Surviving in Mountain Climate Refugia: New Insights from the Genetic Diversity and Structure of the Relict Shrub Myrtus nivellei (Myrtaceae) in the Sahara Desert

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Migliore, Jérémy ^a   Baumel, Alex ^a   Juin, Marianick ^a   Fady, Bruno ^b   Roig, Anne ^b   Duong, Nathalie ^a   Médail, Frédéric ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b French National Institute for Agriculture   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MICROSATELLITE DNA;

ALGERIA; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ARTICLE; CLIMATE CHANGE; GENE ISOLATION; GENE STRUCTURE; GENETIC VARIABILITY; GENOTYPE; MICROSATELLITE MARKER; MOLECULAR CLONING; MULTILOCUS SEQUENCE TYPING; MYRTUS NIVELLEI; NONHUMAN; PALEOENVIRONMENT; PLANT GENETICS; POPULATION GENETICS; SHRUB; SPECIES REFUGE;

ADAPTATION, PHYSIOLOGICAL; AFRICA, NORTHERN; ALTITUDE; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; BAYES THEOREM; DESERT CLIMATE; ECOSYSTEM; FRESH WATER; GENETIC VARIATION; GENOTYPE; MICROSATELLITE REPEATS; MULTIGENE FAMILY; MULTIVARIATE ANALYSIS; MYRTUS; PHYLOGENY; PHYLOGEOGRAPHY;

EID: 84884215389     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073795     Document Type: Article

References (88)

1. Wilson JS, Pitts J, (2012) Identifying Pleistocene refugia in North American cold deserts using phylogeographic analyses and ecological niche modelling. Divers Distrib 18: 1139-1152.
2. Keppel G, Van Niel KP, Wardell-Johnson GW, Yates CJ, Byrne M, et al. (2012) Refugia: identifying and understanding safe havens for biodiversity under climate change. Glob Ecol Biogeogr 21: 393-404.
3. Hampe A, Rodríguez-Sánchez F, Dobrowski S, Hy FS, Gavin DG, (2013) Climate refugia: from the Last Glacial Maximum to the twenty-first century. New Phytol 197: 16-18.
4. Hewitt GM, (2000) The genetic legacy of the Quaternary ice ages. Nature 405: 907-913.
5. Weiss S, Ferrand N (2007) Phylogeography of southern European refugia. Evolutionary perspectives on the origins and conservation of European biodiversity. Berlin: Springer. 377 p.
6. Bennett KD, Provan J, (2008) What do we mean by 'refugia'? Quat Sci Rev 27: 2449-2455.
7. Médail F, Diadema K, (2009) Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J Biogeogr 36: 1333-1345.
8. Ashcroft MB, (2010) Identifying refugia from climate change. J Biogeogr 37: 1407-1413.
9. Stewart JR, Lister AM, Barnes I, Dalén L, (2010) Refugia revisited: individualistic responses of species in space and time. Proc Biol Sci 277: 661-671.
10. Nieto Feliner G, (2011) Southern European glacial refugia: a tale of tales. Taxon 60: 365-372.
11. Hampe A, Jump AS, (2011) Climate relicts: past, present, future. Annu Rev Ecol Evol Syst 42: 313-333.
12. Fahrig L, (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34: 487-515.
13. Jump AS, Peñuelas J, (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett 8: 1010-1020.
14. Habel JC, Assmann T (2010) Relict species. Phylogeography and conservation biology. Berlin Heidelberg: Springer-Verlag. 468 p.
15. Kropf M, Kadereit JW, Comes HP, (2003) Differential cycles of range contraction and expansion in European high mountain plants during the Late Quaternary: insights from Pritzelago alpina (L.) O. Kuntze (Brassicaceae). Mol Ecol 12: 931-949.
16. Kropf M, Comes HP, Kadereit JW, (2012) Past, present and future of mountain species of the French Massif Central - the case of Soldanella alpina L. subsp. alpina (Primulaceae) and a review of other plant and animal studies. J Biogeogr 39: 799-812.
17. Pepper M, Ho SYW, Fujita MK, Keogh JS, (2011) The genetic legacy of aridification: climate cycling fostered lizard diversification in Australian montane refugia and left low-lying deserts genetically depauperate. Mol Phylogenet Evol 61: 750-759.
18. Danin A, (1999) Desert rocks as plant refugia in the near East. Bot Rev 65: 93-170.
19. Millenium Ecosystem Assessment (2005) The Millenium Ecosystem Assessment. Wahington, DC: World Resources Institute. Available: www.milleniumassessment.org/.
20. Douady CJ, Catzeflis F, Raman J, Springer MS, Stanhope MJ, (2003) The Sahara as a vicariant agent, and the role of Miocene climatic events, in the diversification of the mammalian order Macroscelidea (elephant shrews). Proc Natl Acad Sci U S A 100: 8325-8330.
21. Swezey CS, (2009) Cenozoic stratigraphy of the Sahara, Northern Africa. J Afr Earth Sci 53: 89-121.
22. Rognon P (1980) Pluvial and arid phases in the Sahara: the role of non-climatic factors. In: Van Zinderen-Bakker Sr EM, Coetzee JA, editors. Palaeoecology of Africa and the surrounding islands. Rotterdam: AA Balkema. 45-62.
23. Maley J, (2010) Climate and Palaeoenvironment evolution in north tropical Africa from the end of the Tertiary to the Upper Quaternary. Palaeoecology of Africa 30: 227-278.
24. De Menocal P, Ortiz J, Guilderson T, Adkins J, Sarnthein, et al, (2000) Abrupt onset and termination of the African Humid Period: rapid climate responses to gradual insolation forcing. Quat Sci Rev 19: 347-361.
25. Kröpelin S, Verschuren D, Lézine AM, Eggermont H, Coquyt C, et al. (2008) Climate-driven ecosystem succession in the Sahara: The past 6000 years. Science 320: 765-768.
26. Trape S, (2009) Impact of climate change on the relict tropical fish fauna of Central Sahara: threat for the survival of Adrar mountains fishes, Mauritania. PLoS ONE 4(2): e4400 doi:10.1371/journal.pone.0004400.
27. Brito JC, Martínez-Freiría F, Sierra P, Sillero N, Tarroso P, (2011) Crocodiles in the Sahara desert: an update of distribution, habitats and population status for conservation planning in Mauritania. PLoS ONE 6(2): e14734 doi:10.1371/journal.pone.0014734.
28. Abdoun F, Beddiaf M, (2002) Cupressus dupreziana A. Camus: répartition, dépérissement et régénération au Tassili n'Ajjer, Sahara central. C R Biol 325: 617-627.
29. Quézel P, Martinez C, (1960) Le dernier interpluvial au Sahara central, essai de chronologie palynologique et paléoclimatique. Lybica 6/7: 211-227.
30. Anthelme F, Waziri Mato M, Maley J, (2008) Elevation and local refuges ensure persistence of mountain specific vegetation in the Nigerien Sahara. J Arid Environ 72: 2232-2242.
31. Watrin J, Lézine AM, Hély C, (2009) Plant migration and plant communities at the time of the "green Sahara". C R Geoscience 341: 656-670.
32. Quézel P (1965) La végétation du Sahara, du Tchad à la Mauritanie. Stuttgart: Gustav Fischer Verlag. 336 p.
33. Quézel P, (1978) Analysis of the flora of the Mediterranean and Saharan Africa. Ann Mo Bot Gard 65: 479-534.
34. Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, et al. (2000) Global biodiversity scenarios for the year 2100. Science 287: 1770-1774.
35. Giorgi F, Lionello P, (2008) Climate change projections for the Mediterranean region. Glob Planet Change 63: 90-104.
36. Besnard G, Anthelme F, Baali-Cherif D, (2012) The Laperrine's olive tree (Oleaceae): a wild genetic resource of the cultivated olive and a model-species for studying the biogeography of the Saharan Mountains. Acta Bot Gall: Botany Letters 159: 319-328.
37. Genner MJ, Haesler MP, (2010) Pliocene isolation of a north-west Saharan cichlid fish. J Fish Biol 76: 435-441.
38. Arenas M, Ray N, Currat M, Excoffier L, (2012) Consequences of range contractions and range shifts on molecular diversity. Mol Biol Evol 29: 207-218.
39. Quézel P (1958) Mission botanique au Tibesti. Alger: Mémoire de l'Institut de Recherches Sahariennes 4. 357 p.
40. Govaerts R, Sobral M, Ashton P, Barrie F, Holst BK, et al. (2008) World checklist of Myrtaceae. Kew: Royal Botanic Gardens.
41. Migliore J, Baumel A, Juin M, Médail F, (2012) From Mediterranean shores to central Saharan mountains: key phylogeographical insights from the genus Myrtus. J Biogeogr 39: 942-956.
42. Vos P, Hogers R, Bleeker M, Reijans M, Van de Lee T, et al. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23: 4407-4414.
43. Quézel P (1954) Contribution à l'étude de la flore et de la végétation du Hoggar. Alger: Institut de recherches sahariennes. Monographies régionales 2. 164 p.
44. Leredde C (1957) Etude écologique et phytogéographique du Tassili n'Ajjer. Alger: Travaux de l'Institut de recherches sahariennes, série du Tassili, tome II. 455 p.
45. Dubief J (1959) Le climat du Sahara. Mémoire de l'Institut de recherches sahariennes. Alger: Université d'Alger. 586 p.
46. Battandier J-A, Trabut L, (1911) Contribution à la flore du pays des Touaregs. Bulletin de la Société Botanique de France 58: 669-677.
47. Doyle JJ, Doyle JL, (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11-15.
48. Albaladejo RG, Sebastiani F, González-Martínez SC, González-Varo JP, Vendramin GG, et al. (2010) Isolation of microsatellite markers for the common Mediterranean shrub Myrtus communis (Myrtaceae). Am J Bot 11: e23-e25.
49. Bonin A, Bellemain P, Bronken Eidesen P, Pompanon F, Brochmann C, et al. (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13: 3261-3273.
50. Parks JC, Werth CR, (1993) A study of spatial features of clones in a population of bracken fern, Pteridium aquilinum (Dennstaedtiaceae). Am J Bot 80: 120-126.
51. Peakall R, Smouse PE, (2006) GenAlEx6: Genetic Analysis in Excel. Population genetic software for teaching and research. Mol Ecol 6: 288-295.
52. Kalinowski ST, (2005) HP-Rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5: 187-189.
53. 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.
54. Jombart T, Devillard S, Balloux F, (2010) Discriminant analysis of principal components a new method for the analysis of genetically structured populations. BMC Genetics 11: 94.
55. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
56. Falush D, Stephens M, Pritchard JK, (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567-1587.
57. Falush D, Stephens M, Pritchard JK, (2007) Inference on population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7: 574-578.
58. Evanno G, Regnaul S, Goudet J, (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol Ecol 14: 2611-2620.
59. Wright S, (1943) Isolation by distance. Genetics 28: 114-138.
60. Bakker EG, Van Dam BC, Van Eck HJ, Jacobsen E, (2001) The description of clones of Quercus robur L. and Q. petraea (Matt.) Liebl. with microsatellites and AFLP in an ancient woodland. Plant Biol 3: 616-621.
61. May MR, Provance MC, Sanders AC, Ellstrand NC, Ross-Ibarra J, (2009) A Pleistocene clone of Palmer's Oak persisting in Southern California. PLoS ONE 4(12): e8346 doi:10.1371/journal.pone.0008346.
62. García D, Zamora R, (2003) Persistence, multiple demographic strategies and conservation in long-lived Mediterranean plants. J Veg Sci 14: 921-926.
63. Honnay O, Bossuyt B, (2005) Prolonged clonal growth: escape route or route to extinction? Oikos 108: 427-432.
64. Crawford RMM (2008) Plants at the margin: ecological limits and climate change. Cambridge: Cambridge University Press. 476 p.
65. Kawecki TJ, (2008) Adaptation to marginal habitats. Annu Rev Ecol Evol Syst 39: 321-342.
66. Vonlanthen B, Zhang X, Bruelheide H, (2010) Clonal structure and genetic diversity of three desert phreatophytes. Am J Bot 97: 234-242.
67. Wesche K, Walther D, Wehrden von H, Hensen I, (2011) Trees in the desert: reproduction and genetic structure of fragmented Ulmus pumila forests in Mongolian drylands. Flora 206: 91-99.
68. Baali-Cherif D, Besnard G, (2005) High genetic diversity and clonal growth in relict populations of Olea europaea subsp. laperrinei (Oleaceae) from Hoggar, Algeria. Ann Bot 96: 823-830.
69. Anthelme F, Abdoulkader A, Besnard G, (2008b) Distribution, shape and clonal growth of the rare endemic tree Olea europaea subsp. laperrinei (Oleaceae) in the Saharan mountains of Niger. Plant Ecol 198: 73-87.
70. Pichot C, El Maâtaoui M, Raddi S, Raddi P, (2001) Surrogate mother for endangered Cupressus. Nature 412: 39.
71. Maley J (1981) Etudes palynologiques dans le bassin du Tchad et paléoclimatologie de l'Afrique nord-tropicale de 30 000 ans à l'époque actuelle. Paris: Travaux et documents de l'ORSTOM, 129. 586 p.
72. Besnard G, Christin PA, Bouguedoura N, Anthelme F, (2007a) Spatial genetic structure in the Laperrine's olive (Olea europaea subsp. laperrinei), a long-living tree from the central Saharan mountains. Heredity 99: 649-657.
73. Moritz C, (1994) Defining 'Evolutionary Significant Units' for conservation. Trends Ecol Evol 9: 373-375.
74. Moritz C, (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51: 238-254.
75. Moreau RE, (1961) Problems of Mediterranean-Saharan migration. Ibis 103a: 373-427.
76. Wickens GE, (1976) Speculations on long distance dispersal and the flora of Jebel Marra, Sudan Republic. Kew Bull 31: 105-150.
77. Brochet A-L, Guillemain M, Fritz H, Gauthier-Clerc M, Green AJ, (2009) The role of migratory ducks in the long-distance dispersal of native plants and the spread of exotic plants in Europe. Ecography 32: 919-928.
78. Salewski V, Schmaljohann H, Liechti F, (2010) Spring passerine migrants stopping over in the Sahara are not fall-outs. J Ornithol 151: 371-378.
79. Biebach H, Biebach I, Friedrich W, Heine G, Partecke J, et al. (2000) Strategies of passerine migration across the Mediterranean Sea and the Sahara desert: a radar study. Ibis 142: 623-634.
80. Quézel P (1997) High mountains of the Central Sahara: dispersal, speciation, origin and conservation of the flora. In: Barakat HN, Hegazy AK, editors. Reviews in Ecology: desert conservation and development. Cairo: Metropole. 159-175.
81. Patiny S, Michez D, (2007) Biogeography of bees (Hymenoptera, Apoidea) in Sahara and the Arabian deserts. Insect Syst Evol 38: 19-34.
82. Rossetto M, Kooyman R, (2005) The tension between dispersal and persistence regulates the current distribution of rare palaeoendemic rain forest flora: a case study. J Ecol 93: 906-917.
83. Drake NA, El-Hawat AS, Turner P, Armitage SJ, Salem MJ, et al. (2008) Palaeohydrology of the Fazzan Basin and surrounding regions: the last 7 million years. Palaeogeogr Palaeoclimatol Palaeoecol 263: 131-145.
84. Osborne AH, Vance D, Rohling EJ, Barton N, Rogerson M, et al. (2008) A humid corridor across the Sahara for the migration of early modern humans out of Africa 120,000 years ago. Proc Natl Acad Sci U S A 105: 16444-16447.
85. Albaladejo RG, Carrillo LF, Aparicio A, Fernandez-Manjarres JF, Gonzalez-Varo JP, (2008) Population genetic structure in Myrtus communis L. in a chronically fragmented landscape in the Mediterranean: can gene flow counteract habitat perturbation? Plant Biol 11: 442-453.
86. Aparicio A, Hampe A, Fernández-Carrillo L, Albaladejo RG, (2012) Fragmentation and comparative genetic structure of four Mediterranean woody species: complex interactions between life history traits and the landscape context. Divers Distrib 18: 226-235.
87. Lézine AM (2008) Le pollen, outil d'étude de l'environnement et du climat. Paris: Vuibert. 118 p.
88. Petit-Maire N (1991) Paléoenvironnements du Sahara. Lacs holocènes à Taoudenni (Mali). Paris: CNRS Editions. 239 p.