The hyperdominant tropical tree Eschweilera coriacea (Lecythidaceae) shows higher genetic heterogeneity than sympatric Eschweilera species in French Guiana
PDF

Supplementary Files

Supplementary File 1
Supplementary File 2
Supplementary File 3
Supplementary File 4
Supplementary File 5

Keywords

Eschweilera
microsatellites
species delimitation
hyperdominant tropical trees
species complex
cryptic species

How to Cite

Heuertz, M., Caron, H., Scotti-Saintagne, C., Pétronelli, P., Engel, J., Tysklind, N., Miloudi, S., Gaiotto, F., Chave, J., Molino, J.-F., Sabatier, D., Loureiro, J. and Budde, K. (2020) “The hyperdominant tropical tree Eschweilera coriacea (Lecythidaceae) shows higher genetic heterogeneity than sympatric Eschweilera species in French Guiana”, Plant Ecology and Evolution, 153(1), pp. 67-81. doi: 10.5091/plecevo.2020.1565.

Abstract

Background and aims – The evolutionary history of Amazonia’s hyperabundant tropical tree species, also known as “hyperdominant” species, remains poorly investigated. We assessed whether the hyperdominant Eschweilera coriacea (DC.) S.A.Mori (Lecythidaceae) represents a single genetically cohesive species, and how its genetic constitution relates to other species from the same clade with which it occurs sympatrically in French Guiana.
Methods – We sampled 152 individuals in nine forest sites in French Guiana, representing 11 species of the genus Eschweilera all belonging to the Parvifolia clade, with emphasis on E. coriacea. Samples were genotyped at four simple sequence repeat (SSR) markers. We delimited gene pools, i.e., genetically coherent putative taxa, using STRUCTURE software and principal component analysis. We compared the genetic assignment of individuals with their morphological species determination and estimated genetic diversity and differentiation for gene pools and species. We also estimated genome size using flow cytometry.
Key results – SSR profiles commonly displayed up to four alleles per genotype, suggesting that the investigated Eschweilera species bear a paleopolyploid signature. Flow cytometry suggested that the studied species are diploid with haploid genome sizes of 871–1046 Mbp. We detected five gene pools and observed a good correspondence between morphological and genetic delimitation for Eschweilera sagotiana Miers and the undescribed morphospecies E. sp. 3 (which resembles E. grandiflora (Aubl.) Sandwith), and to a lesser extent for E. decolorans Sandwith and E. micrantha (O.Berg) Miers. Eschweilera coriacea was the most genetically diverse species and included individuals assigned to each gene pool.
Conclusions – We found no conclusive evidence for cryptic species within E. coriacea in French Guiana. SSRs detected fewer gene pools than expected based on morphology in the Parvifolia clade but discriminated evolutionary relationships better than available plastid markers. A positive trend between demographic abundance of species and allelic richness illustrates that hyperdominants may have a high evolutionary potential. This hypothesis can be tested using more powerful genomic data in combination with tree phenotypic trait variation and characterization of niche breadth, to enhance our understanding of the causes of hyperdominance in Amazonian trees.

https://doi.org/10.5091/plecevo.2020.1565
PDF

References

Allié E., Pélissier R., Engel J., Petronelli P., Freycon V., Deblauwe V., Soucémarianadin L., Weigel J., Baraloto C. (2015) Pervasive local-scale tree-soil habitat association in a tropical forest community. PLoS One 10(11): e0141488. https://doi.org/10.1371/journal.pone.0141488

Antonelli A., Sanmartín I. (2011) Why are there so many plant species in the Neotropics? Taxon 60(2): 403–414. https://doi.org/10.1002/tax.602010

Arellano G., Cala V., Macía M.J. (2014) Niche breadth of oligarchic species in Amazonian and Andean rain forests. Journal of Vegetation Science 25(6): 1355–1366. https://doi.org/10.1111/jvs.12180

Arellano G., Jørgensen P.M., Fuentes A.F., Loza M.I., Torrez V., Macía M.J. (2016) Oligarchic patterns in tropical forests: role of the spatial extent, environmental heterogeneity and diversity. Journal of Biogeography 43(3): 616–626. https://doi.org/10.1111/jbi.12653

Baraloto C., Hardy O.J., Paine C.E.T., Dexter K.G., Cruaud C., Dunning L.T., Gonzalez M.-A., Molino J.-F, Sabatier D., Savolainen V., Chave J. (2012) Using functional traits and phylogenetic trees to examine the assembly of tropical tree communities. Journal of Ecology 100(3): 690–701. https://doi.org/10.1111/j.1365-2745.2012.01966.x

Barthlott W., Hostert A., Kier G., Küper W., Kreft H., Mutke J., Rafiqpoor M.D., Sommer J.H. (2007) Geographic patterns of vascular plant diversity at continental to global scales (Geographische Muster der Gefäßpflanzenvielfalt im kontinentalen und globalen Maßstab). Erdkunde 61(4): 305–315. https://www.jstor.org/stable/25648042

Buckley D.P., O’Malley D.M., Apsit V., Prance G.T., Bawa K.S. (1988) Genetics of Brazil “Nut” (Berhollelia excelsa Humb. & Bonpl.: Lecythidaceae): I. Genetic variation in natural populations. Theoretical and Applied Genetics 76(6): 923–928. https://doi.org/10.1007/BF00273682

Caron H., Molino J.-F., Sabatier D., Léger P., Chaumeil P., Scotti-Saintagne C., Frigério J.-M., Scotti I., Franc A., Petit R.J. (2019) Chloroplast DNA variation in a hyperdiverse tropical tree community. Ecology and Evolution 9(8): 4897–4905. https://doi.org/10.1002/ece3.5096

Carstens B.C., Pelletier T.A., Reid N.M., Satler J.D. (2013) How to fail at species delimitation. Molecular Ecology 22(17): 4369–4383. https://doi.org/10.1111/mec.12413

Cavers S., Telford A., Arenal Cruz F., Pérez Castañeda A.J., Valencia R., Navarro C., Buonamici A., Lowe A., Vendramin G.G. (2013) Cryptic species and phylogeographical structure in the tree Cedrela odorata L. throughout the Neotropics. Journal of Biogeography 40(4): 732–746. https://doi.org/10.1111/jbi.12086

Charlesworth B. (2009) Effective population size and patterns of molecular evolution and variation. Nature Reviews Genetics 10: 195–210. https://doi.org/10.1038/nrg2526

Clark L.V., Jasieniuk M. (2011) POLYSAT: an R package for polyploid microsatellite analysis. Molecular Ecology Resources 11(3): 562–566. https://doi.org/10.1111/j.1755-0998.2011.02985.x

Daïnou K., Blanc-Jolivet C., Degen B., Kimani P., Ndiade-Bourobou D., Donkpegan A.S.L., Tosso F., Kaymak E., Bourland N., Doucet J.-L., Hardy O.J. (2016) Revealing hidden species diversity in closely related species using nuclear SNPs, SSRs and DNA sequences – a case study in the tree genus Milicia. BMC Evolutionary Biology 16: 259. https://doi.org/10.1186/s12862-016-0831-9

de Barros L.R.F, de Oliveira Wadt L.H., Mondin M., Pappas Junior. G., Rocha R.T., de Castro Rodrigues Pappas M., Kimura R.K., Martins K. (2019) Draft genome assembly of the tropical tree Bertholletia excelsa using long-read sequence data. In: XXV IUFRO World Congress, 29 sept - 5 October 2019, Curitiba, PR, Brazil, Abstracts: 318. Pesquisa Florestal Brasileira, Colombo, vol. 39, e201902043, Special issue.

Degnan J.H., Rosenberg N.A. (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends in Ecology & Evolution 24(6): 332–340. https://doi.org/10.1016/j.tree.2009.01.009

Doležel J., Greilhuber J., Lucretti S., Meister A., Lysák M.A., Nardi L., Obermayer R. (1998) Plant genome size estimation by flow cytometry: interlaboratory comparison. Annals of Botany 82(Suppl. A): 17–26. https://doi.org/10.1093/oxfordjournals.aob.a010312

De Queiroz K. (2007). Species concepts and species delimitation. Systematic Biology 56(6): 879–886. https://doi.org/10.1080/10635150701701083

Doyle J., Doyle J.L. (1987) Genomic plant DNA preparation from fresh tissue-CTAB method. Phytochemical Bulletin 19(1): 11–15.

Duminil J., Di Michele M. (2009) Plant species delimitation: a comparison of morphological and molecular markers. Plant Biosystems 143(3): 528–542. https://doi.org/10.1080/11263500902722964

Duminil J., Caron H., Scotti I., Cazal S.-O., Petit R. J. (2006) Blind population genetics survey of tropical rainforest trees. Molecular Ecology 15(12): 3505–3513. https://doi.org/10.1111/j.1365-294X.2006.03040.x

Duminil J., Heuertz M., Doucet J.-L., Bourland N., Cruaud C., Gavory F., Doumenge C., Navascués M., Hardy O.J. (2010) CpDNA-based species identification and phylogeography: application to African tropical tree species. Molecular Ecology 19(24): 5469–5483. https://doi.org/10.1111/j.1365-294X.2010.04917.x

Duminil J., Kenfack D., Viscosi V., Grumiau L., Hardy O.J. (2012) Testing species delimitation in sympatric species complexes: the case of an African tropical tree, Carapa spp. (Meliaceae) Molecular Phylogenetics and Evolution 62(1): 275–285. https://doi.org/10.1016/j.ympev.2011.09.020

Earl D.A., vonHoldt B.M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361. https://doi.org/10.1007/s12686-011-9548-7

Eiserhardt W.L., Couvreur T.L.P., Baker W.J. (2017) Plant phylogeny as a window on the evolution of hyperdiversity in the tropical rainforest biome. New Phytologist 214(4): 1408–1422. https://doi.org/10.1111/nph.14516

Evanno G., Regnaut S., Goudet J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14(8): 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x

Falush D., Stephens M., Pritchard J.K. (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7(4): 574–578. https://doi.org/10.1111/j.1471-8286.2007.01758.x

Funk V., Hollowell T., Berry P., Kelloff C., Alexander S.N. (2007) Checklist of the Plants of the Guiana Shield (Venezuela: Amazonas, Bolivar, Delta Amacuro; Guyana, Surinam, French Guiana) Contributions from the United States National Herbarium, vol. 55. Washington, DC, National Museum of Natural History.

Galbraith D.W., Harkins K.R., Maddox J.M., Ayres N.M., Sharma D.P., Firoozabady E. (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220(4601): 1049–1051. https://doi.org/10.1126/science.220.4601.1049

Gentry A.H. (1982) Neotropical floristic diversity: phytogeographical connections between Central and South America, Pleistocene climatic fluctuations, or an accident of the Andean orogeny? Annals of the Missouri Botanical Garden 69(3): 557–593. https://doi.org/10.2307/2399084

Gonzalez M.A., Baraloto C., Engel J., Mori S.A., Pétronelli P., Riéra B., Chave, J. (2009) Identification of Amazonian trees with DNA barcodes. PloS One 4: e7483. https://doi.org/10.1371/journal.pone.0007483

Goodwin Z.A., Harris D.J., Filer D., Wood J.R.I., Scotland R.W. (2015) Widespread mistaken identity in tropical plant collections. Current Biology 25(22): R1066–R1067. https://doi.org/10.1016/j.cub.2015.10.002

Grivet D., Climent J., Zabal-Aguirre M., Neale D.B., Vendramin G.G., González-Martínez S.C. (2013) Adaptive evolution of Mediterranean pines. Molecular Phylogenetics and Evolution 68(3): 555–566. https://doi.org/10.1016/j.ympev.2013.03.032

Guichoux E., Garnier-Géré P., Lagache L., Lang T., Boury C., Petit R.J. (2013) Outlier loci highlight the direction of introgression in oaks. Molecular Ecology 22(2): 450–462. https://doi.org/10.1111/mec.12125

Hardy O.J. (2016) Population genetics of autopolyploids under a mixed mating model and the estimation of selfing rate. Molecular Ecology Resources 16(1): 103–117. https://doi.org/10.1111/1755-0998.12431

Hardy O.J., Vekemans X. (2002) Spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2(4): 618–620. https://doi.org/10.1046/j.1471-8286.2002.00305.x

Hardy O.J., Dainou K., Donkpegan A., Duminil J., Ewedje E.-E., Ikabanga D.U. (2017) Are we underestimating the number of plant species in the tropics? New insights from population genetics approaches applied on African forest trees. In: Scientific abstracts from the 7th International Barcode of Life Conference. Genome 60: 942.

Hartl D. (2000) A primer of population genetics. 3rd Ed. Sunderland, Sinauer Associates, Inc.

Hoban S., Arntzen J.A., Bruford M.W., Godoy J.A., Rus Hoelzel A., Segelbacher G., Vilà C., Bertorelle G. (2014) Comparative evaluation of potential indicators and temporal sampling protocols for monitoring genetic erosion. Evolutionary Applications 7(9): 984–998. https://doi.org/10.1111/eva.12197

Hoffmann A.A., Sgrò C.M., Kristensen T.N. (2017) Revisiting adaptive potential, population size, and conservation. Trends in Ecology & Evolution 32(7): 506–517. https://doi.org/10.1016/j.tree.2017.03.012

Huang X., Madan A. (1999) CAP3: A DNA sequence assembly program. Genome Research 9: 868–877. https://doi.org/10.1101/gr.9.9.868

Huang Y.-Y., Mori S.A., Kelly L.M. (2015) Toward a phylogenetic-based generic classification of Neotropical Lecythidaceae - I. Status of Bertholletia, Corythophora, Eschweilera and Lecythis. Phytotaxa 203: 85–121. https://doi.org/10.11646/phytotaxa.203.2.1

Jombart T. (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24(11): 1403–1405. https://doi.org/10.1093/bioinformatics/btn129

Joshi N.A., Fass J.N. (2011) Sickle: a sliding-window, adaptive, quality-based trimming tool for FastQ files (Version 1.33) [Software]. Available at https://github.com/najoshi/sickle [accessed 27 Jan. 2020].

Kalinowski S.T. (2011) The computer program STRUCTURE does not reliably identify the main genetic clusters within species: simulations and implications for human population structure. Heredity 106: 625–632. https://doi.org/10.1038/hdy.2010.95

Knowles L.L., Carstens B.C. (2007) Delimiting species without monophyletic gene trees. Systematic Biology 56(6): 887–895. https://doi.org/10.1080/10635150701701091

Kopelman N.M., Mayzel J., Jakobsson M., Rosenberg N.A., Mayrose I. (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources 15(5): 1179–1191. https://doi.org/10.1111/1755-0998.12387

Kowal R.R. (1989) Chromosome numbers of Asteranthos and the putatively related Lecythidaceae. Brittonia 41: 131–135. https://doi.org/10.2307/2807517

Kowal R.R., Mori S.A., Kallunki J.A. (1977) Chromosome numbers of Panamanian Lecythidaceae and their use in subfamilial classification. Brittonia 29: 399–. https://doi.org/10.2307/2806482

Levis C., Costa F.R.C., Bongers F., Peña-Claros M., Clement C.R., Junqueira A.B., Neves E.G., et al. (2017) Persistent effects of pre-Columbian plant domestication on Amazonian forest composition. Science 355(6328): 925–931. https://doi.org/10.1126/science.aal0157

Loiselle B.A., Sork V.L., Nason J., Graham C. (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). American Journal of Botany 82(11): 1420. https://doi.org/10.2307/2445869

Lopes M.A. (2007) Population structure of Eschweilera coriacea (DC.) S. A. Mori in forest fragments in eastern Brazilian Amazonia. Revista Brasileira de Botânica 30(3): 509–519. https://doi.org/10.1590/S0100-84042007000300015

Loureiro J., Rodriguez E., Doležel J., Santos C. (2007) Two new nuclear isolation buffers for plant DNA flow cytometry: a test with 37 species. Annals of Botany 100(4): 875–888. https://doi.org/10.1093/aob/mcm152

Luo A., Ling C., Ho S.Y.W., Zhu C.-D. (2018) Comparison of methods for molecular species delimitation across a range of speciation scenarios. Systematic Biology 67(5): 830–846. https://doi.org/10.1093/sysbio/syy011

Macía M.J., Svenning J.-C. (2005) Oligarchic dominance in western Amazonian plant communities. Journal of Tropical Ecology 21(6): 613–626. https://doi.org/10.1017/S0266467405002579

Maddison W.P. (1997) Gene trees in species trees. Systematic Biology 46(3): 523–536. https://doi.org/10.1093/sysbio/46.3.523

Mallet J., Besansky N., Hahn M.W. (2016) How reticulated are species? BioEssays 38(2): 140–149. https://doi.org/10.1002/bies.201500149

Martin M. (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal 17(1): 10–12. https://doi.org/10.14806/ej.17.1.200

McMichael C.H., Feeley K.J., Dick C.W., Piperno D.R., Bush M.B. (2017) Comment on “Persistent effects of pre-Columbian plant domestication on Amazonian forest composition.” Science 358(6361): eaan8347. https://doi.org/10.1126/science.aan8347

Medrano M., López-Perea E., Herrera C.M. (2015) Population genetics methods applied to a species delimitation problem: endemic trumpet daffodils (Narcissus section Pseudonarcissi) from the Southern Iberian Peninsula. International Journal of Plant Sciences 175(5): 501–517. https://doi.org/10.1086/675977

Meglécz E., Costedoat C., Dubut V., Gilles A., Malausa T., Pech N., Martin J.-F. (2010) QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics 26 (3): 403–404. https://doi.org/10.1093/bioinformatics/btp670

Mirarab S., Reaz R., Bayzid M.S., Zimmermann T., Swenson M.S., Warnow T. (2014) ASTRAL: genome-scale coalescent-based species tree estimation. Bioinformatics 30(17): i541–i548. https://doi.org/10.1093/bioinformatics/btu462

Mori S.A. (1987) The Lecythidaceae of a lowland Neotropical forest: La Fumée Mountain, French Guiana. Memoirs of the New York Botanical Garden, vol. 44. New York, New York Botanical Garden Press.

Mori S.A., Lepsch-Cunha N. (1995) The Lecythidaceae of a Central Amazonian moist forest. Memoirs of the New York Botanical Garden, vol. 75. New York, New York Botanical Garden Press.

Mori S.A., Prance G.T. (1990) Lecythidaceae, Part 2. The zygomorphic-flowered New World genera (Couroupita, Corythophora, Bertholletia, Couratari, Eschweilera, & Lecythis), with a study of secondary xylem of Neotropical Lecythidaceae by Carl H. de Zeeuw. Flora Neotropica, Monograph 21 (II). New York, New York Botanical Garden Press. https://www.jstor.org/stable/4393724

Mori S.A., Becker P., Kincaid D. (2001) Lecythidaceae of a Central Amazonian lowland forest. In Bierregaard R.O. Jr, Gascon C., Lovejoy T., Mesquita R. (eds.) Lessons from Amazonia: The ecology and conservation of a fragmented forest: 54–67. New Haven and London, Yale University Press.

Mori S.A., Tsou C.-H., Wu C.-C., Cronholm B., Anderberg A.A. (2007) Evolution of Lecythidaceae with an emphasis on the circumscription of Neotropical genera: information from combined ndhF and trnL-F sequence data. Annals of Botany 94(3): 289–301. https://doi.org/10.3732/ajb.94.3.289

Mori S.A., Kiernan E.A., Smith N.P., Kelley L.M., Huang Y-Y., Prance G.T., Thiers B. (2017) Observations on the phytogeography of the Lecythidaceae (Brazil nut family). Phytoneuron 30: 1–85.

Nordborg M. (2001) Coalescent theory. In Balding D.J., Bishop M.J., Cannings C. (eds.) Handbook of Statistical Genetics: 179-212. Chichester, John Wiley & Sons.

Orozco-terWengel P., Corander J., Schlötterer C. (2011) Genealogical lineage sorting leads to significant, but incorrect Bayesian multilocus inference of population structure. Molecular Ecology 20(6): 1108–1121. https://doi.org/10.1111/j.1365-294X.2010.04990.x

Parisod C., Holderegger R., Brochmann C. (2010) Evolutionary consequences of autopolyploidy. New Phytologist 186(1): 5–17. https://doi.org/10.1111/j.1469-8137.2009.03142.x

Pennington R.T., Lavin M. (2016) The contrasting nature of woody plant species in different neotropical forest biomes reflects differences in ecological stability. New Phytologist 210(1): 25–37. https://doi.org/10.1111/nph.13724

Peters C.M., Balick M.J., Kahn F., Anderson A.B. (1989) Oligarchic forests of economic plants in Amazonia: Utilization and conservation of an important tropical resource. Conservation Biology 3(4): 341–349. https://www.jstor.org/stable/2386215

Pitman N.C.A., Terborgh J.W., Silman M.R., Percy Núñez V., Neill D.A., Cerón C.E., Palacios W.A., Aulestia M. (2001) Dominance and distribution of tree species in Upper Amazonian terra firme forests. Ecology 82(8): 2101–2117. https://doi.org/10.1890/0012-9658(2001)082[2101:DADOTS]2.0.CO;2

Pitman N.C.A., Silman M.R., Terborgh J.W. (2013) Oligarchies in Amazonian tree communities: a ten-year review. Ecography 36(2): 114–123. https://doi.org/10.1111/j.1600-0587.2012.00083.x

Prance G.T., Mori S.A. (1979) Lecythidaceae–Part 1. The actinomorphic-flowered New World Lecythidaceae (Asteranthos, Gustavia, Grias, Allantoma, & Cariniana). Flora Neotropica, Monograph 21(I). New York, New York Botanical Garden Press. http://www.jstor.org/stable/4393721

Pritchard J.K., Stephens M., Donnelly P. (2000) Inference of population structure using multilocus genotype data. Genetics 155(2): 945–959.

R Development Core Team (2008) R: a language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. Available at https://www.r-project.org/ [accessed 27 Jan. 2020].

Rosenberg N.A., Nordborg M. (2002) Genealogical trees, coalescent theory and the analysis of genetic polymorphisms. Nature Reviews Genetics 3: 380–390. https://doi.org/10.1038/nrg795

Rosenberg N.A., Mahajan S., Ramachandran S., Zhao C., Pritchard J.K., Feldman M.W. (2005) Clines, clusters, and the effect of study design on the inference of human population structure. PLoS Genetics 1: e70. https://doi.org/10.1371/journal.pgen.0010070

Rousset F. (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145(4): 1219–1228.

Rozen S., Skaletsky H. (2000) Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology 132: 365–386. https://doi.org/10.1385/1-59259-192-2:365

Santos A.S., Borges D.B., Vivas C.V., Berg C.V.D., Rodrigues P.S., Tarazi R., Gaiotto F.A. (2019) Gene pool sharing and genetic bottleneck effects in subpopulations of Eschweilera ovata (Cambess.) Mart. ex Miers (Lecythidaceae) in the Atlantic Forest of southern Bahia, Brazil. Genetics and Molecular Biology 42(3): 655–665. https://doi.org/10.1590/1678-4685-gmb-2018-0140

Shi T., Huang H., Barker M.S. (2010) Ancient genome duplications during the evolution of kiwifruit (Actinidia) and related Ericales. Annals of Botany 106(3): 497–504. https://doi.org/10.1093/aob/mcq129

Storey J.D. (2003) The positive false discovery rate: a Bayesian interpretation and the q-value. The Annals of Statistics 31(6): 2013–2035. https://doi.org/10.1214/aos/1074290335

Techen N., Arias R.S., Glynn N.C., Pan Z., Khan I.A., Scheffler B.E. (2010) Optimized construction of microsatellite-enriched libraries. Molecular Ecology Resources 10(3): 508–515. https://doi.org/10.1111/j.1755-0998.2009.02802.x

ter Steege H., Pitman N.C.A., Phillips O.L., Chave J., Sabatier D., Duque A., et al. (2006) Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443: 444–447. https://doi.org/10.1038/nature05134

ter Steege H., Pitman N.C.A., Sabatier D., Baraloto C., Salomão R.P., Guevara J.E., et al. (2013) Hyperdominance in the Amazonian tree flora. Science 342(6156): 1243092. https://doi.org/10.1126/science.1243092

Torroba-Balmori P., Budde K.B., Heer K., González-Martínez S.C., Olsson S., Scotti-Saintagne C., Casalis M., Sonké B., Dick C.W., Heuertz M. (2017) Altitudinal gradients, biogeographic history and microhabitat adaptation affect fine-scale spatial genetic structure in African and Neotropical populations of an ancient tropical tree species. PloS One 12: e0182515. https://doi.org/10.1371/journal.pone.0182515

Turchetto-Zolet A.C., Pinheiro F., Salgueiro F., Palma-Silva C. (2013) Phylogeographical patterns shed light on evolutionary process in South America. Molecular Ecology 22(5): 1193–1213. https://doi.org/10.1111/mec.12164

Vekemans X., Hardy O.J. (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Molecular Ecology 13(4): 921–935. https://doi.org/10.1046/j.1365-294X.2004.02076.x

Weir B.S., Cockerham C.C. (1984) Estimating F-statistics for the analysis of population structure Evolution 38(6): 1358–1370. https://doi.org/10.1111/j.1558-5646.1984.tb05657.x

Willyard A., Cronn R., Liston A. (2009) Reticulate evolution and incomplete lineage sorting among the ponderosa pines. Molecular Phylogenetics and Evolution 52(2): 498–511. https://doi.org/10.1016/j.ympev.2009.02.011

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.