Abstract
Campanula fenestrellata subsp. fenestrellata and C. fenestrellata subsp. istriaca belong to the morphologically and phylogenetically well established amphi-Adriatic group Campanula ser. Garganicae. The two morphologically differentiated endemic taxa are distributed on the north-eastern Adriatic islands and coast. In order to study the relationships among C. fenestrellata s.l. populations and to gain insight into genetic basis of taxonomic separation established on morphology, we examined amplified fragment length polymorphisms (AFLPs) as well as nuclear and plastid DNA sequences (ITS and trnL–trnF). With the sequence data, no structure and no distinction between the two subspecies were observed. The AFLPs separated populations geographically and inferred high number of most likely clusters. The northern and the southernmost populations were assigned to uniform separate clusters indicating the longer isolation of respective populations, while the admixed populations were evident in the central area where the two taxa geographically overlap, indicating the presence of gene flow. Distinct fragmentation patterns and the existence of several temporally continuous microrefugia during the Quaternary climatic oscillations likely promoted strong genetic differentiation within the species range, while secondary postglacial contacts are reflected in observed admixture. Although the two taxa exhibited differences in ecological preferences, niche conservatism was detected. Overall, phylogeographic reconstruction of C. fenestrellata s.l. populations highlights the importance of microrefugia in shaping the intraspecific genetic variation as well as of melting-pot areas in rearranging such variation as a result of a more recent admixture.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Albarrán-Lara AL, Petit RJ, Kremer A, Caron H, Peñaloza-Ramírez JM, Gugger PF, Dávila-Aranda PD, Oyama K (2019) Low genetic differentiation between two morphologically and ecologically distinct giant-leaved Mexican oaks. Pl Syst Evol 305:89–101. https://doi.org/10.1007/s00606-018-1554-8
Aleksić JM, Geburek T (2010) Mitochondrial DNA reveals complex genetic structuring in a stenoendemic conifer Picea omorika [(Panč.) Purk.] caused by its long persistence within the refugial Balkan region. Pl Syst Evol 285:1–11. https://doi.org/10.1007/s00606-009-0250-0
Aleksić JM, Škondrić S, Lakušić D (2018) Comparative phylogeography of capitulate Campanula species from the Balkans, with description of a new species, C. daucoides. Pl Syst Evol 304:549–575. https://doi.org/10.1007/s00606-018-1490-7
Avise JC, Ball RM (1990) Principles of genealogical concordance in species concepts and biological taxonomy. In: Futuyma DJ, Antonovics J (eds) Oxford surveys in evolutionary biology. Oxford University Press, New York, pp 45–68
Bardy KE, Albach DC, Schneeweiss GM, Fischer MA, Schönswetter P (2010) Disentangling phylogeography, polyploid evolution and taxonomy of a woodland herb (Veronica chamaedrys group, Plantaginaceae s.l.) in southeastern Europe. Molec Phylogen Evol 57:771–786. https://doi.org/10.1016/j.ympev.2010.06.025
Bardy KE, Schönswetter P, Schneeweiss GM, Fischer MA, Albach DC (2011) Extensive gene flow blurs species boundaries among Veronica barrelieri, V. orchidea and V. spicata (Plantaginaceae) in southeastern Europe. Taxon 60:108–121
Bogdanović S, Brullo S, Rešetnik I, Lakušić D, Satovic Z, Liber Z (2014a) Campanula skanderbegii: molecular and morphological evidence of a new Campanula species (Campanulaceae) endemic to Albania. Syst Bot 39:1250–1260. https://doi.org/10.1600/036364414x682571
Bogdanović S, Brullo S, Rešetnik I, Šatović Z, Liber Z (2014b) Campanula teutana, a new isophyllous Campanula (Campanulaceae) from the Adriatic region. Phytotaxa 162:1–17. https://doi.org/10.11646/phytotaxa.162.1.1
Bogdanović S, Rešetnik I, Brullo S, Shuka L (2015) Campanula aureliana (Campanulaceae), a new species from Albania. Pl Syst Evol 301:1555–1567. https://doi.org/10.1007/s00606-014-1171-0
Bogdanović S, Rešetnik I, Jeričević M, Jeričević N, Brullo S (2019) Molecular and morphological survey on Campanula cremnophila (Campanulaceae), a new isophyllous species from Croatia. Pl Syst Evol 305:687–703. https://doi.org/10.1007/s00606-019-01599-x
Broennimann O, Fitzpatrick MC, Pearman PB, Petitpierre B, Pellissier L, Yoccoz NG, Thuiller W, Fortin M, Randin C, Zimmermann NE, Graham CH, Guisan A (2012) Measuring ecological niche overlap from occurrence and spatial environmental data. Global Ecol Biogeogr 21:481–497. https://doi.org/10.1111/j.1466-8238.2011.00698.x
Caković D, Stešević D, Schönswetter P, Frajman B (2015) How many taxa? Spatiotemporal evolution and taxonomy of Amphoricarpos (Asteraceae, Carduoideae) on the Balkan Peninsula. Organisms Diversity Distrib 15:429–445. https://doi.org/10.1007/s13127-015-0218-6
Carović-Stanko K, Liber Z, Politeo O, Strikić F, Kolak I, Milos M, Satovic Z (2011) Molecular and chemical characterization of the most widespread Ocimum species. Pl Syst Evol 294:253–262. https://doi.org/10.1007/s00606-011-0471-x
Corander J, Marttinen P (2006) Bayesian identification of admixture events using multi-locus molecular markers. Molec Ecol 15:2833–2843. https://doi.org/10.1111/j.1365-294X.2006.02994.x
Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374
Damboldt J (1965) Zytotaxonomische revision der isophyllen Campanulae in Europa. Bot Jahrb Syst 84:302–358
Degen A (1938) Flora Velebitica III. kötet. A Magyar Tudományos Akadémia Kiadása, Budapest
Di Cola V, Broennimann O, Petitpierre B, Breiner FT, Damen M, Randin C, Engler R, Pottier J, Pio D, Dubuis A, Pellissier L (2017) ecospat: an R package to support spatial analyses and modeling of species niches and distributions. Ecography 40:774–787. https://doi.org/10.1111/ecog.02671
Dice LR (1945) Measures of the amount of ecologic association between species. Ecology 26:297–302
Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011) Geneious v5.4. Available at: http://www.geneious.com/
Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservatio Genet Resources 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
Ehrich D (2006) AFLPdat: a collection of R functions for convenient handling of AFLP data. Molec Ecol Notes 6:603–604. https://doi.org/10.1111/j.1471-8286.2006.01380.x
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molec 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. Molec Ecol Resources 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitocondrial DNA restriction sites. Genetics 131:479–491
Felsenstein J (1985) Confidence-limits on phylogenies—an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.2307/2408678
Frajman B, Schneeweiss GM (2009) A campanulaceous fate: the Albanian stenoendemic Asyneuma comosiforme in fact belongs to isophyllous Campanula. Syst Bot 34:595–601. https://doi.org/10.1600/036364409789271173
Frajman B, Záveská E, Gamisch A, Moser T, Schönswetter P, STEPPE Consortium (2019) Integrating phylogenomics, phylogenetics, morphometrics, relative genome size and ecological niche modelling disentangles the diversification of Eurasian Euphorbia seguieriana sl (Euphorbiaceae). Molec Phylogen Evol 134:238–252. https://doi.org/10.1016/j.ympev.2018.10.046
Grdiša M, Liber Z, Radosavljević I, Carović-Stanko K, Kolak I, Satovic Z (2014) Genetic diversity and structure of Dalmatian pyrethrum (Tanacetum cinerariifolium Trevir./Sch./Bip., Asteraceae) within the Balkan Refugium. PLoS ONE 9:e105265. https://doi.org/10.1371/journal.pone.0105265
Grdiša M, Radosavljević I, Liber Z, Stefkov G, Ralli P, Chatzopoulou PS, Carović-Stanko K, Šatović Z (2019) Divergent selection and genetic structure of Sideritis scardica populations from southern Balkan Peninsula as revealed by AFLP fingerprinting. Sci Rep 9:12767. https://doi.org/10.1038/s41598-019-49097-x
Hamilton CW, Reichard SH (1992) Current practice in the use of subspecies, variety, and forma in the classification of wild plants. Taxon 41:485–498. https://doi.org/10.2307/1222819
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electronica 4:9
Herrmann D, Poncet BN, Manel S, Rioux D, Gielly L, Taberlet P, Gugerli F (2010) Selection criteria for scoring amplified fragment length polymorphisms (AFLPs) positively affect the reliability of population genetic parameter estimates. Genome 53:302–310. https://doi.org/10.1139/g10-006
Janković I, Šatović Z, Liber Z, Kuzmanović N, Radosavljević I, Lakušić D (2016) Genetic diversity and morphological variability in the Balkan endemic Campanula secundiflora s.l. (Campanulaceae). Bot J Linn Soc 180:64–88. https://doi.org/10.1111/boj.12359
Janković I, Satovic Z, Liber Z, Kuzmanović N, Di Pietro R, Radosavljević I, Nikolov Z, Lakušić D (2019) Genetic and morphological data reveal new insights into the taxonomy of Campanula versicolor s.l. (Campanulaceae). Taxon 68:340–369. https://doi.org/10.1002/tax.12050
Kolář F, Fuxová G, Záveská E, Nagano AJ, Hyklová L, Lučanová M, Kudoh H, Marhold K (2016) Northern glacial refugia and altitudinal niche divergence shape genome-wide differentiation in the emerging plant model Arabidopsis arenosa. Molec Ecol 25:3929–3949. https://doi.org/10.1111/mec.13721
Kreuzer M, Tribsch A, Nyffeler R (2014) Ecological and genetic differentiation of two subspecies of Saussurea alpina in the Western Alps. Alpine Bot 124:49–58. https://doi.org/10.1007/s00035-014-0128-9
Kutnjak D, Schönswetter P, Dullinger S, Kuttner M, Niketić M, Frajman B (2014) Escaping to the summits: phylogeography and predicted range dynamics of Cerastium dinaricum, an endangered high mountain plant endemic to the western Balkan Peninsula. Molec Phylogen Evol 78:365–374. https://doi.org/10.1016/j.ympev.2014.05.015
Lakušić D, Liber Z, Nikolić T, Surina B, Kovačić S, Bogdanović S, Stefanović S (2013) Molecular phylogeny of the Campanula pyramidalis species complex (Campanulaceae) inferred from chloroplast and nuclear non-coding sequences and its taxonomic implications. Taxon 62:505–524. https://doi.org/10.12705/623.1
Lewontin RC (1972) The apportionment of human diversity. Evol Biol 6:381–398
Liber Z, Kovačić S, Nikolić T, Likić S, Rusak G (2008) Relations between western Balkan endemic Campanula L. (Campanulaceae) lineages: evidence from chloroplast DNA. Pl Biosystems 142:40–50. https://doi.org/10.1080/11263500701872283
Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1007. https://doi.org/10.1111/j.1461-0248.2008.01229
Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gömöry D, Latalowa M, Litt T, Paule L, Roure JM, Tantau I, Van Der Knaap WO, Petit RJ, De Beaulieu J (2006) A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 171:199–221. https://doi.org/10.1111/j.1469-8137.2006.01740.x
McCormack JE, Zellmer AJ, Knowles LL (2010) Does niche divergence accompany allopatric divergence in Aphelocoma jays as predicted under ecological speciation? Insights from tests with niche models. Evolution 64:1231–1244. https://doi.org/10.1111/j.1558-5646.2009.00900.x
Médail F, Diadema K (2009) Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J Biogeogr 36:1333–1345. https://doi.org/10.1111/j.1365-2699.2008.02051.x
Mereďa P, Hodálová I, Kučera J, Zozomová-Lihová J, Letz DR, Slovák M (2011) Genetic and morphological variation in Viola suavis s.l. (Violaceae) in the western Balkan Peninsula: two endemic subspecies revealed. Syst Biodivers 9:211–231. https://doi.org/10.1080/14772000.2011.603903
Nikolić T (ed) (2019) Flora Croatica database, University of Zagreb, Faculty of Science. Availble at: http://hirc.botanic.hr/fcd. Accessed 10 Sep 2019
Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. Available at: www.abc.se/~nylander/
Olšavská K, Slovák M, Marhold K, Štubňová E, Kučera J (2016) On the origins of Balkan endemics: the complex evolutionary history of the Cyanus napulifer group (Asteraceae). Ann Bot (Oxford) 118:1071–1088. https://doi.org/10.1093/aob/mcw142
Park J-M, Kovačić S, Liber Z, Eddie WM, Schneeweiss GM (2006) Phylogeny and biogeography of isophyllous species of Campanula (Campanulaceae) in the Mediterranean area. Syst Bot 31:862–880. https://doi.org/10.1600/036364406779695924
Peterson AT (2011) Ecological niche conservatism: a time-structured review of evidence. J Biogeogr 38:817–827. https://doi.org/10.1111/j.1365-2699.2010.02456.x
Petit R, Aguinagalde I, de Beaulieu JL, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Müller-Starck G, Demesure-Musch B, Palmé A, Martín JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565. https://doi.org/10.1126/science.1083264
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Pyron RA, Costa GC, Patten MA, Burbrink FT (2015) Phylogenetic niche conservatism and the evolutionary basis of ecological speciation. Biol Rev 90:1248–1262. https://doi.org/10.1111/brv.12154
Rambaut A, Drummond AJ (2007) Tracer v1.4. Available at: http://beast.bio.ed.ac.uk/tracer
Rešetnik I, Baričevič D, Batîr Rusu D, Carović-Stanko K, Chatzopoulou P, Dajić-Stevanović Z, Gonceariuc M, Grdiša M, Greguraš D, Ibraliu A, Jug-Dujaković M, Krasniqi E, Liber Z, Murtić S, Pećanac D, Radosavljević I, Stefkov G, Stešević D, Šoštarić I, Šatović Z (2016a) Genetic diversity and demographic history of wild and cultivated/naturalised plant populations: evidence from Dalmatian sage (Salvia officinalis L., Lamiaceae). PLoS ONE 11:e0159545. https://doi.org/10.1371/journal.pone.0159545
Rešetnik I, Frajman B, Schönswetter P (2016b) Heteroploid Knautia drymeia (Caprifoliaceae) includes K. gussonei and cannot be separated into diagnosable subspecies. Amer J Bot 103:21300–21313. https://doi.org/10.3732/ajb.1500506
Rödder D, Engler JO (2011) Quantitative metrics of overlaps in Grinnellian niches: advances and possible drawbacks. Global Ecol Biogeogr 20:915–927. https://doi.org/10.1111/j.1466-8238.2011.00659.x
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Schoener TW (1968) Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704–726
Schönswetter P, Tribsch A (2005) Vicariance and dispersal in the alpine perennial Bupleurum stellatum L. (Apiaceae). Taxon 54:725–732. https://doi.org/10.2307/25065429
Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana
Slade D, Škvorc Ž, Ballian D, Gračan J, Papeš D (2008) The chloroplast DNA polymorphisms of White Oaks of section Quercus in the Central Balkans. Silvae Genet 57:227–234. https://doi.org/10.1515/sg-2008-0035
Slovák M, Kučera J, Turis P, Zozomová-Lihová J (2012) Multiple glacial refugia and postglacial colonization routes inferred for a woodland geophyte, Cyclamen purpurascens: Patterns concordant with the Pleistocene history of broadleaved and coniferous tree species. Biol J Linn Soc 105:741–760
Španiel S, Marhold K, Zozomová-Lihová J (2017) The polyploid Alyssum montanum-A. repens complex in the Balkans: a hotspot of species and genetic diversity. Pl Syst Evol 303:1443–1465. https://doi.org/10.1007/s00606-017-1470-3
Sun Y, Skinner DZ, Liang GH, Hulbert SH (1994) Phylogenetic analysis of Sorghum and related taxa using internal transcribed spacers of nuclear ribosomal DNA. Theor Appl Genet 89:26–32. https://doi.org/10.1007/bf00226978
Surina B, Schönswetter P, Schneeweiss GM (2011) Quaternary range dynamics of ecologically divergent species (Edraianthus serpyllifolius and E. tenuifolius, Campanulaceae) within the Balkan refugium. J Biogeogr 38:1381–1393. https://doi.org/10.1111/j.1365-2699.2011.02493.x
Surina B, Schneeweiss GM, Glasnović P, Schönswetter P (2014) Testing the efficiency of nested barriers to dispersal in the Mediterranean high mountain plant Edraianthus graminifolius (Campanulaceae). Molec Ecol 23:2861–2875. https://doi.org/10.1111/mec.12779
Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Mol Biol 17:1105–1109. https://doi.org/10.1007/bf00037152
Temunović M, Franjić J, Satovic Z, Grgurev M, Frascaria-Lacoste N, Fernández-Manjarrés JF (2012) Environmental heterogeneity explains the genetic structure of Continental and Mediterranean populations of Fraxinus angustifolia Vahl. PLoS ONE 7:e42764. https://doi.org/10.1371/journal.pone.0042764
Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M (1995) AFLP: a new technique for DNA fingerprinting. Nucl Acids Res 23:4407–4414. https://doi.org/10.1093/nar/23.21.4407
Warren DL, Glor RE, Turelly M (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62:2868–2883. https://doi.org/10.1111/j.1558-5646.2008.00482.x
Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Rev Ecol Evol S 36:519–539. https://doi.org/10.1146/annurev.ecolsys.36.102803.095431
Wiens JJ, Ackerly DD, Allen AP, Anacker BL, Buckley LB, Cornell HV, Damschen EI, Davies TJ, Grytnes JA, Harrison SP, Hawkins BA (2010) Niche conservatism as an emerging principle in ecology and conservation biology. Ecol Lett 13:1310–1324. https://doi.org/10.1111/j.1461-0248.2010.01515.x
Acknowledgements
This study was partially financed by the HAZU project “Genetic diversity of Croatian endemic Campanula”.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Stanislav Španiel.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Contribution to “Plants of the Balkan Peninsula in Space and Time”.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Information on Electronic Supplementary Material
Information on Electronic Supplementary Material
Online Resource 1. Checklist of taxa, collection details, voucher information and GenBank accession numbers of Campanula species analysed in this study.
Online Resource 2. ITS and trnL-trnF alignments.
Online Resource 3. Characteristics of the trnL-trnF and ITS data sets analysed using maximum parsimony (MP) and Bayesian inference (BI).
Online Resource 4. The AFLP pairwise population Fst for fourteen populations of C. fenestrellata s.l.
Online Resource 5.a The most probable value of Evanno’s delta K for 116 individuals of the fourteen populations of Campanula fenestrellata s.l., b the Bayesian analysis of the population structure using the software STRUCTURE assuming K=2, the proportions of the ancestry of each population in each of the defined gene pools are color-coded.
Rights and permissions
About this article
Cite this article
Rešetnik, I., Temunović, M., Liber, Z. et al. Phylogeography of Campanula fenestrellata s.l. (Campanulaceae) in the northern Adriatic. Plant Syst Evol 306, 42 (2020). https://doi.org/10.1007/s00606-020-01668-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-020-01668-6