Skip to main content
Log in

Biogeography of neutral genes and recent evolutionary history of pines in the Mediterranean Basin

  • Review Paper
  • Published:
Annals of Forest Science Aims and scope Submit manuscript

Abstract

Context

Mediterranean pines share many common life-history traits. They are found at almost all altitudinal levels around the Mediterranean Basin, from sea level to high-elevation mountains, and from hot and dry to wet and cold bioclimates. Their distribution ranges from widespread to regional and narrow, and from dense extensive populations to small populations of scattered individuals. They have been extensively used by human civilizations for millennia.

Aims

I show which are the main phylogenetic, ecological, and climatic factors explaining the patterns of within and among-population genetic diversity in Mediterranean pines.

Methods

I use a narrative synthesis approach and multiple examples from the literature on pine species from the Mediterranean Basin and California.

Results

While Mediterranean pines have the highest levels of differentiation worldwide, their genetic diversity increases from west to east and is significantly reduced in low-elevation species. Factors such as ancestral adaptation to wildfire, reduction of effective population size during the Last Glacial Maximum, long distance dispersal during the Holocene, and more recent adaptation to patchy environmental conditions could explain these patterns.

Conclusion

Because of contrasted ecological, demographic, historical, and geographical processes, and despite their common biological attributes, pines of the Mediterranean Basin display complex biogeographic patterns at neutral gene level that can help retrace their evolutionary history. Although individual species often represent unique case studies that make generalizations risky, locating habitats of significantly high and low genetic diversity is key for detecting and understanding the major factors affecting gene diversity and may prove useful for profiling areas of high conservation value in the Mediterranean.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Alía R., Martín S (2003) EUFORGEN Technical Guidelines for genetic conservation and use for Maritime pine (Pinus pinaster). International Plant Genetic Resources Institute, Rome, Italy

  • Austerlitz F, Mariette S, Machon N, Gouyon P-H, Godelle B (2000) Effects of colonization processes on genetic diversity: differences between annual plants and tree species. Genetics 154:1309–1321

    PubMed  CAS  Google Scholar 

  • Barbéro M, Loisel R, Quézel P, Richardson DM, Romane F (1998) Pines of the Mediterranean Basin. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge Univ. Press, Cambridge

    Google Scholar 

  • Benito-Garzón M, de Dios RS, Ollero HS (2007) Predictive modelling of tree species distributions on the Iberian Peninsula during the Last Glacial Maximum and Mid-Holocene. Ecography 30:120–134

    Google Scholar 

  • Benito-Garzón M, Alia R, Robson TR, Zavala MA (2011) Intra-specific variability and plasticity influence potential tree species. Glob Ecol Biogeogr 20:766–778

    Article  Google Scholar 

  • Bucci G, Gonzalez-Martinez SC, Le Provost G, Plomion C, Ribeiro MM, Sebastiani F, Alia R, Vendramin GG (2007) Range-wide phylogeography and gene zones in Pinus pinaster Ait. revealed by chloroplast microsatellite markers. Mol Ecol 16:2137–2153

    Article  PubMed  CAS  Google Scholar 

  • Chambel MR, Climent J, Alía R (2007) Divergence among species and populations of Mediterranean pines in biomass allocation of seedlings grown under two watering regimes. Ann For Sci 64:87–97

    Article  Google Scholar 

  • Climent J, Costa e Silva F, Chambel MR, Pardos M, Almeida MH (2009) Freezing injury in primary and secondary needles of Mediterranean pine species of contrasting ecological niches. Annals of Forest Science, 66, article 407

    Google Scholar 

  • Eckert AJ, Hall BD (2006) Phylogeny, historical biogeography, and patterns of diversification for Pinus (Pinaceae): phylogenetic tests of fossil-based hypotheses. Mol Phylogenet Evol 40:166–182

    Article  PubMed  CAS  Google Scholar 

  • Eveno E, Collada C, Guevara MA, Léger V, Soto A, Díaz L, Léger P et al (2008) Contrasting patterns of selection at Pinus pinaster Ait. drought stress candidate genes as revealed by genetic differentiation analyses. Mol Biol Evol 25:417–437

    Article  PubMed  CAS  Google Scholar 

  • Fady B (2005) Is there really more biodiversity in Mediterranean forest ecosystems? Taxon 54:905–910

    Article  Google Scholar 

  • Fady B, Conord C (2010) Macroecological patterns of species and genetic diversity in vascular plants of the Mediterranean Basin. Divers Distrib 16:53–64

    Article  Google Scholar 

  • Fady B, Médail F (2004) Mediterranean forest ecosystems. In: Burley J, Evans J, Youngquist JA (eds) Encyclopedia of forest science. Elsevier, London, pp 1403–1414

    Chapter  Google Scholar 

  • Fady B, Semerci H, Vendramin GG (2003) Technical guidelines for genetic conservation and use for Aleppo pine (Pinus halepensis) and Brutia pine (Pinus brutia). EUFORGEN. International Plant Genetic Resources Institute, Rome, 6p

    Google Scholar 

  • Fady B, Fineschi S, Vendramin GG (2004) EUFORGEN technical guidelines for genetic conservation and use for Italian stone pine (Pinus pinea). International Plant Genetic Resources Institute, Rome

    Google Scholar 

  • Fallour D, Fady B, Lefèvre F (1997) Study on isozyme variation in Pinus pinea L.: evidence of low polymorphism. Silvae Genetica 46:201–207

    Google Scholar 

  • Farjon A (2008) A natural history of conifers. Timber Press, Portland

    Google Scholar 

  • Fernandes P, Rigolot E (2007) The fire ecology and management of maritime pine (Pinus pinaster Ait.). For Ecol Manag 241:1–13

    Article  Google Scholar 

  • Gernandt DS, Lopez GG, Garcia SO, Liston A (2005) Phylogeny and classification of Pinus. Taxon 54:29–42

    Article  Google Scholar 

  • Gitzendanner MA, Soltis PS (2000) Patterns of genetic variation in rare and widespread plant congeners. Am J Bot 87:783–792, 2000

    Article  PubMed  CAS  Google Scholar 

  • Gómez A, González-Martínez SC, Collada C, Climent J, Gil L (2003) Complex population genetic structure in the endemic Canary island pine revealed using chloroplast microsatellite markers. Theor Appl Genet 107:1123–1131

    Article  PubMed  Google Scholar 

  • Gómez A, Vendramin GG, González-Martínez SC, Alía R (2005) Genetic diversity and differentiation of two Mediterranean pines (Pinus halepensis Mill. and Pinus pinaster Ait.) along a latitudinal cline using chloroplast microsatellite markers. Divers Distrib 11:257–263

    Article  Google Scholar 

  • González Martínez SC, Alía R, Gil L (2002) Population genetic structure in a Mediterranean pine (Pinus pinaster Ait.): a comparison of allozyme markers and quantitative traits. Heredity 89:199–206

    Article  PubMed  Google Scholar 

  • González-Martínez SC, Mariette S, Ribeiro MM, Burban C, Raffin A, Chambel MR, Ribeiro CA et al (2004) Genetic resources in maritime pine (Pinus pinaster Aiton): molecular and quantitative measures of genetic variation and differentiation among maternal lineages. For Ecol Manag 197:103–115

    Article  Google Scholar 

  • Grivet D, Sebastiani F, Gonzalez-Martinez SC, Vendramin GG (2009) Patterns of polymorphism resulting from long-range colonization in the Mediterranean conifer Aleppo pine. New Phytol 184:1016–1028

    Article  PubMed  CAS  Google Scholar 

  • Grivet D, Sebastiani F, Alia R, Bataillon T, Torre S, Zabal-Aguirre M, Vendramin GG, Gonzalez-Martinez SC (2011) Molecular footprints of local adaptation in two mediterranean conifers. Mol Biol Evol 28:101–116

    Article  PubMed  CAS  Google Scholar 

  • Hampe A, Petit RJ (2005) Conserving biodiversity under climate change?: the rear edge matters. Ecology Letters 8(5):461–467

    Google Scholar 

  • Hamrick JL, Godt MJW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. New For 6:95–124

    Article  Google Scholar 

  • He T, Pausas JG, Belcher CM, Schwilk DW, Lamont BB (2012) Fire-adapted traits of Pinus arose in the fiery Cretaceous. New Phytol 194:751–759

    Article  PubMed  Google Scholar 

  • Heuertz M, Teufel J, González-Martínez SC, Soto A, Fady B, Alía R, Vendramin GG (2010) Geography determines genetic relationships between species of mountain pine (Pinus mugo complex) in Western Europe. J Biogeogr 37:541–556

    Article  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  PubMed  CAS  Google Scholar 

  • Hewitt G (2004) Genetic consequences of climatic oscillations in the Quaternary. Phil Trans Roy Soc Lond B 359:183–195

    Article  CAS  Google Scholar 

  • Isajev V, Fady B, Semerci H, Andonowski V (2005) Technical guidelines for genetic conservation and use of European black pine (Pinus nigra). EUFORGEN. International Plant Genetic Resources Institute, Rome, 6p

    Google Scholar 

  • Keeley JE (2012) Ecology and evolution of pine life histories. Ann For Sci 69. doi:10.1007/s13595-012-0201-8

  • Klaus W (1989) Mediterranean pines and their history. Plant Systematics and Evolution 162:133–163

  • Kurt Y, González-Martínez SC, Alia R, Isik K (2012) Genetic differentiation in Pinus brutia Ten using molecular markers and quantitative traits: the role of altitude. Ann For Sci 69:34345–34351

    Article  Google Scholar 

  • Lamy JB, Bouffier L, Burlett R, Plomion C, Cochard H et al (2011) Uniform selection as a primary force reducing population genetic differentiation of cavitation resistance across a species range. PLoS One 6:e23476

    Article  PubMed  CAS  Google Scholar 

  • Le Corre V, Kremer A (1998) Cumulative effects of founding events during colonisation on genetic diversity and differentiation in an island and stepping-stone model. J Evol Biol 11:495–512

    Article  Google Scholar 

  • Liepelt S, Cheddadi R, de Beaulieu JL, Fady B, Gömöry D, Hussendörfer E, Konnert M, Litt T, Longauer R, Terhürne-Berson R, Ziegenhagen B (2009) Postglacial range expansion and its genetic imprints in Abies alba (Mill.)—a synthesis from paleobotanic and genetic data. Rev Palaeobot Palynology 153:139–149

    Article  Google Scholar 

  • Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gomory D, Latalowa M, Litt T, Paule L, Roure JM, Tantau I, van der Knaap WO, Petit RJ, de Beaulieu JL (2006) A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 171:199–221

    Article  PubMed  CAS  Google Scholar 

  • Médail F, Diadema K (2009) Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J Biogeogr 36:1333–1345

    Article  Google Scholar 

  • Médail F, Quézel P (1999) Biodiversity hotspots in the Mediterranean basin: setting global conservation priorities. Conserv Biol 13:1510–1513

    Article  Google Scholar 

  • Mezquida ET, Benkman CW (2005) The geographic selection mosaic for squirrels, crossbills and Aleppo pine. J Evol Biol 18:348–357

    Article  PubMed  CAS  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  PubMed  CAS  Google Scholar 

  • Pausas J, Bradstock R, Keith D, Keeley J (2004) Plant functional traits in relation to fire in crown-fire ecosystems. Ecology 85:1085–1100

    Article  Google Scholar 

  • Pausas JG, Keeley JE, Verdu M (2006) Inferring differential evolutionary processes of plant persistence traits in Northern Hemisphere Mediterranean fire-prone ecosystems. J Ecol 94:31–39

    Article  Google Scholar 

  • Petit RJ, Aguinagalde I, de Beaulieu JL, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Muller-Starck GM, Demesure-Musch B, Palme A, Martin JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565

    Article  PubMed  CAS  Google Scholar 

  • Petit RJ, Hampe A, Cheddadi R (2005) Climate changes and tree phylogeography in the Mediterranean. Taxon 54:877–885

    Article  Google Scholar 

  • Price RA, Liston A, Strauss SH (1998) Phylogeny and systematics of Pinus. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge Univ Press, Cambridge

    Google Scholar 

  • Quézel P, Médail F (2003) Ecologie et biogéographie des forêts du bassin méditerranéen. Elsevier, Paris

    Google Scholar 

  • Richardson DM, Rejmánek M (2011) Trees and shrubs as invasive alien species—a global review. Divers Distrib 17:788–809

    Article  Google Scholar 

  • Rodriguez-Sanchez F, Hampe A, Jordano P, Arroyo J (2010) Past tree range dynamics in the Iberian Peninsula inferred through phylogeography and palaeodistribution modelling: a review. Rev Palaeobot Palynol 162:507–521

    Article  Google Scholar 

  • Roques L, Hamel F, Fayard J, Fady B, Klein EK (2010) Recolonisation by diffusion can generate increasing rates of spread. Theor Popul Biol 77:205–212

    Article  PubMed  CAS  Google Scholar 

  • Santos-del-Blanco L, Notivol E, Zas R, Chambel MR, Majada J, Climent J (2010) Variation of early reproductive allocation in multi-site genetic trials of Maritime pine and Aleppo pine. For Syst 19:381–392

    Google Scholar 

  • Savolainen O, Pyhäjärvi T, Knürr T (2007) Gene flow and local adaptation in trees. Ann Rev Ecol Evol Syst 38:595–619

    Article  Google Scholar 

  • Schwilk DW, Ackerly DD (2001) Flammability and serotiny as strategies: correlated evolution in pines. Oikos 94:326–336

    Article  Google Scholar 

  • Soto A, Robledo-Arnuncio JJ, Gonzalez-Martinez SC, Smouse PE, Alia R (2010) Climatic niche and neutral genetic diversity of the six Iberian pine species: a retrospective and prospective view. Mol Ecol 19:1396–1409

    Article  PubMed  CAS  Google Scholar 

  • Tapias R, Climent J, Pardos JA, Gil L (2004) Life histories of Mediterranean pines. Plant Ecol 171:53–68

    Article  Google Scholar 

  • Van Andel TH (2002) The climate and landscape of middle part of Weichselian glaciation in Europe: the stage 3 project. Quat Res 57:2–8

    Article  Google Scholar 

  • Vellend M, Geber MA (2005) Connections between species diversity and genetic diversity. Ecol Lett 8:767–781

    Article  Google Scholar 

  • Vendramin GG, Fady B, González-Martínez SC, Hu FS, Scotti I, Sebastiani F, Soto A, Petit RJ (2008a) Genetically depauperate but widespread: the case of an emblematic Mediterranean pine. Evolution 62:680–688

    Article  PubMed  Google Scholar 

  • Vendramin GG, Fineschi S, Fady B (2008b) EUFORGEN Technical Guidelines for genetic conservation and use of Bosnian pine (Pinus heldreichii). Bioversity International, Rome, p 6

    Google Scholar 

  • Vranckx G, Jacquemyn H, Muys B, Honnay O (2012) Meta-analysis of susceptibility of woody plants to loss of genetic diversity through habitat fragmentation. Conserv Bio 26:228–237

    Article  Google Scholar 

  • Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was made possible by financial support from the European Network of Excellence EVOLTREE, from the Eranet Biodiversa LINKTREE project and from the European Union Capacities Program AGORA project. I thank F. Lefèvre and three anonymous reviewers for helpful comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bruno Fady.

Additional information

Handling Editor: Eric Rigolot

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fady, B. Biogeography of neutral genes and recent evolutionary history of pines in the Mediterranean Basin. Annals of Forest Science 69, 421–428 (2012). https://doi.org/10.1007/s13595-012-0219-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13595-012-0219-y

Keywords

Navigation