Skip to main content

Phenotypic variability and genetic differentiation in continental and island populations of Colobanthus quitensis (Caryophyllaceae: Antarctic pearlwort)

An Erratum to this article was published on 01 September 2017

This article has been updated

Abstract

Colobanthus quitensis (Antarctic pearlwort) is one of the only two native vascular plants to inhabit the extreme environmental conditions of Antarctica. Colobanthus quitensis has a wide geographic distribution, both in latitude and altitude, and always inhabits extreme environments. This makes it crucial for understanding environmental tolerance mechanisms, and a useful model for studies regarding genetic diversity and intraspecific morphology. Several morphological and molecular descriptors were applied to C. quitensis populations, constituting the first study of its kind in these species. We postulated that morphological variability is strongly linked to geographic distribution, and that this is manifested in external morphological characteristics and genetic structure. A large intra- and interpopulational morphological variability was verified. Both morphological variability and genetics made it possible to form two separate groups between continental and Antarctic island populations. The genetic diversity was high to moderate with the least amount of diversity towards the north. The genetic structure was high, and the gene flow between populations was low. The correlation between morphological, genetic, geographic and altitudinal distances permits the proposal of an isolation by distance model that can be used between populations with high Bio-geographical influence. Understanding what factors lead to local or colonization adaptation, and determining the morphological variations and genetic differentiation in populations of C. quitensis, is vital for the understanding of the evolutionary history that has contributed to the success of the establishment of this species in an environment as extreme as Antarctica. Additionally, this study demonstrates the usefulness of the combined use of morpho-physiological and molecular markers for variability and diversity studies.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Change history

  • 01 September 2017

    An erratum to this article has been published.

References

  • Acuña-Rodríguez I, Osses R, Cortés-Vásquez J, Torres C, Molina-Montenegro MA (2014) Genetic diversity of Colobanthus quitensis across the Drake Passage. Plant Genet Resour 12:147–150. doi:10.1017/S1479262113000270

    Article  Google Scholar 

  • Alberdi M, Bravo LA, Gutierrez A, Gidekel M, Corcuera LJ (2002) Ecophysiology of Antarctic vascular plants. Physiol Plant 115:479–486. doi:10.1034/j.1399-3054.2002.1150401.x

    CAS  Article  PubMed  Google Scholar 

  • Alexander JM, Edwards PJ (2010) Limits to the niche and range margins of alien species. Oikos 37:1377–1386. doi:10.1111/j.1600-0706.2009.17977.x

    Article  Google Scholar 

  • Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetic. Nat Rev Genet 11:679–709. doi:10.1038/nrg2844

    Article  Google Scholar 

  • Androsiuk P, Chwedorzeswska K, Szandar K, Giełwanowska I (2015) Genetic variability of Colobanthus quitensis from King George Island (Antarctica). Pol Polar Res 36:281–295. doi:10.1515/popore-2015-0017

    Google Scholar 

  • Archibald JK, Crawford DJ, Santos-Guerra A, Mort ME (2006) The utility of automated analysis of inter-simple sequence repeat (ISSR) loci for resolving relationships in the canary island species of tolpis. Am J Bot 93:1154–1162. doi:10.3732/ajb.93.8.1154

    CAS  Article  PubMed  Google Scholar 

  • Bascuñán-Godoy L, Uribe E, Zúñiga-Feest A, Corcuera LJ, Bravo LA (2006) Low temperatura regulates sucrose-phosphate synthase activity in Colobanthus quitensis (Kunth) Bartl. By decreasing its sensitivity to Pi and increased activation by glucose-6-phosphate. Polar Biol 29:1011–1017. doi:10.1007/s00300-006-0144-3

    Article  Google Scholar 

  • Bascuñán-Godoy L, García-Plazaola J, Bravo LA, Corcuera LJ (2010) Leaf functional and micro-morphological photoprotective attributes in two ecotypes of Colobanthus quitensis from the Andes and Maritime Antarctic. Polar Biol 33:885–896. doi:10.1007/s00300-010-0765-4

    Article  Google Scholar 

  • Bascuñán-Godoy L, Sanhueza C, Cuba-Díaz M, Zúñiga GE, Corcuera LJ, Bravo LA (2012) Cold acclimation limits low temperature induced photoinhibition by promoting a higher photochemical quantum yield and a more effective PSII restoration in darkness in the Antarctic rather than the Andean ecotype of Colobanthus quitensis Kunth Bartl (Cariophyllaceae). BMC Plant Biol 12:114. doi:10.1186/1471-2229-12-114

    Article  PubMed  PubMed Central  Google Scholar 

  • Beyer L, Bölter M, Seppelt RD (2000) Nutrient and thermal regime, microbial biomass and vegetation of Antarctic soils in the Windmill Islands Region of east Antarctica (Wilkes Land). Arct Antarct Alp Res 32:30–39. doi:10.2307/1552407

    Article  Google Scholar 

  • Bokhorst S, Huiskes AHL, Convey P, Sinclair BJ, Lebouvier M, Van de Vijver B, Wall DH (2011) Microclimate impacts of passive warming methods in Antarctica: implications for climate change studies. Polar Biol 34:1421–1435. doi:10.1007/s00300-011-0997-y

    Article  Google Scholar 

  • Bradshaw AD, Hardwick K (1989) Evolution and stress genotypic and phenotypic components. Biol J Linn Soc 37:137–155. doi:10.1111/j.1095-8312.1989.tb02099.x

    Article  Google Scholar 

  • Bravo LA, Saavedra-Mella FA, Vera F, Guerra A, Cavieres LA, Ivanov AL, Huner NP, Corcuera LJ (2007) Effect of cold acclimation on the photosynthetic performance of two ecotypes of Colobanthus quitensis (Kunth) Bartl. J Exp Bot 58:3581–3590

    CAS  Article  PubMed  Google Scholar 

  • Carlquist S (1974) Island biology. Columbia University Press, New York. doi:10.5962/bhl.title.63768

    Book  Google Scholar 

  • Convey P (1996) Reproduction of Antarctic flowering plants. Antarct Sci 8:127–134. doi:10.1017/S0954102096000193

    Google Scholar 

  • Convey P (2010) Terrestrial biodiversity in Antarctica: recent advances and future challenges. Polar Sci 4:135–147. doi:10.1016/j.polar.2010.03.003

    Article  Google Scholar 

  • Convey P (2011) Antarctic terrestrial biodiversity in a changing world. Polar Biol 34:1629–1641. doi:10.1007/s00300-011-1068-0

    Article  Google Scholar 

  • Convey P (2013) Antarctic ecosystems. Encyclopedia of biodiversity. Elsevier, San Diego. doi:10.1016/b978-0-12-384719-5.00264-1

    Google Scholar 

  • Convey P, Gibson JAE, Hillenbrand CD, Hodgson DA, Pugh PJA, Smellie JL, Stevens ML (2008) Antarctic terrestrial life—challenging the history of the frozen continent? Biol Rev 83:103–117. doi:10.1111/j.1469-185x.2008.00034.x

    Article  PubMed  Google Scholar 

  • Convey P, Bindschadler RA, Di Prisco G, Fahrbach E, Gutt J, Hodgson DA, Mayewski CP (2009) Antarctic climate change and the environment. Antarct Sci 21:541–563. doi:10.1017/s0954102009990642

    Article  Google Scholar 

  • Convey P, Hopkins DW, Roberts SJ, Tyler AN (2011) Global southern limit for flowering plants and moss peat accumulation. Polar Res 30:8929. doi:10.3402/polar.v30i0.8929

    Article  Google Scholar 

  • Convey P, Chown SL, Clarke A, Barnes DKA, Cummings V, Ducklow H, Frati F, Green TGA, Gordon S, Griffiths H, Howard-Williams C, Huiskes AHL, Laybourn-Parry J, Lyons B, McMinn A, Peck LS, Quesada A, Schiaparelli S, Wall D (2014) The spatial structure of Antarctic biodiversity. Ecol Monogr 84:203244. doi:10.1890/12-2216.1

    Article  Google Scholar 

  • Cordero C (2012) Caracterización y análisis de variabilidad moroflógica y genética en poblaciones de Colobanthus quitensis (KUNTH) Bartl. (Caryophylaceae) [Undergraduate thesis. Plant Biotechnology Eng.]. Universidad de Concepción, Chile

  • Cuba-Díaz M (2011) El clavelito antártico y los mecanismos que lo protegen del frio polar. Bol Antárt Chil 30:8–9

    Google Scholar 

  • Cuba-Díaz M, Cid K, Navarrete A, Retamal C, Bravo LA (2011). Cold and photoperiod regulated expression of sucrose phosphate synthase (SPS) favors sucrose accumulation in Colobanthus quitensis during the Antarctic summer. In: Bravo LA, Leppe M (eds) VIII Reunión Chilena de Investigación Antártica Libro Resumen, pp 98–102. http://www.inach.cl/wp-content/uploads/2011/08. Accessed 30 Oct 2011

  • Cuba-Díaz M, Acuña D, Klagges M, Dollenz O, Cordero C (2013) Colobanthus quitensis de la Marisma, una nueva población para la colección genética de la especie. In: Leppe M, Molina-Montenegro M, González M, MacDonell S, Lavín P, Oses R, Gallardo J, Rivadeneira M, Arata J, Canales R (eds) Avances en Ciencia Antártica Latinoamericana. VII Congreso Latinoamericano de Ciencia Antártica, pp 436–439

  • Dewoody J, Trewin H, Taylor G (2015) Genetic and morphological differentiation in Populus nigra L.: isolation by colonization or isolation by adaptation? Mol Ecol 24:2641–2655. doi:10.1111/mec.13192

    Article  PubMed  PubMed Central  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50

    CAS  Article  Google Scholar 

  • Gianoli E, Zuñiga-Feest A, Reyes-Diaz M, Bravo LA, Corcuera LJ (2004) Ecotypic differentiation in morphology and cold resistance in populations of Colobanthus quitensis from the Andes of central Chile and the maritime Antarctic. Arct Antarct Alp Res 36:470–475. doi:10.1657/1523-0430(2004)036[0484:edimac]2.0.co;2

    Article  Google Scholar 

  • Haider S, Alexander J, Kueffer C (2011) Elevational distribution limits of non-native species: combining observational and experimental evidence. Plant Ecol Divers 4:363–371. doi:10.1080/17550874.2011.637973

    Article  Google Scholar 

  • Hamrick JL, Godt JW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc B 351:1291–1298. doi:10.1098/rstb.1996.0112

    Article  Google Scholar 

  • Hartl DL, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer Associates, Inc., Sunderland

    Google Scholar 

  • Jelling AJ, Usher MB, Leech RM (1983) Variation in the chloroplast to cell area index in Deschampsia antarctica along a 16° latitudinal gradient. Brit Antarct Surv B 61:13–20

    Google Scholar 

  • Kellman-Sopyla W, Giełwanowska I (2015) Germination capacity of five polar Caryophyllaceae and Poaceae species under different temperature conditions. Polar Biol 38:1753–1765. doi:10.1007/s00300-015-1740-x

    Article  Google Scholar 

  • Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738. doi:10.1016/0040-5809(71)90033-5

    CAS  PubMed  PubMed Central  Google Scholar 

  • Klagges M, Cordero C, Cuba-Díaz M (2013) Las poblaciones de Colobanthus quitensis presentan diferenciaciones morfo-fisiológicas que podrían evidenciar la formación de ecotipo en su hábitat. In: Leppe M, Molina-Montenegro M, González M, MacDonell S, Lavín P, Oses R, Gallardo J, Rivadeneira M, Arata J, Canales R. eds. Avances en Ciencia Antártica Latinoamericana. VII Congreso Latinoamericano de Ciencia Antártica

  • Körner CH (2003) Alpine plant life. Functional plant ecology of high mountain ecosystems. Springer, Berlin

    Google Scholar 

  • Kremer A, Kleinschmit J, Cottrell J, Cundall EP, Deans JD, Ducousso A, König AO, Lowe AJ, Munro RC, Petit RJ, Stephane BR (2002) Is there a correlation between chloroplastic and nuclear divergence, or what are the roles of history and selection on genetic diversity in European oaks? For Ecol Manag 156:75–87. doi:10.1016/s0378-1127(01)00635-1

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Manzur MI (2006) La diversidad genética, biodiversidad de Chile, patrimonio y desafíos. Comisión Nacional del Medio Ambiente de Chile

  • McGraw JB, Day TA (1997) Size and characteristics of a natural seed bank in Antarctic. Arct Antarct Alp Res 29:213–216. doi:10.2307/1552048

    Article  Google Scholar 

  • Miller MP (1997) Tools for population genetic analyses (TFPGA). Northern. Arizona University, Flagstaff. http://www.ccg.unam.mx/~vinuesa/tlem09/docs/TFPGADOC.PDF

  • Molina-Montenegro MA, Quiroz CL, Torres-Díaz C, Atala C (2011) Functional differences in response to drought in the invasive Taraxacum officinale from native and introduced alpine habitat ranges. Plant Ecol Div 4:37–44. doi:10.1080/17550874.2011.577459

    Article  Google Scholar 

  • Molina-Montenegro MA, Torres-Díaz C, Carrasco-Urra F, González-Silvestre LA, Gianoli E (2012) Phenotypic plasticity in two antarctic populations of Colobanthus quitensis (Caryophyllaceae) under a simulated global change scenario. Gayana Bot 69:152–160

    Article  Google Scholar 

  • Monty A, Mahy G (2009) Climal differentiation during invasion: senecio inaequidens (Asteraceae) along altitudinal gradients in Europe. Oecologia 159:305–315. doi:10.1007/s00442-008-1228-2

    Article  PubMed  Google Scholar 

  • Moore DM (1970) Studies in Colobanthus quitensis (Kunth) Bartl. and Deschampsia antarctica Desv. II. Taxonomy, distribution and relationships. Br Antarct Surv B 23:63–80

    Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497. doi:10.1111/j.1399-3054.1962.tb08052.x

    CAS  Article  Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292. doi:10.1086/282771

    Article  Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323. doi:10.1073/pnas.70.12.3321

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273. doi:10.1073/pnas.76.10.5269

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Parnikoza I, Kozeretska I, Kunakh V (2011) Vascular plants of the maritime Antarctic: origin and adaptation. Am J Plant Sci 2:381–395. doi:10.4236/ajps.2011.23044

    Article  Google Scholar 

  • Piña-Escutia JL, Vences-Contreras C, Gutiérrez-Martínez G, Vásquez-García M, Arzate-Fernández A (2010) Morphological and molecular characterization of nine botanical varieties of Tigridia pavonia (L.f) DC. Agrociencia 44:147–158

    Google Scholar 

  • Poulin E, González-Wevar C, Díaz A, Gérard K, Hüne M (2014) Divergence between Antarctic and South American marine invertebrates: what molecular biology tells us about Scotia Arc geodynamics and the intensification of the Antarctic Circumpolar Current. Glob Plan Chang 123:392–399. doi:10.1016/j.gloplacha.2014.07.017

    Article  Google Scholar 

  • Romero M, Casanova A, Iturra G, Reyes A, Montenegro G, Alberdi M (1999) Leaf anatomy of Deschampsia antarctica (Poaceae) from the maritime Antarctic and its plastic response to changes in growth conditions. Rev Chil Hist Nat 72:411–425

    Google Scholar 

  • Royer DL, McElwain JC, Adams JM, Wilf P (2008) Sensitivity of leaf size and shape to climate within Acer rubrum and Quercus kelloggii. New Phytol 179:808–817. doi:10.1111/j.1469-8137.2008.02496.x

    Article  PubMed  Google Scholar 

  • Ruhland CT, Day TA (2001) Size and longevity of seed banks in Antarctica and the influence of ultraviolet-B radiation on survivorship, growth and pigment concentrations of Colobanthus quitensis seedlings. Environ Exp Bot 45:143–154. doi:10.1016/s0098-8472(00)00089-7

    CAS  Article  PubMed  Google Scholar 

  • Ruiz E, Balboa K, Negritto M, Baeza C, Fuentes G, Briceño V (2010) Genetic and morphological variation and population structure in Alstroemeria hookeri subsp. hookeri (Alstroemeriaceae), endemic to Chile. Rev Chil Hist Nat 83:605–616. doi:10.4067/s0716-078x2010000400013

    Article  Google Scholar 

  • Salinas N, Armijos V, Jiménez P, Proaño K (2011) Caracterización y estudio de la diversidad genética del piñón (Jatropha curcas) mediantes el uso de marcadores moleculares. Ciencia 14:31–40

    Google Scholar 

  • Sanhueza C, Vallejos V, Cavieres LA, Sáez P, Bravo LA, Corcuera LJ (2017) Growing temperature affects seed germination of the antarctic plant Colobanthus quitensis (Kunth) Bartl (Caryophyllaceae). Polar Biol 40:449–455. doi:10.1007/s00300-016-1972-4

  • Shannon CE, Weaver W (1949) The mathematical theory of communication. The University of Illinois Press, Urbana

    Google Scholar 

  • Smith RIL (2003) The enigma of Colobanthus quitensis and Deschampsia antartica. In: Huiskes AHL, Gieskes WWC, Rozema J, Schoro RML, van der Vies SM, Wolff WJ (eds) Antarctic biology in a global context, pp 34–239

  • Sneath PHA, Sokal RR (1973) Numerical taxonomy: the principles and practice of numerical classification. W.H Freeman Company, San Francisco. doi:10.2307/2412767

    Google Scholar 

  • Suma N, Srimathi P (2014) Influence of water flotation technique on seed and seedling quality characteristics of Sesamum indicum. IOSR J Agric Vet Sci 7:51–53. doi:10.9790/2380-07825153

    Article  Google Scholar 

  • Westergaard KB, Alsos IG, Popp M, Engelskjøn T, Flatberg KI, Brochmann C (2011) Glacial survival may matter after all: nunatak signatures in the rare European populations of two west-arctic species. Mol Ecol 20:376–393. doi:10.1111/j.1365-294x.2010.04928.x

    Article  PubMed  Google Scholar 

  • Wirtz N, Printzen C, Thorsten Lumbsch H (2012) Using haplotype networks, estimation of gene flow and phenotypic characters to understand species delimitation in fungi of a predominantly Antarctic Usnea group (Ascomycota, Parmeliaceae). Org Divers Evol 12:17–37. doi:10.1007/s13127-011-0066-y

    Article  Google Scholar 

  • Xiong FS, Day TA (2001) Effect of solar ultraviolet-B radiation during springtime ozone depletion on photosynthesis and biomass production of antarctic vascular plants. Plant Physiol 125:738–751. doi:10.1104/pp.125.2.738

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Yeh FC, Yang RC, Boyle T (1999) PopGene Microsoft windows-based freeware for population genetic analysis. University of Alberta, Edmonton. http://www.ualberta.ca/fyeh/popgene.download.html. Accessed 12 Jan 2014

  • Zúñiga-Feest A, Bascuñán-Godoy L, Reyes-Díaz M, Bravo LA, Corcuera LJ (2009) Is survival after ice encasement related with sugar distribution in organs of the Antarctic plants Deschampsia antarctica Desv. (Poaceae) and Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae). Polar Biol 32:583–591. doi:10.1007/s00300-008-0553-6

    Article  Google Scholar 

Download references

Acknowledgements

This research was undertaken with financing from the Chilean Antarctic Institute through the INACH RT_03-09 and INACH RG_02-13 projects. We wish to thank the Chilean Antarctic Institute, the Chilean Air Force, Chilean Navy and Henryk Arctowski Polish Antarctic Station for the logistical support during the on-site activities. The authors would like to thank Dieter Piepenburg, Peter Convey, and the other two reviewers, for their thorough analysis that has led to a significant improvement in this work. Finally, we wish to thank the editors at International Journal Revisions for their contributions and comprehensive English language revision.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marely Cuba-Díaz.

Ethics declarations

Conflicts of interest

The authors confirm no conflicts of interest.

Additional information

An erratum to this article is available at https://doi.org/10.1007/s00300-017-2188-y.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 29 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Cuba-Díaz, M., Klagges, M., Fuentes-Lillo, E. et al. Phenotypic variability and genetic differentiation in continental and island populations of Colobanthus quitensis (Caryophyllaceae: Antarctic pearlwort). Polar Biol 40, 2397–2409 (2017). https://doi.org/10.1007/s00300-017-2152-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-017-2152-x

Keywords

  • Antarctic
  • Ecotypes
  • Genetic structure
  • Genetic variability
  • Morphological diversity
  • Antarctic pearlwort