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PLOS ONE  2011 

Macroevolutionary Patterns in the Aphidini Aphids (Hemiptera: Aphididae): Diversification, Host Association, and Biogeographic Origins

DOI: 10.1371/journal.pone.0024749

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Abstract:

Background Due to its biogeographic origins and rapid diversification, understanding the tribe Aphidini is key to understanding aphid evolution. Major questions about aphid evolution include origins of host alternation as well as age and patterns of diversification in relation to host plants. To address these questions, we reconstructed the phylogeny of the Aphidini which contains Aphis, the most diverse genus in the family. We used a combined dataset of one nuclear and four mitochondrial DNA regions. A molecular dating approach, calibrated with fossil records, was used to estimate divergence times of these taxa. Principal Findings Most generic divergences in Aphidini occurred in the Middle Tertiary, and species-level divergences occurred between the Middle and Late Tertiary. The ancestral state of host use for Aphidini was equivocal with respect to three states: monoecy on trees, heteroecy, and monoecy on grasses. The ancestral state of Rhopalosiphina likely included both heteroecy and monoecy, whereas that of Aphidina was most likely monoecy. The divergence times of aphid lineages at the generic or subgeneric levels are close to those of their primary hosts. The species-level divergences in aphids are consistent with the diversification of the secondary hosts, as a few examples suggest. The biogeographic origin of Aphidini as a whole was equivocal, but the major lineages within Aphidina likely separated into Nearctic, Western Palearctic, and Eastern Palearctic regions. Conclusions Most generic divergences in Aphidini occurred in the Middle Tertiary when primary hosts, mainly in the Rosaceae, were diverging, whereas species-level divergences were contemporaneous with diversification of the secondary hosts such as Poaceae in the Middle to Late Tertiary. Our results suggest that evolution of host alternation within Aphidini may have occurred during the Middle Tertiary (Oligocene) when the secondary hosts emerged.

 References

[1]  Dixon AFG (1987) The way of life of aphids: host specificity, speciation and distribution. In: Minks AK, Harrewijn P, editors. Aphids their biology, natural enemies and control, Vol A. Amsterdam: Elsevier. pp. 197–207.
[2]  Blackman RL, Eastop VF (1994) Aphids on the World's Trees: An Identification and Information Guide. Wallingford: CAB International. 987 p.
[3]  Blackman RL, Eastop VF (2000) Aphids on the World's Crops: An Identification and Information Guide. Chichester: John Wiley & Sons Ltd. 466 p.
[4]  Moran NA (1988) The evolution of host-plant alternation in aphids: Evidence for specialization as a dead end. The American Naturalist 132: 681–706.
[5]  Moran NA (1992) The evolution of aphid life cycles. Annual Review of Entomology 37: 321–348.
[6]  Mitter C, Farrell B, Futuyma D (1991) Phylogenetic studies of insect-plant interactions: Insights into the genesis of diversity. Trends in Ecology and Evolution 6: 290–293.
[7]  Farrell BD, Mitter C (1998) The timing of insect/plant diversification: Might Tetraopes (Coleoptera: Cerambycidae) and Asclepias (Asclepiadaceae) have co-evolved? Biological Journal of the Linnean Society 63: 553–577.
[8]  Weiblen GD (2001) Phylogenetic relationships of fig wasps pollinating functionally dioecious Ficus based on mitochondrial DNA sequences and morphology. Systematic Biology 50: 243–267.
[9]  Futuyma DJ, Agrawal AA (2009) Macroevolution and the biological diversity of plants and herbivores. Proceedings of the National Academy of Sciences of the United States of America 106: 18054–18061.
[10]  Lopez-Vaamonde C, Wikstr？m N, Kjer KM, Weiblen GD, Rasplus JY, et al. (2009) Molecular dating and biogeography of fig-pollinating wasps. Molecular Phylogenetics and Evolution 52: 715–726.
[11]  Lopez-Vaamonde C, Wikstr？m N, Labandeira C, Godfray HCJ, Goodman SJ, et al. (2006) Fossil-calibrated molecular phylogenies reveal that leaf-mining moths radiated millions of years after their host plants. Journal of Evolutionary Biology 19: 1314–1326.
[12]  Lopez-Vaamonde C, Rasplus JY, Weiblen GD, Cook JM (2001) Molecular phylogenies of fig wasps: Partial cocladogenesis of pollinators and parasites. Molecular Phylogenetics and Evolution 21: 55–71.
[13]  Percy DM, Page RDM, Cronk QCB (2004) Plant-insect interactions: Double-dating associated insect and plant lineages reveals asynchronous radiations. Systematic Biology 53: 120–127.
[14]  Blackman RL, Eastop VF (2006) Aphids on the World's Herbaceous Plants and Shrubs, Vol. 2, The Aphids. Chichester: John Wiley & Sons Ltd. pp. 1025–1439.
[15]  Heie OE (1987) Paleontology and phylogeny. In: Minks AK, Harrewijn P, editors. Aphids Their Biology, Natural Enemies and Control, vol A. Amsterdam: Elsevier. pp. 367–391.
[16]  von Dohlen CD, Moran NA (2000) Molecular data support a rapid radiation of aphids in the Cretaceous and multiple origins of host alternation. Biological Journal of the Linnean Society 71: 689–717.
[17]  Favret C (2011) Aphid Species File. Version 1.0/4.0. Available at: http://Aphid.SpeciesFile.org. Accessed 2011 Mar 11.
[18]  Wojciechowski W (1992) Studies on the Systematic System of Aphids (Homoptera, Aphidinea). Katowice: Uniwersytet Slaski.
[19]  Heie OE (1994) Aphid ecology in the past and a new view on the evolution of Macrosiphini. In: Leather SR, editor. Individuals, Populations and Patterns in Ecology. Andover, Hampshire, UK: Intercept Ltd. pp. 409–418.
[20]  Moran NA (1990) Aphid life cycles: Two evolutionary steps. The American Naturalist 136: 135–138.
[21]  von Dohlen CD, Rowe CA, Heie OE (2006) A test of morphological hypotheses for tribal and subtribal relationships of Aphidinae (Insecta: Hemiptera: Aphididae) using DNA sequences. Molecular Phylogenetics and Evolution 38: 316–329.
[22]  Havill NP, Foottit RG, von Dohlen CD (2007) Evolution of host specialization in the Adelgidae (Insecta: Hemiptera) inferred from molecular phylogenetics. Molecular Phylogenetics and Evolution 44: 357–370.
[23]  Foottit RG, Maw HEL, Von Dohlen CD, Hebert PDN (2008) Species identification of aphids (Insecta: Hemiptera: Aphididae) through DNA barcodes. Molecular Ecology Resources 8: 1189–1201.
[24]  Remaudiere G, Remaudiere M (1997) Catalogue des Aphididae du Monde. Homoptera Aphidoidea; Catalogue of the world's Aphididae. Paris: INRA. 473 p.
[25]  von Dohlen CD, Teulon DAJ (2003) Phylogeny and historical biogeography of New Zealand indigenous aphidini aphids (Hemiptera, Aphididae): An hypothesis. Annals of the Entomological Society of America 96: 107–116.
[26]  Kim H, Lee S (2008) A molecular phylogeny of the tribe Aphidini (Insecta: Hemiptera: Aphididae) based on the mitochondrial tRNA/COII, 12S/16S and the nuclear EF1α genes. Systematic Entomology 33: 711–721.
[27]  Kim H, Lee W, Lee S (2010) Morphometric relationship, phylogenetic correlation, and character evolution in the species-rich genus Aphis (Hemiptera: Aphididae). PLoS One 5: e11608.
[28]  Kim H, Hoelmer KA, Lee W, Kwon YD, Lee S (2010) Molecular and morphological identification of the soybean aphid and other Aphis species on the primary host Rhamnus davurica in Asia. Annals of the Entomological Society of America 103: 532–543.
[29]  Turcinaviciene J, Rakauskas R, Pedersen BV (2006) Phylogenetic relationships in the “grossulariae” species group of the genus Aphis (Hemiptera: Sternorrhyncha: Aphididae): Molecular evidence. European Journal of Entomology 103: 597–604.
[30]  Coeur d'acier A, Jousselin E, Martin JF, Rasplus JY (2007) Phylogeny of the genus Aphis Linnaeus, 1758 (Homoptera: Aphididae) inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 42: 598–611.
[31]  Thao ML, Baumann L, Baumann P (2004) Organization of the mitochondrial genomes of whiteflies, aphids, and psyllids (Hemiptera, Sternorrhyncha). BMC Evolutionary Biology 4: 25.
[32]  Carletto J, Blin A, Vanlerberghe-Masutti F (2009) DNA-based discrimination between the sibling species Aphis gossypii Glover and Aphis frangulae Kaltenbach. Systematic Entomology 34: 307–314.
[33]  Yang ZX, Chen XM, Havill NP, Feng Y, Chen H (2010) Phylogeny of Rhus gall aphids (Hemiptera: Pemphigidae) based on combined molecular analysis of nuclear EF1 alpha and mitochondrial COII genes. Entomological Science 13: 351–357.
[34]  Qiao G, Wang J, Zhang G (2008) Toxoptera Koch (Hemiptera: Aphididae), a generic account, description of a new species from China, and keys to species. Zootaxa 1746: 1–14.
[35]  Martinez-Torres D, Buades C, Latorre A, Moya A (2001) Molecular systematics of aphids and their primary endosymbionts. Molecular Phylogenetics and Evolution 20: 437–449.
[36]  Ortiz-Rivas B, Martinez-Torres D (2010) Combination of molecular data support the existence of three main lineages in the phylogeny of aphids (Hemiptera: Aphididae) and the basal position of the subfamily Lachninae. Molecular Phylogenetics and Evolution 55: 305–317.
[37]  Moran NA (1989) A 48-million-year-old aphid-host plant association and complex life cycle: biogeographic evidence. Science 245: 173–175.
[38]  Moran NA, Munson MA, Baumann P, Ishikawa H (1993) A Molecular Clock in Endosymbiotic Bacteria is Calibrated Using the Insect Hosts. Proceedings of the Royal Society of London Series B-Biological Sciences 253: 167–171.
[39]  Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.
[40]  Stern DL (1994) A phylogenetic analysis of soldier evolution in the aphid family Hormaphididae. Proceedings of the Royal Society of London Series B-Biological Sciences 256: 203–209.
[41]  Normark BB (1996) Phylogeny and evolution of parthenogenetic weevils of the Aramigus tessellatus species complex (Coleoptera: Curculionidae: Naupactini): Evidence from mitochondrial DNA sequences. Evolution 50: 734–745.
[42]  Harry M, Solignac M, Lachaise D (1998) Molecular evidence for parallel evolution of adaptive syndromes in fig-breeding Lissocephala (Drosophilidae). Molecular Phylogenetics and Evolution 9: 542–551.
[43]  Jermiin L, Crozier RH (1994) The cytochrome b region in the mitochondrial DNA of the ant Tetraponera rufoniger: sequence divergence in Hymenoptera may be associated with nucleotide content. Journal of Molecular Evolution 38: 282–294.
[44]  Simon C, Frati F, Beckenbach A, Crespi B, Liu H, et al. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene-sequences and a compilation of conserved polymerase chain-reaction primers. Annals of the Entomological Society of America 87: 651–701.
[45]  Simon C, Franke A, Martin A (1991) The polymerase chain reaction: DNA extraction and amplication. In: Hewitt GM, Johnston AWB, Young JPW, editors. Molecular Techniques in Taxonomy. Berlin: Springer. 410 p.
[46]  Palumbi SR (1996) Nucleic acids II: The polymerase chain reaction. In: Hillis DM, editor. Molecular Systematics. Sunderland: Sinauer Press. pp. 205–247.
[47]  von Dohlen CD, Kurosu U, Aoki S (2002) Phylogenetics and evolution of the eastern Asian-eastern North American disjunct aphid tribe, Hormaphidini (Hemiptera: Aphididae). Molecular Phylogenetics and Evolution 23: 257–267.
[48]  Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24: 4876–4882.
[49]  Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics 9: 299–306.
[50]  Castresana J (2002) GBLOCLKS: Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Version 0.91b. Copyrighted by J. Castresana, EMBL.
[51]  Swofford DL (1998) PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods), Version 4.0b10. Sunderland, MA: Sinauer Associates.
[52]  Farris JS, Kallersjo M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10: 315–319.
[53]  Nylander J (2004) MrModeltest 2.0. Program distributed by the author. Uppsala university, Evolutionary biology centre.
[54]  Posada D, Crandall KA (1998) MODELTEST: Testing the model of DNA substitution. Bioinformatics 14: 817–818.
[55]  Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: Advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53: 793–808.
[56]  Posada D (2008) jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.
[57]  Stamatakis A (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.
[58]  Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
[59]  Rambaut A, Drummond AJ (2009) Tracer v1.5. Available at: http://beast.bio.ed.ac.uk/tracer. Accessed 2011 Mar 11.
[60]  Dunn KA, McEachran JD, Honeycutt RL (2003) Molecular phylogenetics of myliobatiform fishes (Chondrichthyes: Myliobatiformes), with comments on the effects of missing data on parsimony and likelihood. Molecular Phylogenetics and Evolution 27: 259–270.
[61]  Wiens JJ (2003) Missing data, incomplete taxa, and phylogenetic accuracy. Systematic Biology 52: 528–538.
[62]  Wiens JJ (2003) Incomplete taxa, incomplete characters, and phylogenetic accuracy: Is there a missing data problem? Journal of Vertebrate Paleontology 23: 297–310.
[63]  Philippe H, Snell EA, Bapteste E, Lopez P, Holland PWH, et al. (2004) Phylogenomics of eukaryotes: Impact of missing data on large alignments. Molecular Biology and Evolution 21: 1740–1752.
[64]  Fulton TL, Strobeck C (2006) Molecular phylogeny of the Arctoidea (Carnivora): Effect of missing data on supertree and supermatrix analyses of multiple gene data sets. Molecular Phylogenetics and Evolution 41: 165–181.
[65]  Bouchenak-Khelladi Y, Salamin N, Savolainen V, Forest F, van der Bank M, et al. (2008) Large multi-gene phylogenetic trees of the grasses (Poaceae): Progress towards complete tribal and generic level sampling. Molecular Phylogenetics and Evolution 47: 488–505.
[66]  Wiens JJ (2005) Can incomplete taxa rescue phylogenetic analyses from long-branch attraction? Systematic Biology 54: 731–742.
[67]  Wiens JJ (2006) Missing data and the design of phylogenetic analyses. Journal of Biomedical Informatics 39: 34–42.
[68]  Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. Journal of Molecular Evolution 29: 170–179.
[69]  Shimodaira H (2002) An approximately unbiased test of phylogenetic tree selection. Systematic Biology 51: 492–508.
[70]  Maddison WP, Maddison DR (2007) Mesquite: A modular system for evolutionary analysis. Version 2.6. Available at: http://mesquiteproject.org. Accessed 2011 Mar 11.
[71]  Yang Z (1997) PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555–556.
[72]  Shimodaira H, Hasegawa M (2001) CONSEL: For assessing the confidence of phylogenetic tree selection. Bioinformatics 17: 1246–1247.
[73]  Heie OE (1994) The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. V. Family Aphididae: Part 2 of tribe Macrosiphini of subfamily Aphidinae, and family Lachninae. Leiden, Netherlands: E.J. Brill/Scandinavian Science Press Ltd. 242 p.
[74]  Clark MA, Moran NA, Baumann P (1999) Sequence evolution in bacterial endosymbionts having extreme base compositions. Molecular Biology and Evolution 16: 1586–1598.
[75]  Kishino H, Thorne JL, Bruno WJ (2001) Performance of a divergence time estimation method under a probabilistic model of rate evolution. Molecular Biology and Evolution 18: 352–361.
[76]  Thorne JL, Kishino H (2002) Divergence time and evolutionary rate estimation with multilocus data. Systematic Biology 51: 689–702.
[77]  Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.
[78]  Gradstein FM, Ogg JG (2004) Geologic Time Scale 2004 - Why, how, and where next! Lethaia 37: 175–181.
[79]  Rutschmann F (2005) Bayesian molecular dating using PAML/multidivtime. A step-by-step manual. University of Zurich, Switzerland. Available at http://www.plant.ch. Accessed 2011 Mar 11.
[80]  Felsenstein J (1984) DNAML in PHYLIP 2.6. University of Washington, Seattle.:. Available at: http://evolution.genetics.washington.edu. Accessed 2011 Mar 11.
[81]  Rambaut A (2009) FigTree v1.3.1. Available at: http://tree.bio.ed.ac.uk/software/figtre？e. Accessed 2011 Mar 11.
[82]  Pagel M, Meade A, Barker D (2004) Bayesian estimation of ancestral character states on phylogenies. Systematic Biology 53: 673–684.
[83]  Pagel M, Meade A (2007) BayesTraits, version 1.0 - Draft Manual. Available at: http://www.evolution.rdg.ac.uk. Accessed 2011 Mar 11.
[84]  Stroyan HLG (1984) Aphids–Pterocommatinae and Aphidinae (Aphidini) Homoptera, Aphididae. Handbk. Ident. Br. Insects 2, pt. 6. London: Dramrite Printers Ltd.
[85]  Heie OE (1986) The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. III. Family Aphididae: subfamily Pterocommatinae & tribe Aphidini of subfamily Aphidinae. Klampenborg, Denmark: Scandinavian Science Press Ltd.
[86]  Teulon DAJ, Stufkens MAW (1998) Current status of New Zealand indigenous aphids. Wellington, New Zealand: Department of Conservation. pp. 1–23.
[87]  Lee S, Holman J, Havelka J (2002) Illustrated Catalogue of Aphididae in the Korean Peninsula. Part I, Subfamily Aphidinae (Hemiptera: Sternorrhyncha). Daejoen, Rep. of Korea: Korea Research Institute of Bioscience and Biotechnology. 329 p.
[88]  Lee S, Kim H (2006) Economic Insects of Korea 28 (Insecta Koreana Suppl. 35), Aphididae: Aphidini (Hemiptera: Sternorrhyncha). Suwon, Rep. of Korea: National Institue of Agricultural Science and Technology.
[89]  Wikstr？m N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: Calibrating the family tree. Proceedings of the Royal Society of London Series B-Biological Sciences 268: 2211–2220.
[90]  Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, et al. (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596–1604.
[91]  Taylor TN, Taylor EL, Krings M (2009) Paleobotany, The biology and evolution of fossil plants. London: Academic Press, Ltd.
[92]  Kim KJ, Choi KS, Jansen RK (2005) Two chloroplast DNA inversions originated simultaneously during the early evolution of the sunflower family (Asteraceae). Molecular Biology and Evolution 22: 1783–1792.
[93]  Bremer K, Friis EM, Bremer B (2004) Molecular phylogenetic dating of asterid flowering plants shows early Cretaceous diversification. Systematic Biology 53: 496–505.
[94]  Bremer B, Eriksson T (2009) Time tree of Rubiaceae: Phylogeny and dating the family, subfamilies, and tribes. International Journal of Plant Sciences 170: 766–793.
[95]  Richardson JE, Chatrou LW, Mols JB, Erkens RHJ, Pirie MD (2004) Historical biogeography of two cosmopolitan families of flowering plants: Annonaceae and Rhamnaceae. Philosophical Transactions of the Royal Society B-Biological Sciences 359: 1495–1508.
[96]  Jian SG, Soltis PS, Gitzendanner MA, Moore MJ, Li R, et al. (2008) Resolving an ancient, rapid radiation in Saxifragales. Systematic Biology 57: 38–57.
[97]  Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Systematic Biology 54: 575–594.
[98]  Stefanovic S, Pfeil BE, Palmer JD, Doyle JJ (2009) Relationships among phaseoloid legumes based on sequences from eight chloroplast regions. Systematic Botany 34: 115–128.
[99]  Ford VS, Gottlieb LD (2007) Tribal relationships within Onagraceae inferred from PgiC sequences. Systematic Botany 32: 348–356.
[100]  Rutschmann F, Eriksson T, Abu Salim K, Conti E (2007) Assessing calibration uncertainty in molecular dating: The assignment of fossils to alternative calibration points. Systematic Biology 56: 591–608.
[101]  Vicentini A, Barber JC, Aliscioni SS, Giussani LM, Kellogg EA (2008) The age of the grasses and clusters of origins of C-4 photosynthesis. Global Change Biology 14: 2963–2977.
[102]  Mackenzie A, Dixon AFG (1990) Host alternation in aphids: Constraint versus optimization. The American Naturalist 136: 132–134.
[103]  Heie OE (1992) The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. IV. Family Aphididae: Part 1 of tribe Macrosiphini of subfamily Aphidinae. Leiden, Netherlands: E.J. Brill/Scandinavian Science Press Ltd.
[104]  Parham JF, Irmis RB (2008) Caveats on the use of fossil calibrations for molecular dating: A comment on near et al. The American Naturalist 171: 132–136.
[105]  Powell G, Tosh CR, Hardie J (2006) Host plant selection by aphids: Behavioral, evolutionary, and applied perspectives. Annual Review of Entomology 51: 309–330.
[106]  Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292: 686–693.
[107]  Yamamoto S, Sota T (2007) Phylogeny of the Geometridae and the evolution of winter moths inferred from a simultaneous analysis of mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution 44: 711–723.
[108]  Mackenzie A (1996) A trade-off for host plant utilization in the black bean aphid, Aphis fabae. Evolution 50: 155–162.
[109]  Kundu R, Dixon AFG (1995) Evolution of complex life cycles in aphids. Journal of Animal Ecology 64: 245–255.
[110]  Havill NP, Foottit RG (2007) Biology and evolution of Adelgidae. Annual Review of Entomology 52: 325–349.
[111]  Holman J (1987) Notes on Aphis species from the Soviet Far East, with descriptions of eight new species (Homoptera, Aphididae). Acta Entomologica Bohemoslovaca 84: 353–387.
[112]  Wang HC, Moore MJ, Soltis PS, Bell CD, Brockington SF, et al. (2009) Rosid radiation and the rapid rise of angiosperm-dominated forests. Proceedings of the National Academy of Sciences of the United States of America 106: 3853–3858.

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