Skip to main content

Advertisement

SpringerLink
Log in

Low genetic differentiation despite high fragmentation in the endemic serpentinophyte Minuartia smejkalii (M. verna agg., Caryophyllaceae) revealed by RADSeq SNP markers

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

Abstract

Minuartia smejkalii is an obligate serpentinophyte plant endemic to the Czech Republic. Since the 1960s, the species’ habitat has undergone strong human-mediated fragmentation, resulting in extinction of some populations and dramatic size reduction of the remaining populations. Thus, contrary to the typically stable serpentine habitats, M. smejkalii habitats underwent a recent and severe decline, which can exacerbate the effects of fragmentation on population genetic structure. We examined the genetic structure of all known M. smejkalii populations and two populations of M. corcontica and M. caespitosa, which are closely related, using RADSeq. The results indicate low, but clear differentiation among the three species, thus supporting the status of M. smejkalii as an independent taxon, though more extensive analysis of the whole group is needed. We further show high genetic diversity within M. smejkalii populations, low to moderate among-populations differentiation, and moderate regional differentiation. This could be due to the outcrossing mating system of M. smejkalii promoting high levels of gene flow and historical factors (multiple founder events, a recent bottleneck and/or a genetic time lag). We finally demonstrate that 2–3% of the markers show differentiation patterns consistent with divergent selection, suggesting that some local adaptation might have occured in M. smejkalii. Based on our observations, but without any experimental testing for local adaptation, if a conservation action is to be carried out, we recommend strictly separating the material from the two regions, and if possible, separating the populations within a region.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

Genomic data is available at BioSample, ID: SUB5620362.

References

  • Agapow P-M, Burt A (2001) Indices of multilocus linkage disequilibrium. Mol Ecol Notes 1:101–102

    Article  CAS  Google Scholar 

  • Babst-Kostecka AA, Parisod C, Godé C, Vollenweider P, Pauwels M (2014) Patterns of genetic divergence among populations of the pseudometallophyte Biscutella laevigata from southern Poland. Plant Soil 383:245–256

    Article  CAS  Google Scholar 

  • Bilz M (2011) The IUCN Red List of Threatened Species. Minuartia smejkalii. The IUCN Red List of Threatened Species 2011

  • Borgen L (1999) Genetic variation in Minuartia (Caryophyllaceae) in Svalbard. Nord J Bot 19:179–192

    Article  Google Scholar 

  • Brady KU, Kruckeberg AR, Bradshaw HD Jr (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266

    Article  Google Scholar 

  • Brown AHD, Feldman MW, Nevo E (1980) Multilocus structure of natural populations of Hordeum spontaneum. Genetics 96:523–536

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bushnell B (2014) BBMap: a fast, accurate, splice-aware aligner

  • Cabrera-Toledo D, Gonzalez-Astorga J, Vovides AP (2008) Heterozygote excess in ancient populations of the critically endangered Dioon caputoi (Zamiaceae, Cycadales) from central Mexico. Bot J Linn Soc 158:436–447

    Article  Google Scholar 

  • Cheptou P-O, Hargreaves AL, Bonte D, Jacquemyn H (2017) Adaptation to fragmentation: evolutionary dynamics driven by human influences. Philos Trans R Soc B 372:20160037

    Article  Google Scholar 

  • Chytrý M, Danihelka J, Kaplan Z, Pyšek P (2017) Flora and vegetation of the Czech Republic. Springer, Cham

    Book  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dillenberger MS, Kadereit JW (2014) Maximum polyphyly: multiple origins and delimitation with plesiomorphic characters require a new circumscription of Minuartia (Caryophyllaceae). Taxon 63:64–88

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Dray S, Chessel D, Thioulouse J (2003) Co-inertia analysis and the linking of ecological data tables. Ecology 84:3078–3089

    Article  Google Scholar 

  • Ducousso A, Petit D, Valero M, Vernet P (1990) Genetic variation between and within populations of a perennial grass: Arrhenatherum elatius. Heredity 65:179

    Article  Google Scholar 

  • Dvořáková M (1988) Minuartia smejkalii, eine neue Art aus der Minuartia gerardii-Gruppe (Caryophyllaceae). Preslia 60:1–9

    Google Scholar 

  • Dvořáková M (2003) Minuartia pauciflora, a Carpathian endemic species of the M-verna group. Preslia 75:349–356

    Google Scholar 

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

    Article  CAS  PubMed  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 

  • Epps CW, Keyghobadi N (2015) Landscape genetics in a changing world: disentangling historical and contemporary influences and inferring change. Mol Ecol 24:6021–6040

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Foll M, Gaggiotti OE (2008) A genome scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993

    Article  PubMed  PubMed Central  Google Scholar 

  • Fuentes-Pardo AP, Ruzzante DE (2017) Whole-genome sequencing approaches for conservation biology: advantages, limitations and practical recommendations. Mol Ecol 26:5369–5406

    Article  CAS  PubMed  Google Scholar 

  • Gitzendanner MA, Soltis PS (2000) Patterns of genetic variation in rare and widespread plant congeners. Am J Bot 87:783–792

    Article  CAS  PubMed  Google Scholar 

  • Grulich V (2012) Red List of vascular plants of the Czech Republic. Preslia 84:631–645

    Google Scholar 

  • Hamrick JL, Godt MJW (1989) Allozyme diversity in plant species. In: Brown AHD, Clegg MT, Kahler AL, Weir BS (eds) Plant population genetics, breeding and genetic resources. Sinauer Associates, Sunderland, pp 43–63

    Google Scholar 

  • Harrison S, Rajakaruna N (2011) Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley

    Google Scholar 

  • Hejný S, Slavík B (2003) Květena ČR, díl 2. Academia, Praha

    Google Scholar 

  • Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18:147–155

    Article  Google Scholar 

  • Huson DH, Bryant D (2005) Estimating phylogenetic trees and networks using SplitsTree 4. Manuscr. Prep. Softw. www.split.org. Accessed 22 Dec 2019

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

    CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    PubMed  PubMed Central  Google Scholar 

  • Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281

    Article  PubMed  PubMed Central  Google Scholar 

  • Knaus BJ, Grünwald NJ (2017) VCFR: a package to manipulate and visualize variant call format data in R. Mol Ecol Resour 17:44–53

    Article  CAS  PubMed  Google Scholar 

  • Kogura Y, Seeb JE, Azuma N, Kudo H, Abe S, Kaeriyama M (2011) The genetic population structure of lacustrine sockeye salmon, Oncorhynchus nerka, in Japan as the endangered species. Environ Biol Fishes 92:539–550

    Article  Google Scholar 

  • Kramer AT, Havens K (2009) Plant conservation genetics in a changing world. Trends Plant Sci 14:599–607

    Article  CAS  PubMed  Google Scholar 

  • Kruckeberg AR (1984) California serpentines: flora, vegetation, geology, soils, and management problems. University of California Press, Berkeley

    Google Scholar 

  • Kubát K (2002) Klíč ke květeně České republiky. Acad, Praha

    Google Scholar 

  • Lanes ÉC, Pope NS, Alves R, Carvalho Filho NM, Giannini TC, Giulietti AM, Imperatriz-Fonseca VL, Monteiro W, Oliveira G, Silva AR (2018) Landscape genomic conservation assessment of a narrow-endemic and a widespread morning glory from Amazonian savannas. Front Plant Sci 9:532

    Article  PubMed  PubMed Central  Google Scholar 

  • Leipold M, Tausch S, Hirtreiter M, Poschlod P, Reisch C (2018) Sampling for conservation genetics: how many loci and individuals are needed to determine the genetic diversity of plant populations using AFLP? Conserv Genet Resour. https://doi.org/10.1007/s12686-018-1069-1

    Article  Google Scholar 

  • Lindenmayer DB, Fischer J (2013) Habitat fragmentation and landscape change: an ecological and conservation synthesis. Island Press, Washington, DC

    Google Scholar 

  • Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annu Rev Ecol Syst 27:237–277

    Article  Google Scholar 

  • Lodhi MA, Ye G-N, Weeden NF, Reisch BI (1994) A simple and efficient method for DNA extraction from grapevine cultivars and Vitis species. Plant Mol Biol Report 12:6–13

    Article  CAS  Google Scholar 

  • Lomolino MV, Riddle BR, Whittaker RJ (2017) Biogeography: biological diversity across space and time. Sinauer Associates Inc., Sunderland

    Google Scholar 

  • Mariette S, Le Corre V, Austerlitz F, Kremer A (2002) Sampling within the genome for measuring within-population diversity: trade-offs between markers. Mol Ecol 11:1145–1156

    Article  CAS  PubMed  Google Scholar 

  • Mattner J, Zawko G, Rossetto M, Krauss SL, Dixon KW, Sivasithamparam K (2002) Conservation genetics and implications for restoration of Hemigenia exilis (Lamiaceae), a serpentine endemic from Western Australia. Biol Conserv 107:37–45

    Article  Google Scholar 

  • Mayer MS, Soltis PS, Soltis DE (1994) The evolution of the Streptanthus glandulosus complex (Cruciferae): genetic divergence and gene flow in serpentine endemics. Am J Bot 81:1288–1299

    Article  Google Scholar 

  • McKay JK, Christian CE, Harrison S, Rice KJ (2005) “How local is local?”—a review of practical and conceptual issues in the genetics of restoration. Restor Ecol 13:432–440

    Article  Google Scholar 

  • McNeely JA (2002) The role of taxonomy in conserving biodiversity. J Nat Conserv 10:145–153

    Article  Google Scholar 

  • Mengoni A, Gonnelli C, Galardi F, Gabbrielli R, Bazzicalupo M (2000) Genetic diversity and heavy metal tolerance in populations of Silene paradoxa L. (Caryophyllaceae): a random amplified polymorphic DNA analysis. Mol Ecol 9:1319–1324

    Article  CAS  PubMed  Google Scholar 

  • Meusel H, Jäger E, Rauschert J, Weinert E (1965) Vergleichende Chorologie der zentraleuropäischen Flora. Jena

  • Mimura M, Yahara T, Faith DP, Vázquez-Domínguez E, Colautti RI, Araki H, Javadi F, Núñez-Farfán J, Mori AS, Zhou S (2017) Understanding and monitoring the consequences of human impacts on intraspecific variation. Evol Appl 10:121–139

    Article  PubMed  Google Scholar 

  • Montalvo AM, Ellstrand NC (2000) Transplantation of the Subshrub Lotus scoparius: testing the home-site advantage hypothesis. Conserv Biol 14:1034–1045

    Article  Google Scholar 

  • Moore AJ, Merges D, Kadereit JW (2013) The origin of the serpentine endemic Minuartia laricifolia subsp. ophiolitica by vicariance and competitive exclusion. Mol Ecol 22:2218–2231

    Article  CAS  PubMed  Google Scholar 

  • Morris GP, Hu Z, Grabowski PP, Borevitz JO, de Graaff M-A, Miller RM, Jastrow JD (2016) Genotypic diversity effects on biomass production in native perennial bioenergy cropping systems. Gcb Bioenergy 8:1000–1014

    Article  PubMed  Google Scholar 

  • Mosca E, Eckert AJ, Di Pierro EA, Rocchini D, La Porta N, Belletti P, Neale DB (2012) The geographical and environmental determinants of genetic diversity for four alpine conifers of the European Alps. Mol Ecol 21:5530–5545

    Article  CAS  PubMed  Google Scholar 

  • Novák FA (1960) Fylogenese serpentinových typů. [Phylogeny of serpentine types.]. Preslia 32:1–8

    Google Scholar 

  • Nybom H, Bartish IV (2000) Effects of life history traits and sampling strategies on genetic diversity estimates obtained with RAPD markers in plants. Perspect Plant Ecol Evol Syst 3:93–114

    Article  Google Scholar 

  • Paradis E (2010) pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26:419–420

    Article  CAS  PubMed  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Pešout P (2001) Final report: the rescue of Dolnokralovice serpentines and part of Vltava slopes in cooperation with owners. ČSOP, Vlašim

  • 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 90:502–503

    Article  Google Scholar 

  • Quintela-Sabarís C, Vendramin GG, Castro-Fernández D, Fraga MI (2010) Chloroplast microsatellites reveal that metallicolous populations of the Mediterranean shrub Cistus ladanifer L have multiple origins. Plant Soil 334:161–174

    Article  CAS  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Quilón I, Santos-del-Blanco L, Serra-Varela MJ, Koskela J, González-Martínez SC, Alía R (2016) Capturing neutral and adaptive genetic diversity for conservation in a highly structured tree species. Ecol Appl 26:2254–2266

    Article  PubMed  Google Scholar 

  • Russello MA, Waterhouse MD, Etter PD, Johnson EA (2015) From promise to practice: pairing non-invasive sampling with genomics in conservation. PeerJ 3:e1106

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sádlo J, Petřík P, Boublík K, Rychtařík P, Šímová I (2011) Diverzita rostlinstva Hradčanských stěn (Dokesko) a její příčiny [Habitats, vegetation and flora of the Hradčanské stěny rocks (Doksy region, northern Bohemia): causes of diversity]. Zpr Čes Bot Společ 46:17–38

    Google Scholar 

  • Shafer AB, Wolf JB, Alves PC, Bergström L, Bruford MW, Brännström I, Colling G, Dalén L, De Meester L, Ekblom R (2015) Genomics and the challenging translation into conservation practice. Trends Ecol Evol 30:78–87

    Article  PubMed  Google Scholar 

  • Słomka A, Sutkowska A, Szczepaniak M, Malec P, Mitka J, Kuta E (2011) Increased genetic diversity of Viola tricolor L. (Violaceae) in metal-polluted environments. Chemosphere 83:435–442

    Article  PubMed  CAS  Google Scholar 

  • Smith JM, Smith NH, O’Rourke M, Spratt BG (1993) How clonal are bacteria? Proc Natl Acad Sci 90:4384–4388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turchetto C, Segatto ALA, Mäder G, Rodrigues DM, Bonatto SL, Freitas LB (2016) High levels of genetic diversity and population structure in an endemic and rare species: implications for conservation. AoB Plants. https://doi.org/10.1093/aobpla/plw002

    Article  PubMed  PubMed Central  Google Scholar 

  • Wege JA, Thiele KR, Shepherd KA, Butcher R, Macfarlane TD, Coates DJ (2015) Strategic taxonomy in a biodiverse landscape: a novel approach to maximizing conservation outcomes for rare and poorly known flora. Biodivers Conserv 24:17–32

    Article  Google Scholar 

  • Whitlock R, Hipperson H, Thompson DBA, Butlin RK, Burke T (2016) Consequences of in situ strategies for the conservation of plant genetic diversity. Biol Conserv 203:134–142

    Article  Google Scholar 

  • Whittaker RH (1954) The ecology of serpentine soils. Ecology 35:258–288

    Article  Google Scholar 

  • Wolf A (2001) Conservation of endemic plants in serpentine landscapes. Biol Conserv 100:35–44

    Article  Google Scholar 

  • Wolf AT, Harrison SP (2001) Effects of habitat size and patch isolation on reproductive success of the serpentine morning glory. Conserv Biol 15:111–121

    Article  Google Scholar 

  • Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418

    Article  CAS  PubMed  Google Scholar 

  • Zawko G, Krauss SL, Dixon KW, Sivasithamparam K (2001) Conservation genetics of the rare and endangered Leucopogon obtectus (Ericaceae). Mol Ecol 10:2389–2396

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The study was supported by Project LIFE for Minuartia (Grant No. LIFE15NAT/CZ/000818), which is implemented with the financial contribution of the European Union, the Life program and with the financial contribution of the Ministry of Environment of the Czech Republic and party by and the long-term research development Project RVO 67985939.

Author information

Authors and Affiliations

  1. Department of Biology and Ecology, Faculty of Science, University of Ostrava, Ostrava, Czech Republic

    Bojana Stojanova

  2. Institute of Botany, Academy of Sciences of the Czech Republic, Průhonice, Czech Republic

    Maria Šurinová, Vojtěch Zeisek, Zuzana Münzbergová & Hana Pánková

  3. Department of Botany, Faculty of Science, Charles University, Prague, Czech Republic

    Maria Šurinová, Vojtěch Zeisek & Zuzana Münzbergová

Authors
  1. Bojana Stojanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Šurinová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vojtěch Zeisek
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zuzana Münzbergová
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hana Pánková
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bojana Stojanova.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10592_2019_1239_MOESM1_ESM.pdf

Supplementary material 1—BayeScan results of the detection of outlier loci. FST – the locus component of the FST estimate under a multinomial Dirichlet model, q-value – posterior probability of the selection model after correction for multiple testing. (PDF 361 kb)

10592_2019_1239_MOESM2_ESM.pdf

Supplementary material 2—Boxplot of the depth of coverage of the 12 000RADSeq markers initially developed for the study. (PDF 504 kb)

10592_2019_1239_MOESM3_ESM.pdf

Supplementary material 3—BIC for each number of K estimated for the K-mean clustering of the entire data set (M. smejkalii, M. corcontica, and M. caespitosa). (PDF 616 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stojanova, B., Šurinová, M., Zeisek, V. et al. Low genetic differentiation despite high fragmentation in the endemic serpentinophyte Minuartia smejkalii (M. verna agg., Caryophyllaceae) revealed by RADSeq SNP markers. Conserv Genet 21, 187–198 (2020). https://doi.org/10.1007/s10592-019-01239-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-019-01239-4

Keywords

Search

Navigation