholar 

  • Hayworth D, Bowles M, Schaal B, Williamson K (2001) Clonal population structure of the Federal threatened Mead’s milkweed, as determined by RAPD analysis, and its conservation implications. In: Proceedings of the Seventeenth North American Prairie Conference: Seeds for the future, roots of the past, p 182–190

  • Hobbs RJ, Yates CJ (2003) Impacts of ecosystem fragmentation on plant populations: generalising the idiosyncratic. Aust J Bot 51:471–488

    Article  Google Scholar 

  • Honnay O, Bossuyt B (2005) Prolonged clonal growth: escape route or route to extinction? Oikos 108:427–432

    Article  Google Scholar 

  • Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Jombart T, Ahmed I (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jost L (2008) G(ST) and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  PubMed  Google Scholar 

  • Kabat SM, Dick CW, Hunter MD (2010) Isolation and characterization of microsatellite loci in the common milkweed, Asclepias syriaca (Apocynaceae). Am J Bot 97:E37–E38

    Article  CAS  PubMed  Google Scholar 

  • Kephart SR (1981) Breeding systems in Asclepias incarnata L., A. syriaca L., and A. verticillata L. Am J Bot 68:226–232

    Article  Google Scholar 

  • Kephart SR (1983) The partitioning of pollinators among three species of Asclepias. Ecology 64:120–133

    Article  Google Scholar 

  • Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460

    Article  CAS  PubMed  Google Scholar 

  • Lewis PO, Zaykin D (2001) Genetic data analysis: computer program for analysis of allelic data, version 1.1. University of Connecticut, Connecticut

  • Lipow SR, Wyatt R (2000) Single gene control of postzygotic self-incompatibility in poke milkweed, Asclepias exaltata L. Genetics 154:893–907

    PubMed Central  CAS  PubMed  Google Scholar 

  • Moody-Weis JM, Heywood JS (2001) Pollination limitation to reproductive success in the Missouri evening primrose, Oenothera macrocarpa (Onagraceae). Am J Bot 88:1615–1622

    Article  CAS  PubMed  Google Scholar 

  • Morris WF, Doak DF (2002) Quantitative conservation biology: theory and practice of population viability analysis. Sinauer Associates, Sunderland, MA, U.S.A

  • Nei M, Chesser RK (1983) Estimation of fixation indexes and gene diversities. Ann Hum Genet 47:253–259

    Article  CAS  PubMed  Google Scholar 

  • Newman BJ, Ladd P, Brundrett M, Dixon KW (2013) Effects of habitat fragmentation on plant reproductive success and population viability at the landscape and habitat scale. Biol Conserv 159:16–23

    Article  Google Scholar 

  • O’Quinn RL, Fishbein M (2009) Isolation, characterization and cross-species amplification of polymorphic microsatellite loci in Asclepias (Apocynaceae). Conserv Genet 10:1437–1440

    Article  Google Scholar 

  • Ouborg NJ, Vergeer P, Mix C (2006) The rough edges of the conservation genetics paradigm for plants. J Ecol 94:1233–1248

    Article  Google Scholar 

  • Palmer B, Armstrong L (2000) Demography and monitoring of Welsh’s milkweed (Asclepias welshii) at Coral Pink Sand Dunes. In: Southwestern rare and endangered plants: Proceedings of the Third Conference, p 59–69

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

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pielou EC (1969) An introduction to mathematical ecology. Wiley-Interscience, New York

    Google Scholar 

  • Plants of Concern 2013 Plants of Concern (POC): An online database of rare plant data [web application]. POC, Chicago Botanic Garden, Glencoe, IL. Available with permission from http://www.plantsofconcern.org. Accessed 11 Oct 2013

  • Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rousset F (2008) GENEPOP′007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  CAS  PubMed  Google Scholar 

  • Scobie AR, Wilcock CC (2009) Limited mate availability decreases reproductive success of fragmented populations of Linnaea borealis, a rare, clonal self-incompatible plant. Ann Bot 103:835–846

    Article  PubMed Central  CAS  PubMed  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 USA 101:15261–15264

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Swink F, Wilhelm G (1994) Plants of the Chicago region, 4th edn. Indiana Academy of Science, Indianapolis

    Google Scholar 

  • Tecic DL, McBride JL, Bowles ML, Nickrent DL (1998) Genetic variability in the federal threatened Mead’s milkweed, Asclepias meadii Torrey (Asclepiadaceae), as determined by allozyme electrophoresis. Ann Mo Bot Gard 85:97–109

    Article  Google Scholar 

  • USDA, NRCS (2013) The PLANTS database. National Plant Data Team, Greensboro, NC 27401-4901 USA. http://plants.usda.gov. Accessed 21 Oct 2013

  • Vekemans X, Schierup MH, Christiansen FB (1998) Mate availability and fecundity selection in multi-allelic self-incompatibility systems in plants. Evolution 52:19–29

    Article  Google Scholar 

  • Wagenius S, Lonsdorf E, Neuhauser C (2007) Patch aging and the S-allee effect: breeding system effects on the demographic response of plants to habitat fragmentation. Am Nat 169:383–397

    Article  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wheeler RE (2010) multResp() lmPerm. The R project for statistical computing. http://www.r-project.org/

  • Wilcock C, Neiland R (2002) Pollination failure in plants: why it happens and when it matters. Trends Plant Sci 7:270–277

    Article  CAS  PubMed  Google Scholar 

  • Wilk JA, Kramer AT, Ashley MV (2009) High variation in clonal vs. sexual reproduction in populations of the wild strawberry, Fragaria virginiana (Rosaceae). Ann Bot 104:1413–1419

    Article  PubMed Central  PubMed  Google Scholar 

  • Willson MF, Price PW (1977) Evolution of inflorescence size in Asclepias (Asclepiadaceae). Evolution 31:495–511

    Article  Google Scholar 

  • Winter DJ (2012) MMOD: an R library for the calculation of population differentiation statistics. Mol Ecol Resour 12:1158–1160

    Article  CAS  PubMed  Google Scholar 

  • Wyatt R (1976) Pollination and fruit-set in Asclepias: a reappraisal. Am J Bot 63:845–851

    Article  Google Scholar 

  • Wyatt R, Broyles SB (1994) Ecology and evolution of reproduction in milkweeds. Annu Rev Ecol Syst 25:423–441

    Article  Google Scholar 

  • Wyatt R, Broyles SB (1997) The weedy tropical milkweeds Asclepias curassavica and A. fruticosa are self-compatible. Biotropica 29:232–234

    Article  Google Scholar 

  • Young AG, Broadhurst LM, Thrall PH (2012) Non-additive effects of pollen limitation and self-incompatibility reduce plant reproductive success and population viability. Ann Bot 109:643–653

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank S. R. Hill and V. Nuzzo for their guidance in locating populations, S. Masi for help with obtaining permits and samples, R. Bruner, R. Henderson, and the Prairie Enthusiasts for field assistance, M. Bowles for advice on hand pollination, L. Rericha-Anchor for conducting pollinator observations, and the Ashley lab for comments on the manuscript. The authors thank Illinois Nature Preserves Commission, McHenry Conservation District, Forest Preserve District of Cook County, Illinois Department of Natural Resources, and Wisconsin Department of Natural Resources for access to the sites. The A. lanuginosa population monitoring data was collected by C. Akins, D. Beaver, S. Beaver, D. Blevins, L. Bolt, D. Buckley, L. Clarizio, E. Collins, S. Fix, L. Hartzig, C. Howard, D. Krause, M. Kuhl, C. Mason, E. Mayfield, M. McNab, D. Moreland, G. Moreland, M. Nelson, C. Nye, J. Perbix, D. Purn, G. Rajsky, D. Schwaegler, W. Schennum, C. Sedlak, L. Sedlak, T. Thornrose, K. Williams, A. Wilson, and B. Wingate. This work was supported by the Provost Award from University of Illinois at Chicago, Sigma Xi Grant-in-Aid of Research, Division of Botany Travel Award and Student Research Award from Illinois State Academy of Science, and Illinois Department of Natural Resources/Illinois Endangered Species Protection Board, Grant No. RC11EO4 W (40-G0503-801).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mary V. Ashley.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, E.S., Zaya, D.N., Fant, J.B. et al. Genetic factors accelerate demographic decline in rare Asclepias species. Conserv Genet 16, 359–369 (2015). https://doi.org/10.1007/s10592-014-0663-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-014-0663-3

Keywords

Navigation