Skip to main content
SpringerLink
Log in

Microsatellite loci transferability and genetic diversity of the aquatic plant Nymphoides fallax Ornduff (Menyanthaceae), endemic to the Mexican and Guatemalan highlands

  • Research paper
  • Published:
Limnology Aims and scope Submit manuscript

Abstract

Nymphoides species are cosmopolitan aquatics with floating leaves and frequent in freshwater wetlands. Nymphoides fallax is restricted to highlands of Mexico and Guatemala. We tested the transferability of 10 microsatellite loci previously developed for N. peltata in 18 populations of N. fallax. Seven polymorphic loci were successfully amplified. Allele sizes were automatically obtained using 2100 Bioanalyzer Expert software. Genotypes were determined using the allele dosage method. Chromosome counts confirmed that N. fallax is a tetraploid. Alleles per locus ranged from 5 to 17; the observed and expected heterozygosities per population ranged from 0.51 to 0.66 and from 0.72 to 0.81, respectively. We observed higher genetic diversity within populations (92%) than among populations (8%). Our results show that cross-amplification is a valid technique for studying Nymphoides. No clones were found, indicating that N. fallax relies heavily on sexual reproduction. Our work may stimulate further population genetic studies of the genus Nymphoides that could be useful for conservation programs, as well as to promote additional research on landscape genetics and reproductive mechanisms in aquatic plants.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alix K, Gérard PR, Schwarzacher T, Heslop-Harrison JS (2017) Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants. Ann Bot 120(2):183–194

    Article  PubMed  PubMed Central  Google Scholar 

  • Assoumane A, Zoubeirou AM, Rodier-Goud M, Favreau B, Bezançon G, Verhaegen D (2013) Highlighting the occurrence of tetraploidy in Acacia senegal (L.) Willd. and genetic variation patterns in its natural range revealed by DNA microsatellite markers. Tree Genet Genom 9:93–106

    Article  Google Scholar 

  • Barrett SCH, Shore JS (2008) New insights on heterostyly: comparative biology, ecology and genetics. In: Franklin-Tong VE (ed) Self-incompatibility in flowering plants. Springer, Berlin, pp 3–32

    Chapter  Google Scholar 

  • Calhoun AJ, Mushet DM, Bell KP, Boix D, Fitzsimons JA, Isselin-Nondedeu F (2017) Temporary wetlands: challenges and solutions to conserving a ‘disappearing’ ecosystem. Biol Cons. https://doi.org/10.1016/j.biocon.2016.11.024

    Article  Google Scholar 

  • Cao QJ, Mei FF, Wang L (2017) Population genetic structure in six sympatric and widespread aquatic plants inhabiting diverse lake environments in China. Ecol Evol 7(15):5713–5723

    Article  PubMed  PubMed Central  Google Scholar 

  • Castro-Castro A, Vargas-Amado G, Castañeda-Nava JJ, Harker M, Munguía-Lino G, Santacruz-Ruvalcaba F, Rodríguez A (2017) Números cromosómicos para tres especies de Cosmos sección Discopoda (Asteraceae, Coreopsideae), con notas citogeográficas. Acta Botánica Mexicana 118:41–51

    Article  Google Scholar 

  • Cook CD (1990) Seed dispersal of Nymphoides peltata (SG Gmelin) O. Kuntze (Menyanthaceae). Aquat Bot 37(4):325–340

    Article  Google Scholar 

  • 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):40–69

    Article  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garino C, Rinaldi M, de Paolis A, Travaglia F, Coïsson JD, Arlorio M (2014) Improving the application of SSR polymorphism analysis coupled with Lab-on-a-chip® capillary electrophoresis to assess food authenticity: Italian pigmented rice as case study. Food Res Int 64:790–798. https://doi.org/10.1016/j.foodres.2014.08.008

    Article  CAS  PubMed  Google Scholar 

  • Grünwald NJ, Goodwin SB, Milgroom MG, Fry WE (2003) Analysis of genotypic diversity data for populations of microorganisms. Phytopathology 93:738–746

    Article  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Resour 2(4):618–620. https://doi.org/10.1046/j.1471-8286.2002.00305.x

    Article  CAS  Google Scholar 

  • Hardy O, Vekemans X (2015) SPAGeDi 1.5. A program for Spatial Pattern Analysis of Genetic Diversity. User’s manual. Available via Université Libre de Bruxelles, Brussells, Belgium. https://ebe.ulb.ac.be/ebe/SPAGeDi_files/SPAGeDi_1.5_Manual.pdf. Accessed 27 Feb 2018

  • Hedrick PW (2011) Genetics of populations, 4th edn. Jones and Bartlett, Boston

    Google Scholar 

  • Hedrick PW (2013) High inbreeding in sheep or erroneous estimation? J Hered 104(2):298–299

    Article  PubMed  Google Scholar 

  • Huang W, Chen Q, Chen K (2015) Seed bank characteristics of the Nymphoides peltata population in Lake Taihu. Scientific Reports. https://doi.org/10.1038/srep13261

    Article  PubMed  PubMed Central  Google Scholar 

  • Husband BC, Baldwin SJ, Suda J (2013) The incidence of polyploidy in natural plant populations: major patterns and evolutionary processes. In: Greilhuber J, Dolezel J, Wendel J (eds) Plant genome diversity, vol 2. Springer, Vienna, pp 255–276

    Chapter  Google Scholar 

  • Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with mixed (clonal/sexual) reproduction. PeerJ 2:e281. https://doi.org/10.7717/peerj.281

    Article  PubMed  PubMed Central  Google Scholar 

  • Kirov I, Divashuk M, Van Laere K, Soloviev A, Khrustaleva L (2014) An easy “SteamDrop” method for high quality plant chromosome preparation. Mol Cytogen. https://doi.org/10.1186/1755-8166-7-21

    Article  Google Scholar 

  • Landgrave R, Moreno-Casasola P (2012) Evaluación cuantitativa de la pérdida de humedales en México. Investigación Ambiental 4(1):19–35

    Google Scholar 

  • Larson D (2007) Reproduction strategies in introduced Nymphoides peltata populations revealed by genetic markers. Aquat Bot 86(4):402–406

    Article  Google Scholar 

  • Li ZZ, Sun SS, Wang QF, Chen JM (2017) RNA-seq analysis of the distylous plant Nymphoides peltata Identified ortholog genes between long-and short-styled flowers. Front in Ecol Evol 5(59):1–3. https://doi.org/10.3389/fevo.2017.00059

    Article  Google Scholar 

  • Liao YY, Yue XL, Guo YH, Gituru WR, Wang QF, Chen JM (2013) Genotypic diversity and genetic structure of populations of the distylous aquatic plant Nymphoides peltata (Menyanthaceae) in China. J Syst Evol 51(5):536–544. https://doi.org/10.1111/jse.12023

    Article  Google Scholar 

  • Liu XL, Jiang FF, Wang ZW et al (2017) Wider geographic distribution and higher diversity of hexaploids than tetraploids in Carassius species complex reveal recurrent polyploidy effects on adaptive evolution. Sci Rep. https://doi.org/10.1038/s41598-017-05731-0

    Article  PubMed  PubMed Central  Google Scholar 

  • Magalhães TL, Martínez M (2018) Temporary freshwater wetlands floristics in central Mexico highlands. Bot Sci 96(1):138–156. https://doi.org/10.17129/botsci.1532

    Article  Google Scholar 

  • Magallán F, Martínez M, Hernández Sandoval L, Oyama K (2009) Estructura Genética de poblaciones de Eriocaulon bilobatum (Eriocaulaceae): una especie amenazada de humedades temporales. Boletín de la Sociedad Botánica de México 85:81–88

    Google Scholar 

  • Magallán F, Martínez M, Hernández-Sandoval L, González-Rodríguez A, Oyama K (2013) Diversidad genética de Lilaea scilloides (Juncaginaceae) en el centro de México. Revista Mexicana de Biodiversidad 84(1):240–248

    Article  Google Scholar 

  • Martínez M, García A (2001) Flora y vegetación acuática de localidades selectas del estado de Querétaro. Acta Botánica Mexicana 54:1–23

    Google Scholar 

  • Martínez M, Gómez Sánchez M (2006) Descripción anatómica vegetativa de dos especies de Nymphoides (Menyanthaceae). Revista Mexicana de Biodiversidad 77(1):81–87

    Google Scholar 

  • Meirmans PG, Van Tienderen PH (2013) The effects of inheritance in tetraploids on genetic diversity and population divergence. Heredity 110(2):131–137

    Article  CAS  PubMed  Google Scholar 

  • Meirmans PG, Den Nijs H, Van Tienderen PH (2006) Male sterility in triploid dandelions: asexual females vs asexual hermaphrodites. Heredity 96:45–52

    Article  CAS  PubMed  Google Scholar 

  • Moncada P, McCouch S (2004) Simple sequence repeat diversity in diploid and tetraploid Coffea species. Genome 47:501–509

    Article  CAS  PubMed  Google Scholar 

  • Mora-Olivo A, Villaseñor JL, Martínez M (2013) Las plantas vasculares acuáticas estrictas y su conservación en México. Acta Botánica Mexicana 103:27–63

    Article  Google Scholar 

  • Morin PA, Manaster C, Mesnick SL, Holland R (2009) Normalization and binning of historical and multi-source microsatellite data: overcoming the problems of allele size shift with allelogram. Molecular Ecology Resources 9(6):1451–1455. https://doi.org/10.1111/j.1755-0998.2009.02672.x

    Article  PubMed  Google Scholar 

  • Mushet DM, Calhoun AJ, Alexander LC, Cohen MJ, DeKeyser ES, Fowler L, Lane CR, Lang MW, Rains MC, Walls SC (2015) Geographically isolated wetlands: rethinking a misnomer. Wetlands 35(3):423–431

    Article  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nielsen R, Tarpy DR, Reeve HK (2003) Estimating effective paternity number in social insects and the effective number of alleles in a population. Mol Ecol 12(11):3157–3164. https://doi.org/10.1046/j.1365-294X.2003.01994.x

    Article  PubMed  Google Scholar 

  • Nishihiro J, Uesugi R, Takagawa S, Washitani I (2009) Toward the restoration of a sustainable population of a threatened aquatic plant, Nymphoides peltata: Integrated genetic/demographic studies and practices. Biol Cons 142(9):1906–1912

    Article  Google Scholar 

  • Ornduff R (1969) Neotropical Nymphoides (Menyanthaceae): meso-American and West Indian species. Brittonia 21(4):346–352

    Article  Google Scholar 

  • Ornduff R (1970) Cytogeography of Nymphoides (Menyanthaceae). Taxon 19(5):715–719. https://doi.org/10.2307/1219284

    Article  Google Scholar 

  • Pekel JF, Cottam A, Gorelick N, Belward AS (2016) High-resolution mapping of global surface water and its long-term changes. Nature 540:418–422. https://doi.org/10.1038/nature20584

    Article  CAS  PubMed  Google Scholar 

  • Robertson A, Rich TCG, Allen AM et al (2010) Hybridization and polyploidy as drivers of continuing evolution and speciation in Sorbus. Mol Ecol 19:1675–1690

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available via https://www.R-project.org/. Accessed 27 Feb 2018

  • Shibayama Y, Uesugi R, Tsumura Y, Washitani I (2006) Conservation of the Lake Kasumigaura population of Nymphoides indica (L.) Kuntze based on genetic evaluation using microsatellite markers. Limnology 7(3):193–197

    Article  Google Scholar 

  • Soltis PS, Marchant DB, Van de Peer Y, Soltis DE (2015) Polyploidy and genome evolution in plants. Curr Opin Genet Dev 35:119–125

    Article  CAS  PubMed  Google Scholar 

  • Sweetman AC, Kettenring KM, Mock KE (2013) The pattern and structure of genetic diversity of Schoenoplectus maritimus: implications for wetland revegetation. Aquat Bot 104:47–54

    Article  Google Scholar 

  • Takagawa S, Washitani I, Uesugi R, Tsumura Y (2006) Influence of inbreeding depression on a lake population of Nymphoides peltata after restoration from the soil seed bank. Conserv Genet 7(5):705–716

    Article  Google Scholar 

  • Tani N, Kawahara T, Yoshimaru H (2005) Development and diversity of microsatellite markers for endangered species, Morus boninensis Koidz., to establish conservation program. Mol Ecol Notes 5:398–400

    Article  CAS  Google Scholar 

  • Tani N, Yoshimaru H, Kawahara T, Hoshi Y, Nobushima F, Yasui T (2006) Determination of the genetic structure of remnant Morus boninensis Koidz. trees to establish a conservation program on the Bonin Islands, Japan. BMC Ecol 6(1):14. https://doi.org/10.1186/1472-6785-6-14doi: 10.1186/1472-6785-6-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Thiers B (2018) Index herbariorum: a global directory of public herbaria and associated staff. new york botanical garden's virtual herbarium. https://sweetgum.nybg.org/science/ih/. Accessed 27 Feb 2018

  • Tippery NP, Les DH (2011) Phylogenetic relationships and morphological evolution in Nymphoides (Menyanthaceae). Syst Bot 36(4):1101–1113

    Article  Google Scholar 

  • Tippery NP, Les DH, Padgett DJ, Jacobs SW (2008) Generic circumscription in Menyanthaceae: a phylogenetic evaluation. Syst Bot 33(3):598–612

    Article  Google Scholar 

  • Tippery NP, Sears NL, Zentner AB, Sivadas V (2018) Evidence for allopolyploid speciation in Nymphoides (Menyanthaceae). Syst Bot 43(1):117–129

    Article  Google Scholar 

  • Tsuda Y, Semerikov V, Sebastiani F, Vendramin GG, Lascoux M (2017) Multispecies genetic structure and hybridization in the Betula genus across Eurasia. Mol Ecol 26(2):589–605

    Article  PubMed  Google Scholar 

  • Uesugi R, Tani N, Goka K, Nishihiro J, Tsumura Y, Washitani I (2005) Isolation and characterization of highly polymorphic microsatellites in the aquatic plant, Nymphoides peltata (Menyanthaceae). Mol Ecol Resour 5(2):343–345

    Article  CAS  Google Scholar 

  • Uesugi R, Nishihiro J, Tsumura Y, Washitani I (2007) Restoration of genetic diversity from soil seed banks in a threatened aquatic plant Nymphoides peltata. Conserv Genet 8(1):111–121

    Article  Google Scholar 

  • Wang Y, Wang QF, Guo YH, Barrett SC (2005) Reproductive consequences of interactions between clonal growth and sexual reproduction in Nymphoides peltata: a distylous aquatic plant. New Phytol 165(1):329–335. https://doi.org/10.1111/j.1469-8137.2004.01234.x

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The research was funded by Consejo Nacional de Ciencia y Tecnologia (CONACyT) through the Laboratorio Nacional de Identificación y Caracterización Vegetal (LaniVeg) research grants during 2016 (No. 272045) and 2017 (No. 281478). The first author holds a postgraduate fellowship from CONACyT (No. 590633). Laboratory work was carried out in Molecular and Plant Systematic Laboratory at the University of Guadalajara. We thank Noemi Cobian and Pilar Zamora for assistance with the molecular analysis, Alex Villalvazo for assistance with the chromosomes count, Marcelo Silva, Roberto Vizcaya, Gerardo Guerrero, and Carlos Varela (in memoriam) for field assistance. We appreciate the comments of two anonymous reviewers.

Author information

Authors and Affiliations

  1. Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Avenida de Las Ciencias, s/n, 76230, Santiago de Querétaro, QRO, Mexico

    Tatiana Lobato-de Magalhães & Mahinda Martínez

  2. Laboratorio de Sistemática Vegetal Molecular, Universidad de Guadalajara, Km. 15.5 Carretera Guadalajara-Nogales, 45110, Zapopan, Jalisco, Mexico

    Dánae Cabrera-Toledo

Authors
  1. Tatiana Lobato-de Magalhães
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dánae Cabrera-Toledo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mahinda Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceived and designed the experiments: TLdM DCT MM. Performed the experiments: TLdM. Analyzed the data: TLdM DCT. Wrote the paper: TLdM. Reviewed drafts of the paper: DCT MM.

Corresponding author

Correspondence to Mahinda Martínez.

Additional information

Handling Editor: Koji TOJO.

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lobato-de Magalhães, T., Cabrera-Toledo, D. & Martínez, M. Microsatellite loci transferability and genetic diversity of the aquatic plant Nymphoides fallax Ornduff (Menyanthaceae), endemic to the Mexican and Guatemalan highlands. Limnology 20, 233–241 (2019). https://doi.org/10.1007/s10201-019-00571-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10201-019-00571-5

Keywords

Search

Navigation