Evolutionary dynamics of emblematic Araucaria species (Araucariaceae) in New Caledonia: nuclear and chloroplast markers suggest recent diversification, introgression, and a tight link between genetics and geography within species

BMC Evolutionary Biology

Pete M Hollingsworth²  Richard A Ennos³  Philip Thomas²  Martin F Gardner²  Myriam Gaudeul¹ 

[1] UMR CNRS-MNHN-UPMC-EPHE 7205 ‘Institut de Systématique, Evolution, Biodiversité’, Muséum National d’Histoire Naturelle, 16 rue Buffon, CP 39, Paris, F-75005, France;Royal Botanic Garden Edinburgh, Edinburgh EH3 5LR, United Kingdom;Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, Edinburgh EH3 9JT, United Kingdom

关键词: Systematics;    Population genetics;    Phylogeography;    Introgression;    Hybridization;    Hotspot;    Diversification;    Conifers;    Closely related species;    Admixture;   

Others  :  1117959
DOI  :  10.1186/s12862-014-0171-6

 received in 2014-03-06, accepted in 2014-07-23,  发布年份 2014

【 摘 要 】

Background

New Caledonia harbours a highly diverse and endemic flora, and 13 (out of the 19 worldwide) species of Araucaria are endemic to this territory. Their phylogenetic relationships remain largely unresolved. Using nuclear microsatellites and chloroplast DNA sequencing, we focused on five closely related Araucaria species to investigate among-species relationships and the distribution of within-species genetic diversity across New Caledonia.

Results

The species could be clearly distinguished here, except A. montana and A. laubenfelsii that were not differentiated and, at most, form a genetic cline. Given their apparent morphological and ecological similarity, we suggested that these two species may be considered as a single evolutionary unit. We observed cases of nuclear admixture and incongruence between nuclear and chloroplast data, probably explained by introgression and shared ancestral polymorphism. Ancient hybridization was evidenced between A. biramulata and A. laubenfelsii in Mt Do, and is strongly suspected between A. biramulata and A. rulei in Mt Tonta. In both cases, extensive asymmetrical backcrossing eliminated the influence of one parent in the nuclear DNA composition. Shared ancestral polymorphism was also observed for cpDNA, suggesting that species diverged recently, have large effective sizes and/or that cpDNA experienced slow rates of molecular evolution. Within-species genetic structure was pronounced, probably because of low gene flow and significant inbreeding, and appeared clearly influenced by geography. This may be due to survival in distinct refugia during Quaternary climatic oscillations.

Conclusions

The study species probably diverged recently and/or are characterized by a slow rate of cpDNA sequence evolution, and introgression is strongly suspected. Within-species genetic structure is tightly linked with geography. We underline the conservation implications of our results, and highlight several perspectives.

【 授权许可】

   
2014 Gaudeul et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Degnan JH, Rosenberg NA: Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol 2009, 24:332-340.
• [2]Joly S, Bruneau A: Incorporating allelic variation for reconstructing the evolutionary history of organisms from multiple genes: an example from Rosa in North America. Syst Biol 2006, 55:623-636.
• [3]Linder CR, Rieseberg LH: Reconstructing patterns of reticulate evolution in plants. Am J Bot 2004, 91:1700-1708.
• [4]Maddison WP, Knowles LL: Inferring phylogeny despite incomplete lineage sorting. Syst Biol 2006, 55:21-30.
• [5]Pillon Y, Johansen JB, Sakishima T, Roalson EH, Price DK, Stacy EA: Gene discordance in phylogenomics or recent plant radiations, an example from Hawaiian Cyrtandra (Gesneriaceae). Mol Phylogenet Evol 2013, 69:293-298.
• [6]Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GA, Kent J: Biodiversity Hotspots for conservation priorities. Nature 2000, 403:853-858.
• [7]Jaffré T, Morat P, Veillon J-M, Rigault F, Dagostini G: Composition and Characterisation of the Native Flora of New Caledonia. In Documents Scientifiques et Techniques. Institut de Recherche pour le Développement Nouméa, New Caledonia; 2001:1-121.
• [8]Grandcolas P, Murienne J, Robillard T, Desutter-Grandcolas L, Jourdan H, Guilbert E, Deharveng L: New Caledonia: a very old Darwinian island? Philos T R Soc B 2008, 363:3309-3317.
• [9]Espeland M, Murienne J: Diversity dynamics in New Caledonia: towards the end of the museum model? BMC Evol Biol 2011, 11:254. BioMed Central Full Text
• [10]Aitchison JC, Clarke GL, Meffre S, Cluzel D: Eocene arc-continent collision in New Caledonia and implications for regional Southwest Pacific tectonic evolution. Geology 1995, 23:161-164.
• [11]Pelletier B: Geology of the New Caledonia Region and its Implications for the Study of the New Caledonian Biodiversity. In Compendium of Marine Species of New Caledonia. Documents Scientifiques et Techniques, vol. II7. Institut de Recherche pour le Développement Nouméa, New Caledonia; 2006:19-32.
• [12]Cruaud A, Jabbour-Zahab R, Genson G, Ungricht S, Rasplus J-Y: Testing the ermergence of New Caledonia: Fig wasp mutualism as a case study and a review of evidence. PLoS One 2012, 7:e30941.
• [13]Pillon Y: Time and tempo of diversification in the flora of New Caledonia. Bot J Linn Soc 2012, 170:288-298.
• [14]Buerki S, Forest F, Callmander MW, Lowry PP II, Devey DS, Munzinger J: Phylogenetic inference of New Caledonian lineages of Sapindaceae: molecular evidence requires a reassessment of generic circumscriptions. Taxon 2012, 61:109-119.
• [15]Duangjai S, Samuel R, Munzinger J, Forest F, Wallnöfer B, Barfuss MHJ, Fischer G, Chase MW: A multi-locus plastid phylogenetic analysis of the pantropical genus Diospyros (Ebenaceae), with an emphasis on the radiation and biogeography origins of the New Caledonian endemic species. Mol Phylogenet Evol 2009, 52:602-620.
• [16]Morat P, Jaffré T, Tronchet F, Munzinger J, Pillon Y, Veillon J-M, Chalopin M: The taxonomic database « FLORICAL » and characteristics of the indigenous flora of New Caledonia. Adansonia 2012, 34:177-219.
• [17]Swenson U, Munzinger J: Taxonomic revision of Pycnandra subgenus Trouettia (Sapotaceae), with six new species from New Caledonia. Aust Syst Bot 2010, 23:333-370.
• [18]Pascal M, de Forges BR, Le Guyader H, Simberloff D: Mining and other Ttreats to the New Caledonia biodiversity hotspot. Conserv Biol 2008, 22:498-499.
• [19]Pillon Y, Munzinger J: Amborella fever and its (little) implication in conservation. Trends Plant Sci 2005, 10:519-520.
• [20]Barrabé L, Maggia L, Pillon Y, Rigault F, Mouly A, Davis AP, Buerki S: New Caledonian lineages of Psychotria (Rubiaceae) reveal different evolutionary histories and the largest documented plant radiation for the archipelago. Mol Phylogenet Evol 2013, 71:15-35.
• [21]Eibl JM, Plunkett GM, Lowry PP II: Evolution of Polyscias sect. Tieghemopanax (Araliaceae) based on nuclear and chloroplast DNA sequence data. Adansonia 2001, 23:23-48.
• [22]Pillon Y, Hopkins HCF, Munzinger J, Amir H, Chase MW: Cryptic species, gene recombination, and hybridization in the genus Spiraeanthemum (Cunoniaceae) from New Caledonia. Bot J Linn Soc 2009, 161:137-152.
• [23]Pillon Y, Munzinger J, Amir H, Hopkins HCF, Chase MW: Reticulate evolution on a mosaic of soils diversification of the NC endemic genus Codia. Mol Ecol 2009, 18:2263-2275.
• [24]Turner B, Paun O, Munzinger J, Duangjai S, Chase MW, Samuel R: Analyses of amplified fragment length polymorphisms (AFLP) indicate rapid radiation of Diospyros species (Ebenaceae) endemic to New Caledonia. BMC Evol Biol 2013, 13:269. BioMed Central Full Text
• [25]Bottin L, Verhaegen D, Tassin J, Olivieri I, Vaillant A, Bouvet J-M: Genetic diversity and population structure of an insular tree, Santalum austrocaledonicum in New Caledonian archipelago. Mol Ecol 2005, 14:1979-1989.
• [26]Bottin L, Tassin J, Nasi R, Bouvet J-M: Molecular, quantitative and abiotic variables for the delineation of evolutionary significant units: case of sandalwood (Santalum austrocaledonicum Vieillard) in New Caledonia. Conserv Genet 2007, 8:99-109.
• [27]Herbert J, Hollingsworth PM, Gardner MF, Mill RR, Thomas PI, Jaffré T: Conservation genetics and phylogenetics of New Caledonian Retrophyllum (Podocarpaceae) species. New Zeal J Bot 2002, 40:175-188.
• [28]Kettle CJ, Hollingsworth PM, Jaffré T, Moran B, Ennos RA: Identifying the early genetic consequences of habitat degradation in a highly threatened tropical conifer, Araucaria nemorosa Laubenfels. Mol Ecol 2007, 16:3581-3591.
• [29]Kurata K, Jaffré T, Setoguchi H: Genetic diversity and geographical structure if the pitcher plant Nepenthes viellardii in New Caledonia; a chloroplast DNA haplotypes analysis. Am J Bot 2008, 95:1632-1644.
• [30]Poncet V, Munoz F, Munzinger J, Pillon Y, Gomez C, Couderc M, Tranchant-Dubreuil C, Hamon S, de Kochko A: Phylogeography and niche modelling of the relict plant Amborella trichopoda (Amborellaceae) reveal multiple Pleistocene refugia in New Caledonia. Mol Ecol 2013, 22:6163-6178.
• [31]Stevenson J, Hope G: A comparison of late Quaternary forest changes in New Caledonia and northeastern Australia. Quaternary Res 2005, 64:382-383.
• [32]Pintaud J-C, Jaffré T, Puig H: Chorology of New Caledonian palms and possible evidence of Pleistocene rain forest refugia. C R Acad Sci 2001, 324:453-463.
• [33]Hewitt GM: Genetic consequences of climatic oscillations in the Quaternary. Philos T R Soc B 2004, 359:183-195.
• [34]Gaudeul M, Rouhan G, Gardner MF, Hollingsworth PM: AFLP markers provide insights into the evolutionary relationships and diversification of New Caledonian Araucaria species. Am J Bot 2012, 99:68-81.
• [35]Proctor J: Vegetation and soil and plant chemistry on ultramafic rocks in the tropical Far East. Perspect Plant Ecol 2003, 6:105-124.
• [36]Kettle CJ: Conservation Genetics of New Caledonian Araucaria. PhD Dissertation: University of Edinburgh; 2006.
• [37]Setoguchi H, Osawa TA, Pintaud J-C, Jaffré T, Veillon J-M: Phylogenetic relationship within Araucariaceae based on rbcL genes sequences. Am J Bot 1998, 85:1507-1516.
• [38]de Laubenfels DJ: Gymnospermes. In Flore de la Nouvelle-Calédonie et Dépendances, vol. 4. Muséum National d’Histoire Naturelle, Paris; 1972.
• [39]Jaffré T, Munzinger J, Lowry PP II: Threats to the conifer species on New Caledonia’s ultramafic massifs and proposals for urgently needed measures to improve their protection. Biodivers Conserv 2010, 19:1485-1502.
• [40]Rigg LS, Enright NJ, Jaffré T, Perry GLW: Contrasting population dynamics of the endemic New Caledonian conifer Araucaria laubenfelsii in maquis and rain forest. Biotropica 2005, 42:479-487.
• [41]Kettle CJ, Ennos RA, Jaffré T, Gardner M, Hollingsworth PM: Cryptic genetic bottlenecks during restoration of an endangered tropical conifer. Biol Conserv 2008, 141:1953-1961.
• [42]Kettle CJ, Ennos RA, Jaffré T, McCoy S, Le Borgne T, Gardner M, Hollingsworth PM: Importance of demography and dispersal for the resilience and restoration of a critically endangered tropical conifer Araucaria nemorosa. Divers Distrib 2012, 18:248-259.
• [43]Burgarella C, Lorenzo Z, Jabbour-Zahab R, Lumaret R, Guichoux E, Petit RJ, Soto A, Gil L: Detection of hybrids in nature: application to oaks (Quercus suber and Q. ilex). Heredity 2009, 102:442-452.
• [44]Krak K, Caklova P, Chrtek J, Fehrer J: Reconstruction of phylogenetic relationships in a highly reticulate group with deep coalescence and recent speciation. Heredity 2013, 110:138-151.
• [45]Ramadugu C, Pfeil BE, Keremane ML, Lee RF, Maureira-Butler IJ, Roose ML: A six nuclear gene phylogeny of Citrus (Rutaceae) taking into account hybridization and lineage sorting. PLoS One 2013, 8:e68410.
• [46]Bouillé M, Bousquet J: Trans-species shared polymorphisms at orthologous nuclear gene loci among distant species in the conifer Picea (Pinaceae): implications for the long-term maintenance of genetic diversity in trees. Am J Bot 2005, 92:63-73.
• [47]Birky CW Jr, Fuerst P, Maruyama T: Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 1989, 121:613-627.
• [48]Robertson A, Hollingsworth PM, Kettle CJ, Ennos RA, Gardner MF: Characterization of nuclear microsatellites in New Caledonian Araucaria species. Mol Ecol Notes 2004, 4:62-63.
• [49]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
• [50]Demesure B, Sodzi N, Petit RJ: A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 1995, 4:129-131.
• [51]Grivet D, Heinze B, Vendramin GG, Petit RJ: Genome walking with consensus primers: application to the large single copy region of chloroplast DNA. Mol Ecol Notes 2001, 1:345-349.
• [52]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
• [53]Falush D, Stephens M, Pritchard JK: Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 2003, 164:1567-1587.
• [54]Earl DA, von Holdt BM: STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 2012, 4:359-361.
• [55]Evanno G, Regnault S, Goudet J: Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 2005, 14:2611-2620.
• [56]Bryant D, Moulton V: Neighbor-Net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 2004, 21:255-265.
• [57]Morrison DA: Networks in phylogenetic analysis: new tools for population biology. Int J Parasitol 2005, 35:567-582.
• [58]Huson DH, Bryant D: Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006, 23:254-267.
• [59]Weir BS, Cockerham CC: Estimating F-statistics for the analysis of population structure. Evolution 1984, 38:1358-1370.
• [60]Goudet J: FSTAT, version 1.2. A computer program to calculate F-statistics. J Hered 1995, 86:485-486.
• [61]Excoffier L, Laval G, Schneider S: Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 2005, 1:47-50.
• [62]El Mousadik A, Petit RJ: Chloroplast DNA phylogeography of the argan tree of Morocco. Mol Ecol 1996, 5:547-555.
• [63]Cornuet J-M, Luikart G: Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 1996, 144:2001-2014.
• [64]Raymond M, Rousset F: GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 1995, 86:248-249.
• [65][http://biodiversityinformatics.amnh.org/open_source/gdmg] webcite Ersts PJ: Geographic Distance Matrix Generator (version 1.2.3). []
• [66]Hardy OJ, Vekemans X: SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2002, 2:618-620.
• [67]Hardy OJ, Charbonnel N, Fréville H, Heuertz M: Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 2003, 163:1467-1482.
• [68]Rosenberg N: DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 2004, 4:137-138.
• [69]Du FK, Petit RJ, Liu JQ: More introgression with less gene flow: chloroplast vs. mitochondrial DNA in the Picea asperata complex in China, and comparison with other Conifers. Mol Ecol 2009, 18:1396-1407.
• [70]Ma X-F, Szmidt AE, Wang X-R: Genetic structure and evolutionary history of a diploid hybrid pine Pinus densata inferred from the nucleotide variation at seven gene loci. Mol Biol Evol 2006, 23:807-816.
• [71]Perron M, Bousquet J: Natural hybridization between black spruce and red spruce. Mol Ecol 1997, 6:725-734.
• [72]Hamrick JL, Godt MJW, Sherman-Broyles SL: Factors Influencing Levels of Genetic Diversity in Woody Plant Species. In Population Genetics of Forest Trees. Edited by Adams WT, Strauss SH, Copes DL, Griffin AR. Kluwer Academic Publishers, Boston; 1992:95-124.
• [73]Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG: Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 2005, 14:189-701.
• [74]O’Connell LM, Mosseler A, Rajora OP: Extensive long-distance pollen dispersal in a fragmented landscape maintains genetic diversity in white spruce. J Hered 2007, 98:640-645.
• [75]Aguirre-Planter E, Furnier GR, Eguiarte LE: Low levels of genetic variation and high levels of genetic differentiation among populations of species of Abies from southern Mexico and Guatemala. Am J Bot 2000, 87:362-371.
• [76]Bekessy SA, Allnutt TR, Premoli AC, Lara A, Ennos RA, Burgman MA, Cortes M, Newton AC: Genetic variation in the vulnerable and endemic monkey puzzle tree, detected using RAPDs. Heredity 2002, 88:243-249.
• [77]Pye MG, Henwood MJ, Gadek PA: Differential levels of genetic diversity and divergence among populations of an ancient Australian rainforest conifer, Araucaria cunninghamii. Plant Syst Evol 2009, 277:173-185.
• [78]Pye MG, Gadek PA: Genetic diversity, differentiation and conservation in Araucaria bidwillii (Araucariaceae), Australia’s Bunya pine. Conserv Genet 2004, 5:619-629.
• [79]de Souza MIF, Salgueiro F, Carnavale-Bottino M, Félix DB, Alvez-Ferreira M, Bittencourt JVM, Margis R: Patterns of genetic diversity in southern and southeastern Araucaria angustifolia (Bert.) O. Kuntze relict populations. Genet Mol Biol 2009, 32:546-556.
• [80]Stefenon VM, Gailing O, Finkeldey R: Genetic structure of Araucaria angustifolia (Araucariaceae) populations in Brazil: implications for the in situ conservation of genetic resources. Plant Biology 2007, 9:516-525.
• [81]Schlögl PS, de Souza AP, Nodari RO: PCR-RFLP analysis of non-coding regions of cpDNA in Araucaria angustifolia (Bert.) O. Kuntze. Genet Mol Biol 2007, 30:423-427.
• [82]Ruiz E, Gonzalez F, Torres-Diaz C, Fuentes G, Mardones M, Stuessy T, Samuel R, Becerra J, Silva M: Genetic Diversity and differentiation within and among Chilean populations of Araucaria araucana (Araucariaceae) based on allozyme variability. Taxon 2007, 56:1221-1228.
• [83]Moritz C: Defining ‘evolutionary significant units’ for conservation. Trends Ecol Evol 1994, 9:373-375.
• [84]Thompson J, Gaudeul M, Debussche M: Conservation value of sites of hybridization in peripheral populations of rare plant species. Conserv Biol 2010, 24:236-245.
• [85]Levin DA, Francisco-Ortega J, Jansen RK: Hybridization and the extinction of rare plant species. Conserv Biol 1996, 10:10-16.
• [86]Lowe AJ, Boshier D, Ward M, Bacles CFE, Navarro C: Genetic resource impacts of habitat loss and degradation: reconciling empirical evidence and predicted theory for neotropical trees. Heredity 2005, 95:255-273.
• [87]Semerikov VL, Lascoux M: Nuclear and cytoplasmic variation within and between Eurasian Larix (Pinaceae) species). Am J Bot 2003, 90:1113-1123.
• [88]Petit RJ, Kremer A, Wagner DB: Finite island model for organelle and nuclear genes in plants. Heredity 1993, 71:630-641.