Abstract
Understanding in what way cold-adapted mountain species have responded to historical climatic fluctuations in southern European refugia and investigating the genetic variation of endemic species is fundamental to predict their survival under contemporary global climate change. Veronica aragonensis (Plantaginaceae) is a tetraploid species endemic to the Iberian Peninsula that survived the climatic oscillations of the Quaternary. This species is adapted to cold environments and is included in several regional Red Lists due to its small and disjunct distribution range in high-mountain habitats (Pyrenees, Pre-Pyrenees and Baetic System). With the aim of deciphering the phylogeographical processes that underlie the presently disjunct distribution pattern of V. aragonensis and to evaluate its conservation status, we used 9 microsatellite loci to genotype 324 individuals from 12 populations representing the three disjunct areas where the species is distributed. Our results suggest that range fragmentation of an ancient continuous distribution of V. aragonensis—particularly in the low elevation mountain ranges located between the Pyrenees and the Baetic System—during the Last Glacial Maximum is the most plausible explanation for the disjunct distribution pattern of the species. Lastly, the intraspecific genetic patterns are discussed to predict how this endemic species can be affected by global climate warming. Based on the genetic data obtained here, an appropriate evaluation of the conservation status of V. aragonensis and some management strategies are provided.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abellán P, Svenning JC (2014) Refugia within refugia–patterns in endemism and genetic divergence are linked to Late Quaternary climate stability in the Iberian Peninsula. Biol J Linn Soc 113:13–28. https://doi.org/10.1111/bij.12309
Ahrens CW, James EA (2015) Range-wide genetic analysis reveals limited structure and suggests asexual patterns in the rare forb Senecio macrocarpus. Biol J Linn Soc 115:256–269. https://doi.org/10.1111/bij.12512
Alarcón M, Vargas P, Sáez L, Molero J, Aldasoro JJ (2012) Genetic diversity of mountain plants: two migration episodes of Mediterranean Erodium (Geraniaceae). Mol Phylogenet Evol 63:866–876. https://doi.org/10.1016/j.ympev.2012.02.031
Alcántara de la Fuente M, Goñi D, Guzman D, Puente J (2007) Catálogo de especies amenazadas en Aragon: Flora. Gobierno de Aragon. Departamento de Medio Ambiente, Huesca
Arribas O (2004) Fauna y paisaje de los Pirineos en la Era Glaciar. Lynx Edicions, Barcelona
Badal García E, Martínez Varea CM (2018) Different parts of the same plants. Charcoals and seeds from Cova de les Cendres (Alicante, Spain). Quat Int 463:391–400. https://doi.org/10.1016/j.quaint.2016.12.020
Buira A, Aedo C, Medina L (2017) Spatial patterns of the Iberian and Balearic endemic vascular flora. Biodivers Conserv 26:479–508. https://doi.org/10.1007/s10531-016-1254-z
Cabezudo B, Talavera S, Blanca G, Salazar C, Cueto M, Valdés B, Hernández Bermejo JE, Herrera CM, Rodríguez Hiraldo C, Navas D (2005) Lista roja de la flora vascular de Andalucía. Junta de Andalucía, Consejería de Medio Ambiente
Calvet M (2004) The Quaternary glaciation of the pyrenees. In: Developments in quaternary sciences, vol 2. Elsevier, Netherlands, pp 119–128
Catalán P, Segarra-Moragues JG, Palop-Esteban M, Moreno JC, González-Candelas F (2006) A Bayesian approach for discriminating among alternative inheritance hypotheses in plant polyploids: the allotetraploid origin of genus Borderea (Dioscoreaceae). Genetics 172:1939–1953. https://doi.org/10.1534/genetics.105.042788
Charrier O, Dupont P, Pornon A, Escaravage N (2014) Microsatellite marker analysis reveals the complex phylogeographic history of Rhododendron ferrugineum (Ericaceae) in the Pyrenees. PLoS ONE 9:e92976. https://doi.org/10.1371/journal.pone.0092976
Clark LV, Schreier AD (2017) Resolving microsatellite genotype ambiguity in populations of allopolyploid and diploidized autopolyploid organisms using negative correlations between allelic variables. Mol Ecol Resour 17:1090–1103. https://doi.org/10.1111/1755-0998.12639
Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843. https://doi.org/10.1111/j.1365-294X.2006.02994.x
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19:11–15
Engler R, Randin CF, Thuiller W, Dullinger S, Zimmermann NE, Araújo MB, Pearman PB, Le Lay G, Piedallu C, Albert C, Choler P, Coldea G, De Lamo X, Dirnböck T, Gégout JC, Gómez-García D, Grytnes JA, Heegaard E, HØIstad F, NoguÉS-Bravo D, Normand S, Puşcaş M, Sebastià MT, Stanisci A, Theurillat JP, Trivedi MR, Vittoz P, Guisan A (2011) 21st century climate change threatens mountain flora unequally across Europe. Global Change Biol 17:2330–2341. https://doi.org/10.1111/j.1365-2486.2010.02393.x
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
García-Cervigón AI, Olano-Mendoza JM, Gozalbo ME, Camarero-Martínez JJ (2012) Arboreal and prostrate conifers coexisting in Mediterranean high mountains differ in their climatic responses. Dendrochronologia 4:279–286. https://doi.org/10.1016/j.dendro.2012.02.004
García-Ruíz JM, Valero-Garcés BL, Martí-Bono C, González-Sampériz P (2003) Asynchroneity of maximum glacier advances in the central Spanish Pyrenees. J Quat Sci 18:61–72. https://doi.org/10.1002/jqs.715
Gentili R, Baroni C, Caccianiga M, Armiraglio S, Ghiani A, Citterio S (2015) Potential warm-stage microrefugia for alpine plants: feedback between geomorphological and biological processes. Ecol Complex 21:87–99. https://doi.org/10.1016/j.ecocom.2014.11.006
Gómez A, Lunt DH (2006) Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. In: Weiss S, Ferrand N (eds) Phylogeography of Southern European refugia. Springer, Netherlands, Dordrecht, pp 155–188
González-Sampériz P, Leroy SAG, Carrión J et al (2010) Steppes, savannahs, forests and phytodiversity reservoirs during the Pleistocene in the Iberian Peninsula. Rev Palaeobot Palynol 162:427–457. https://doi.org/10.1016/j.revpalbo.2010.03.009
Goudet J (2003) FSTAT (ver. 2.9.4), a program to estimate and test population genetics parameters. Available from http://www.unil.ch/izea/softwares/fstat.html
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620. https://doi.org/10.1046/j.1471-8286.2002.00305.x
Hardy OJ, Charbonnel N, Fréville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482
Herben T, Suda J, Klimešová J (2017) Polyploid species rely on vegetative reproduction more than diploids: a re-examination of the old hypothesis. Ann Bot 120:341–349. https://doi.org/10.1093/aob/mcx009
Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913
Holderegger R, Thiel-Egenter C (2009) A discussion of different types of glacial refugia used in mountain biogeography and phylogeography. J Biogeogr 36:476–480. https://doi.org/10.1111/j.1365-2699.2008.02027.x
Huc S (2010) Éboulis mobiles et marqueurs biogéographiques: le cas de la haute montagne des pyrénées orientales. Université de Perpignan, Géographie
Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914. https://doi.org/10.1111/j.1558-5646.1999.tb04571.x
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. https://doi.org/10.1093/bioinformatics/btm233
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
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. https://doi.org/10.7717/peerj.281
Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: An R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788. https://doi.org/10.1111/2041-210X.12067
Körner C (2003) Alpine plant life: funcional plant ecology of high mountain ecosystem, 2nd edn. Springer, Berlin, p 344
Kropf M, Comes HP, Kadereit JW (2006) Long-distance dispersal vs vicariance: the origin and genetic diversity of alpine plants in the Spanish Sierra Nevada. New Phytol 172:169–184. https://doi.org/10.1111/j.1469-8137.2006.01795.x
Loidi J, Biurrun I, García-mijangos I, García- G, Herrera M, Campos JA (2017) The high mountain flora and vegetation. In: Loidi J (ed) The vegetation of the Iberian Peninsula. Springer, Cham, pp 433–458
Martínez-Ortega MM, Delgado L, Albach DC, Elena-Rosselló JA, Rico E (2004) Species boundaries and phylogeographic patterns in cryptic taxa inferred from AFLP Markers: Veronica subgen. Pentasepalae (Scrophulariaceae) in the western mediterranean. Syst Bot 29:965–986. https://doi.org/10.1600/0363644042451071
Martínez-Ortega MM, Sánchez-Agudo JA, Rico E (2009) Veronica L. In: Benedí C, Rico E, Güemes J, Herrero A (eds) Flora iberica: plantas vasculares de la Península Ibérica e Islas Baleares, vol. XIII. Plantaginaceae-Scrophulariaceae, pp 360–434
Médail F, Baumel A (2018) Using phylogeography to define conservation priorities: the case of narrow endemic plants in the Mediterranean Basin hotspot. Biol Conserv 224:258–266. https://doi.org/10.1016/j.biocon.2018.05.028
Meudt H, Rojas-Andrés BM, Prebble JM, Low E, Garnock-Jones PJ, Albach DC (2015) Is genome downsizing associated with diversification in polyploid lineages of Veronica? Bot J Linn Soc 178:243–266. https://doi.org/10.1111/boj.12276
Muñoz-Centeno LM, Albach DC, Sanchez-Agudo JA, Martinez-Ortega MM (2006) Systematic significance of seed morphology in Veronica (Plantaginaceae): a phylogenetic perspective. Ann Bot 98:335–350. https://doi.org/10.1093/aob/mcl120
Navarro FB, Lorite J, Jiménez MN (2003) Estado de conservación y propuesta de protección de Eryngium huteri Porta, Pulsatilla alpina (L.) Delarbre y Saxifraga longifolia Lapeyr en Andalucía (España). Ecología 17:153–160
Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19:153–170
Padilla-García N, Malvar-ferreras T, Lambourdière J, Martínez-Ortega MM, Machon N (2018a) Microsatellite marker development for the tetraploid Veronica aragonensis (Plantaginaceae) using generation sequencing and high-resolution melting analyses. Appl Plant Sci 6:1–6. https://doi.org/10.1002/aps3.1154
Padilla-García N, Rojas-Andrés BM, López-González N, Castro M, Castro S, Loureiro J, Albach DC, Machon N, Martínez-Ortega MM (2018b) The challenge of species delimitation in the diploid-polyploid complex Veronica subsection Pentasepalae. Mol Phylogenet Evol 119:196–209. https://doi.org/10.1016/j.ympev.2017.11.007
Pauli H, Gottfried M, Dullinger S, Abdaladze O, Akhalkatsi M, Benito Alonso JL, Coldea G, Dick J, Erschbamer B, Fernández Calzado R, Ghosn D, Holten JI, Kanka R, Kazakis G, Kollár J, Larsson P, Moiseev P, Moiseev D, Molau U, Molero Mesa J, Nagy L, Pelino G, Puscas M, Rossi G, Stanisci A, Syverhuset AO, Theurillat J-P, Tomaselli M, Unterluggauer P, Villar L, Vittoz P, Grabherr G (2012) Recent plant diversity changes on Europe’s mountain summits. Science 336:353–355. https://doi.org/10.1126/science.1219033
Pauls SU, Nowak C, Bálint M, Pfenninger M (2013) The impact of global climate change on genetic diversity within populations and species. Mol Ecol 22:925–946. https://doi.org/10.1111/mec.12152
Peakall ROD, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
Peredo EL, Revilla MÁ, Jiménez-Alfaro B, Bueno Á, Prieto JAF, Abbott RJ (2009) Historical biogeography of a disjunctly distributed, Spanish alpine plant, Senecio boissieri (Asteraceae). Taxon 58:883–892. https://doi.org/10.1002/tax.583016
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rojas-Andrés BM, Padilla-García N, de Pedro M, López-González N, Delgado L, Albach DC, Castro M, Castro S, Loureiro J, Martínez-Ortega MM (2020) Environmental differences are correlated with the distribution pattern of cytotypes in Veronica subsection Pentasepalae at a broad scale. Ann Bot 125:471–484. https://doi.org/10.1093/aob/mcz182
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. https://doi.org/10.1046/j.1471-8286.2003.00566.x
Sanz M, Schönswetter P, Vallès J, Vilatersana R (2017) Glacial survival in and recent long-distance dispersal to the Iberian Mountains: the phylogeographic history of Artemisia umbelliformis (Asteraceae). Bot J Linn Soc 183:587–599. https://doi.org/10.1093/botlinnean/box002
Scheerer H (1937) Experimentelle und zytologische Untersuchungen innerhalb der Veronica - gruppe Pentasepala. Flora 131:287–323. https://doi.org/10.1016/S0367-1615(17)32983-X
Schinkel C, Kirchheimer B, Dellinger AS, Klatt S, Winkler M, Dullinger S, Hörandl E (2016) Correlations of polyploidy and apomixis with elevation and associated environmental gradients in an alpine plant. AoB Plants 8:plw064. https://doi.org/10.1093/aobpla/plw064
Schönswetter P, Stehlik I, Holderegger R, Tribsch A (2005) Molecular evidence from glacial refugia of mountain plants in the European Alps. Mol Ecol 14:3547–3555. https://doi.org/10.1111/j.1365-294X.2005.02683.x
Segarra-Moragues JG, Palop-Esteban M, González-Candelas F, Catalán P (2007) Nunatak survival vs. tabula rasa in the Central Pyrenees: a study on the endemic plant species Borderea pyrenaica (Dioscoreaceae). J Biogeogr 34:1893–1906. https://doi.org/10.1111/j.1365-2699.2007.01740.x
Stehlik I, Schneller JJ, Bachmann K (2002) Immigration and in situ glacial survival of the low-alpine Erinus alpinus (Scrophulariaceae). Biol J Linn Soc 77:87–103. https://doi.org/10.1046/j.1095-8312.2002.00094.x
Stenberg P, Lundmark M, Saura A (2003) MLGsim: a program for detecting clones using a simulation approach. Mol Ecol Notes 3:329–331. https://doi.org/10.1046/j.1471-8286.2003.00408.x
Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504. https://doi.org/10.1093/bioinformatics/btn478
Theodoridis S, Patsiou TS, Randin C, Conti E (2018) Forecasting range shifts of a cold-adapted species under climate change: are genomic and ecological diversity within species crucial for future resilience? Ecography 41:1357–1369. https://doi.org/10.1111/ecog.03346
Vargas P (2003) Molecular evidence for multiple diversification patterns of alpine plants in Mediterranean Europe. Taxon 52:463–476. https://doi.org/10.2307/3647446
Wahlund S (1928) The combination of populations and the appearance of correlation examined from the standpoint of the study of heredity. Hereditas 11:65–106
Waples RS, Antao T, Luikart G (2014) Effects of overlapping generations on linkage disequilibrium estimates of effective population size. Genetics 197:769–780. https://doi.org/10.1534/genetics.114.164822
Acknowledgements
The authors thank all colleagues who participated in collecting material, especially to G. Sgarlata, M. Daoud, D. González, V. Di Donato, D. Gutiérrez, X. Giráldez, J. Peñas de Giles and A. Abad de Blas. We thank T. Malvar for technical support in the lab and J. Pedraza for computer assistance. We are deeply grateful to P. Tejero for his enthusiastic and motivating help with field sampling planning. Special thanks to J.F. Scheepens (University of Tübingen) and another anonymous reviewer for his/her critical comments on an earlier version of the manuscript. We thank INAGA and Junta de Andalucía for collection licences and all forest rangers that provided us field assistance in the Pyrenees and Sierra de la Sagra. This work was financed by the Spanish Ministerio de Economía y Competitividad (projects CGL2009-07555, CGL2012-32574 and Flora iberica) and the University of Salamanca (Ph.D. grant to NPG cofounded by Banco Santander). This work has made use of the resources of SCAYLE (Centro de Supercomputación de Castilla y León; www.scayle.es), funded by the “European Regional Development Fund (FEDER)”.
Author information
Authors and Affiliations
Contributions
Data collection were performed by NP-G, MMM-O, and NM. Lab work was performed by NP-G. Data analysis was performed by NP-G and JGS-M. The first draft of the manuscript was written by NP-G and JGS-M and MMM-O commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest and confirm that this work is original and has not been published elsewhere, nor it is currently under consideration for publication by another journal.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Padilla-García, N., Machon, N., Segarra-Moragues, J.G. et al. Surviving in southern refugia: the case of Veronica aragonensis, a rare endemic from the Iberian Peninsula. Alp Botany 131, 161–175 (2021). https://doi.org/10.1007/s00035-021-00258-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00035-021-00258-7