Abstract
Chamaerops humilis L. (Mediterranean dwarf palm) is an important floristic element of the western Mediterranean region because it is the only palm species naturally distributed in both Europe and Africa. The combination of a time-calibrated phylogeny, a haplotype network and genetic diversity analyses based on plastid sequences, together with previous nuclear DNA fingerprint results, helped reconstruct the colonization history of the dwarf palm. Based on a sample of 218 individuals taken from 29 geographical areas that cover the current distribution of Chamaerops, we detected four plastid DNA (petA-psbJ) haplotypes distributed in two haplotype groups (lineage 1: haplotypes A/B; lineage 2: haplotypes C/D). Haplotypes A, B, and C showed a widespread geographical distribution in both Africa and Europe, whereas haplotype D was restricted to two African localities. Paleobotanical data, species distribution modeling and divergence time estimates suggest that Chamaerops diverged from Trachycarpus in the Miocene (27.05–6.05 Ma), followed by a split of the two C. humilis lineages that remained isolated during the Miocene-Pliocene. Divergence estimates also support a derived split into two haplotypes (A/B) in the Pleistocene, when the Mediterranean Sea barrier was in existence. This, together with geographical distribution of haplotypes A and B, strongly suggests that the disjunct distribution of C. humilis haplotypes in Europe and Africa is the result of long-distance dispersal (LDD) events rather than vicariance. In agreement with recurrent gene flow (events of LDD colonization), AMOVA revealed that most of the genetic variance was found among populations (61.52%). Irrespective of predominant plant translocations by humans or seed dispersal by natural means, our results support that current populations are the result of relatively recent contacts between Africa and Europe in the Quaternary.
Similar content being viewed by others
References
Abbas B, Renwarin Y, Bintoro MH, Sudarsono H, Surahman M, Ehara H (2010) Genetic diversity of sago palm in Indonesia based on chloroplast DNA (cpDNA) markers. Biodiversitas 11:112–111
Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA (2016) Harnessing the power of RADseq for ecological and evolutionary genomics. Nature Rev Genet 17:81–92
Anstett MC (1999) An experimental study of the interaction between the dwarf palm (Chamaerops humilis) and its floral visitor Derelomus chamaeropsis throughout the life cycle of the weevil. Acta Oecol 20:551–558
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge
Baker WJ, Couvreur TLP (2013) Global biogeography and diversification of palms sheds light on the evolution of tropical lineages. I Historical biogeography J Biogeogr 40:274–285
Baker WJ, Savolainen V, Asmussen-Lange CB, Chase MW, Dransfield J, Forrest F, Harley MM, Uhl MW, Wilkinson M (2009) Complete generic-level phylogenetic analyses of palms (Arecaceae) with comparisons of supertree and supermatrix approaches. Syst Biol 58:240–256
Blondel J (2006) The ‘design’ of Mediterranean landscapes: a millennial story of humans and ecological systems during the historic period. Human Ecol 34:713–729
Blondel J, Aronson J (1999) Biology and wildlife of the Mediterranean region. Oxford University Press, Oxford
Burban C, Petit RJ, Carcreff E, Jactel H (1999) Rangewide variation of the maritime pine bast scale Matsucoccus feytaudi Duc. (Homoptera: Matsucoccidae) in relation to the genetic structure of its host. Mol Ecol 8:1593–1603
Cain SA (1943) Criteria for the indication of center of origin in plant geographical studies. Torreya 43:132–1545
Carrión JS (2012) Paleoflora y paleovegetación de la Península Ibérica e Islas Baleares: Plioceno-Cuaternario. Ministerio de Economía y Competitividad, Madrid, Spain
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Cox B, Moore PD, Ladle R (2016) Biogeography: an ecological and evolutionary approach. Wiley Blackwell, Oxford
del Cañizo JA (2011) Palmeras. Ediciones Mundi-Prensa (in Spanish), Madrid, Spain
Delibes M, Castañeda I, Fedriani JM (2017) Goats spit viable seeds from their cud: an overlooked mechanism of seed dispersal by ruminants. Front Ecol Environm (in press)
do Amaral J (1980) Chamaerops. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Waters SM, Webb DA (eds) Flora Europaea, vol V. Cambridge University Press, Cambridge, p 267
Dransfield J, Uhl NW, Asmussen CB, Baker WJ, Harley MM, Lewis CE (2008) Genera Palmarum: the evolution and classification of palms. Royal Botanic Gardens, London, UK
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214
Dufay M (2010) Impact of plant flowering phenology on the cost/benefit balance in a nursery pollination mutualism, with honest males and cheating females. J Evol Biol 23:977–986
Duggen S, Hoernle K, van den Bogaard P, Rüpke L, Morgan JP (2003) Deep roots on the Messinian salinity crisis. Nature 422:602–606
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
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Fedriani JM, Delibes M (2011) Dangerous liaisons disperse the Mediterranean dwarf palm: fleshy-pulp defensive role against seed predators. Ecology 92:304–315
Fernández-Mazuecos M, Vargas P (2011) Historical isolation versus recent long-distance connections between Europe and Africa in bifid toadflaxes (Linaria sect. Versicolores). PLoS One 6:e22234
Fiz O, Valcárcel V, Vargas P (2002) Phylogenetic position of Mediterranean Astereae and character evolution of daisies (Bellis, Asteraceae) inferred from nrDNA ITS sequences. Mol Phylogenet Evol 25:157–171
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge
Galán A, Castroviejo S (2007) Chamaerops L. In: Castroviejo S, Luceño M, Galán A, Jiménez P, Cabezas F, Medina L (eds) Flora ibérica: plantas vasculares de la Península Ibérica e Islas Baleares, vol XVIII: Cyperaceae-Pontederiaceae. Real Jardín Botánico (CSIC), Madrid, pp 273–275
García-Castaño JL, Terrab A, Ortiz MA, Stuessy TF, Talavera S (2014) Patterns of phylogeography and vicariance of Chamaerops humilis L. (Palmae). Turk J Bot 38:1132–1146
García-Verdugo C, Forrest AD, Fay MF, Vargas P (2010) The relevance of gene flow in metapopulation dynamics of an oceanic island endemic, Olea europaea subsp. guanchica. Evolution 64:3525–3536
Giovino A, Scibetta S, Saia S, Guarino C (2014) Genetic and morphologic diversity of European fan palm (Chamareops humilis L.) populations from different environments from Sicily. Bot J Linn Soc 176:66–81
Grivet D, Petit RJ (2002) Phylogeography of the common ivy (Hedera sp.) in Europe: genetic differentiation through space and time. Mol Ecol 11:1351–1362
Guzmán B, Vargas P (2009) Long-distance colonization of the western Mediterranean by Cistus ladanifer (Cistaceae) despite the absence of special dispersal mechanisms. J Biogeogr 36:954–968
Hasnaoui O, Bouazza M, Benali O, Thinon M (2011) Ethno botanic study of Chamaerops humilis L. var. argentea Andre (Arecaceae) in Western Algeria. Agric J 6:1–6
Herrera J (1989) On the reproductive biology of the dwarf palm, Chamaerops humilis in southern Spain. Principes 33:27–32
Hilpold A, Schönswetter P, Susanna A, García-Jacas N, Vilatersana R (2011) Evolution of the Central Mediterranean Centaurea cineraria group (Asteraceae): evidence for relatively recent, allopatric diversification following transoceanic seed dispersal. Taxon 60:528–538
Jacob M, Pérez-Jordà G, Peña-Chocarro L, Zapata L, Ruíz-Alonso M, López-Sáez JA, Linstädter J (2013) The origins of agriculture in North-West Africa: macro-botanical remains from Epipalaeolithic and Early Neolithic levels of Ifri Oudadane (Morocco). J Archaeol Sci 40:2659–2669
Lacroix A (1896) Sur la découverte d’un gisement d’empreintes végétales dans les cendres volcaniques anciennes de l’île de Phira (Santorin). Compt Rend Hebd Séances Acad Sci Serie D 123:656–659
Lo Presti RM, Oberprieler C (2011) The central Mediterranean as a phytodiversity hotchpotch: phylogeographical patterns of the Anthemis secundiramea group (Compositae, Anthemideae) across the Sicilian Channel. J Biogeogr 38:1109–1124
Mai DH (1989) Development and regional differentiation of the European vegetation during the Tertiary. Plant Syst Evol 162:79–91
Médail F, Quézel P (1997) Hot-spots analysis for conservation of plant biodiversity in the Mediterranean Basin. Ann Missouri Bot Gard 84:112–127
Merlo ME, Alemán MM, Cabello J, Peñas J (1993) On the Mediterranean fan palm. Principes 37:l5l–158
Miller MA, Pfeiffer W, Schwartz T 2010 Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, pp 1–8
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, NY
Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155
Ortiz MA, Tremetsberger K, Talavera S, Stuessy T, García-Castaño JL (2007) silvasPopulation structure of Hypochaeris salzmanniana DC. (Asteraceae), an endemic species to the Atlantic coast on both sides of the strait of Gibraltar, in relation to Quaternary Sea level changes. Mol Ecol 16:541–552
Peterson BJ, Graves WR (2016) Chloroplast phylogeography of Dirca palustris L. indicates populations near the glacial boundary at the last glacial maximum in eastern North America. J Biogeogr 43:314–327
Petit RJ et al (2002) Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. Forest Ecol Managem 156:49–74
Pistone A (1890) Disseminazione zoofila per uccelli fitofagi. Naturalista Sicil 9:229–234
Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256
Quezel P (1985) Definition of the Mediterranean region and the origin of its flora. In: Gómez-Campo C (ed) Plant conservation in the Mediterranean area. W. Junk Publ, Dordrecht, pp 9–24
Rambaut A, Drummond AJ (2007) Tracer v1.4, Available from http://beast.bio.ed.ac.uk/Tracer
Rodríguez M, Delibes M, Fedriani JM (2014) Hierarchical levels of seed predation variation by introduced beetles on an endemic Mediterranean palm. PLoS One 9:e109867
Rodríguez-Sánchez F, Pérez-Barrales R, Ojeda F, Vargas P, Arroyo J (2008) The strait of Gibraltar as a melting pot for plant biodiversity. Quaternary Sci Rev 27:2100–2117
Rundel PW, Arroyo MTK, Cowling RM, Keeley JE, Lamont BB, Vargas P (2016) Mediterranean biomes: evolution of their vegetation, floras, and climate. Ann Rev Ecol Evol Syst 47:383–407
Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94:275–288
Silva JL, Lim S-Y, Kim S-C, Mejías JA (2015) Phylogeography of cliff-dwelling relicts with a highly narrow and disjunct distribution in the western Mediterranean. Am J Bot 102:1538–1551
Soltis DE, Gitzendanner MA, Strenge DD, Soltis PS (1997) Chloroplast DNA intraspecific phylogeography of plants from the Pacific Northwest of North America. Plant Syst Evol 206:353–373
Stillman JH, Armstron E (2017) Genomics are transforming our understanding of responses to climate change. BioScience
Suc JP et al (1995) Structure of West Mediterranean vegetation and climate since 5.3 Ma. Acta Zool Cracrov 38:3–16
Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III Cladogram estimation Genetics 132:619–633
Terrab A, Talavera S, Arista M, Paun O, Stuessy TF, Tremetsberger K (2007) Genetic diversity and geographic structure at chloroplast microsatellites (cpSSRs) in endangered West Mediterranean firs (Abies spp., Pinaceae). Taxon 56:409–416
Thompson JD (2005) Plant evolution in the Mediterranean. Oxford University Press, Oxford
Troia A, Raimondo FM, Geraci A (2012) Does genetic population structure of Ambrosina bassii L. (Araceae, Ambrosineae) attest a post-Messinian land-bridge between Sicily and Africa? Flora 207:646–653
Vargas P, Morton CM, Jury SL (1999) Biogeographic patterns in Mediterranean and Macaronesian species of Saxifraga (Saxifragaceae) inferred from phylogenetic analyses of ITS sequences. Am J Bot 86:724–734
Vendramin GG et al (2008) Genetically depauperate but widespread: the case of an emblematic Mediterranean pine. Evolution 62:680–688
Wang CB, Smith TB (2002) Closing the seed dispersal loop. Trends Ecol Evol 17:379–385
Woodward JC (2009) The physical geography of the Mediterranean. Oxford University Press, Oxford
Acknowledgments
The authors thank to four anonymous reviewers and W. Baker for suggestions that improved the quality of the manuscript, to J. Mayol for information about historical uses of dwarf palm in Baleares; to M. Ahmim, M. d’Amico, G. Calvo, J. Calzada, M. Clavero, C. Delibes, M. Jácome, A. Longo, I. Mateos, M. Navarro, E. Pérez de Gracia, E. Real, Riserva Naturale Orientata dello Zingaro, O. Rodríguez, A. Segura, J. Serrano, A. Vázquez, P. Vázquez, and Servicio de Protección de Especies de las Islas Baleares for field assistance and collection of plant material; and to E. Cano for lab assistance. This research was supported by the Spanish Ministry of Science and Innovation (CGL2010-21926), the Spanish Ministry of Economy and Competitiveness (CGL2015-67865-P), a FCT Portuguese grant (IF/00728/2013) to JMF, and a Juan de la Cierva fellowship to BG.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Data Archiving Statement
We have submitted the petA-psbJ sequences to Genbank. See supplementary Table S2 for accession numbers.
Additional information
Communicated by Z. Kaya
Electronic supplementary material
ESM 1
(DOCX 22 kb)
Rights and permissions
About this article
Cite this article
Guzmán, B., Fedriani, J.M., Delibes, M. et al. The colonization history of the Mediterranean dwarf palm (Chamaerops humilis L., Palmae). Tree Genetics & Genomes 13, 24 (2017). https://doi.org/10.1007/s11295-017-1108-1
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-017-1108-1