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Phylogeography of Brazilian pine (Araucaria angustifolia): integrative evidence for pre-Columbian anthropogenic dispersal

  • Miguel Busarello LauterjungEmail author
  • Alison Paulo Bernardi
  • Tiago Montagna
  • Rafael Candido-Ribeiro
  • Newton Clóvis Freitas da Costa
  • Adelar Mantovani
  • Maurício Sedrez dos Reis
Original Article
Part of the following topical collections:
  1. Taxonomy

Abstract

Phylogeographic studies allow us to better understand the past history of species and the factors that mold their current distribution. Here, we demonstrate the potential human impact on the distribution of a tree species. In particular, it was hypothesized that Araucaria angustifolia, an endangered South American conifer, was dispersed from its Pleistocene glacial refugium to its maximum occurrence distribution (MOD), mainly by pre-Columbian human groups (ca 2000 years ago). In order to test this hypothesis, we sampled 20 A. angustifolia populations in southern Brazil. Our analysis consisted of an integrative phylogeographic approach, supported by ecological aspects of the species. Therefore, we constructed the species chloroplast haplotype network, tested for possible neutrality deviations, genetic divergence, association between genetic and geographic distances, and simulated the amount of time that the species required to reach its MOD without human help. The species showed clear signs of rapid and recent expansion from a single refugium. The haplotype network had a star-like shape. Populations and the species showed negative values for the neutrality tests and low divergence values among populations (FST = 0.041) not associated with geographic distance. The estimated dispersal time required for the species to reach its MOD from its putative refugium without human help is not consistent with the rapid and recent expansion of the species. Hence, we argue that humans played an important role in expanding the distribution of the currently endangered species, and it needs to be accounted for when analyzing landscape genetics or in the development of conservation strategies.

Keywords

Chloroplast DNA Cultural landscape Plant phylogeography Pre-Columbian indigenous people Taquara/Itararé culture 

Notes

Acknowledgements

This work was supported by the National Council of Technological and Scientific Development (CNPq), process no. FAPESC/2780/2012-4 (PRONEX), 309128/2014-5 to M.S.R. and 130894/2015-0 to R.C.R., and the Coordination for the Improvement of Higher Education Personnel (CAPES) for the Master’s scholarship to M.B.L. and doctoral scholarships to A.P.B., T.M., and N.C.F.C. We would like to thank Santa Catarina State University (UDESC), Federal University of Santa Catarina (UFSC), and Conservation and Use of Natural Resources (UCRN) and Physiology of Development and Plant Genetics Laboratory (LFDGV) research groups for logistical support, the Chico Mendes Biodiversity Institute (ICMBio), the Conservation Unities Division (DUC), and landowners that authorized and facilitated the sample collection. Additionally, we thank the anonymous reviewers for their effort in providing comments and suggestions, which substantially improved the manuscript.

Author’s contributions

This research represents part of a Master’ thesis of M.B.L. M.S.R., A.M. and M.B.L. designed the research; M.B.L., A.P.B., R.C.R., T.M. and N.C.F.C. collected the samples and performed the laboratory procedures; M.B.L. performed the analysis and wrote the draft of the manuscript; all authors reviewed and contributed to the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11295_2018_1250_MOESM1_ESM.docx (271 kb)
Supplementary File S1 Supporting ecological evidence (DOCX 271 kb)
11295_2018_1250_MOESM2_ESM.docx (218 kb)
Supplementary File S2 Human occupation records inside the Araucaria Forest domain in the past. (DOCX 218 kb)
11295_2018_1250_MOESM3_ESM.docx (26 kb)
Supplementary File S3 Coordinates of the 20 Araucaria angustifolia studied populations in southern Brazil. (DOCX 26 kb)
11295_2018_1250_MOESM4_ESM.docx (35 kb)
Supplementary File S4 Pairwise FST values (under diagonal) from 20 Araucaria angustifolia populations and their respective p-values (above diagonal). Negative values should be interpreted as zero. (DOCX 35 kb)

References

  1. Adan N, Atchison J, Reis MS, Peroni N (2016) Local knowledge, use and management of ethnovarieties of Araucaria angustifolia (Bert.) Ktze. In the plateau of Santa Catarina, Brazil. Econ Bot 70:353–364.  https://doi.org/10.1007/s12231-016-9361-z CrossRefGoogle Scholar
  2. Auler NMF, Reis MS, Guerra MP, Nodari RO (2002) The genetics and conservation of Araucaria angustifolia: I. Genetic structure and diversity of natural populations by means of non-adaptive variation in the state of Santa Catarina, Brazil. Genet Mol Biol 25:329–338CrossRefGoogle Scholar
  3. Avise JC (2009) Phylogeography: retrospect and prospect. J Biogeogr 36:3–15.  https://doi.org/10.1111/j.1365-2699.2008.02032.x CrossRefGoogle Scholar
  4. Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522.  https://doi.org/10.1146/annurev.es.18.110187.002421 CrossRefGoogle Scholar
  5. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48.  https://doi.org/10.1093/oxfordjournals.molbev.a026036 CrossRefPubMedGoogle Scholar
  6. Barros MJF, Silva-Arias GA, Fregonezi JN, Turchetto-Zolet AC, Iganci JRV, Diniz-Filho JAF, Freitas LB (2015) Environmental drivers of diversity in subtropical highland grasslands. Perspect Plant Ecol Evol Syst 17:360–368.  https://doi.org/10.1016/j.ppees.2015.08.001 CrossRefGoogle Scholar
  7. Behling H (1995) Investigations into the late Pleistocene and Holocene history of vegetation and climate in Santa Catarina (South Brazil). Veg Hist Archaeobot 4:127–152.  https://doi.org/10.1007/BF00203932 CrossRefGoogle Scholar
  8. Behling H (1997) Late quaternary vegetation, climate and fire history of the Araucaria forest and Campos region from Serra Campos Gerais, Paraná state (South Brazil). Rev Palaeobot Palynol 97:109–121CrossRefGoogle Scholar
  9. Behling H, Bauermann SG, Neves PCP (2001) Holocene environmental changes in the São Francisco de Paula region, southern Brazil. J S Am Earth Sci 14:631–639.  https://doi.org/10.1016/S0895-9811(01)00040-2 CrossRefGoogle Scholar
  10. Behling H, Pillar VD, Orlóci L, Bauermann SG (2004) Late quaternary Araucaria forest, grassland (Campos), fire and climate dynamics, studied by high-resolution pollen, charcoal and multivariate analysis of the Cambará do Sul core in southern Brazil. Palaeogeogr Palaeoclimatol Palaeoecol 203:277–297.  https://doi.org/10.1016/S0031-0182(03)00687-4 CrossRefGoogle Scholar
  11. Bitencourt LAV, Krauspenhar PM (2006) Possible prehistoric anthropogenic effect on Araucaria angustifolia (Bert.) O. Kuntze expansion during the late holocene. Rev Bras Paleontol 9:109–116.  https://doi.org/10.4072/rbp.2006.1.12 CrossRefGoogle Scholar
  12. Bittencourt JVM, Sebbenn AM (2007) Patterns of pollen and seed dispersal in a small, fragmented population of the wind-pollinated tree Araucaria angustifolia in southern Brazil. Heredity (Edinb) 99:580–591.  https://doi.org/10.1038/sj.hdy.6801019 CrossRefGoogle Scholar
  13. Bittencourt JVM, Sebbenn AM (2008) Pollen movement within a continuous forest of wind-pollinated Araucaria angustifolia, inferred from paternity and TwoGener analysis. Conserv Genet 9:855–868.  https://doi.org/10.1007/s10592-007-9411-2 CrossRefGoogle Scholar
  14. Cinget B, Gérardi S, Beaulieu J, Bousquet J (2015) Less pollen-mediated gene flow for more signatures of glacial lineages: congruent evidence from balsam fir cpDNA and mtDNA for multiple refugia in eastern and Central North America. PLoS One 10:1–25.  https://doi.org/10.1371/journal.pone.0122815 CrossRefGoogle Scholar
  15. Clement CR (1999) 1492 and the loss of amazonian crop genetic resources. I. The relation between domestication and human population decline. Econ Bot 53:188–202.  https://doi.org/10.1007/bf02866498 CrossRefGoogle Scholar
  16. Corander J, Sirén J, Arjas E (2008) Bayesian spatial modeling of genetic population structure. Comput Stat 23:111–129.  https://doi.org/10.1007/s00180-007-0072-x CrossRefGoogle Scholar
  17. Cun Y-Z, Wang X-Q (2015) Phylogeography and evolution of three closely related species of Tsuga (hemlock) from subtropical eastern Asia: further insights into speciation of conifers. J Biogeogr 42:315–327.  https://doi.org/10.1111/jbi.12421 CrossRefGoogle Scholar
  18. de Filippo C, Bostoen K, Stoneking M, Pakendorf B (2012) Bringing together linguistic and genetic evidence to test the bantu expansion. Proc R Soc B Biol Sci 279:3256–3263.  https://doi.org/10.1098/rspb.2012.0318 CrossRefGoogle Scholar
  19. de Souza MIF, Salgueiro F, Carnavale-Bottino M et al (2009) Patterns of genetic diversity in southern and southeastern Araucaria angustifolia (Bert.) O. Kuntze relict populations. Genet Mol Biol 32:546–556.  https://doi.org/10.1590/S1415-47572009005000052 CrossRefPubMedCentralPubMedGoogle Scholar
  20. Demesure B, Sodzi N, Petit RJ (1995) A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 4:129–134.  https://doi.org/10.1111/j.1365-294X.1995.tb00201.x CrossRefPubMedGoogle Scholar
  21. Denevan WM (1992) The pristine myth: the landscape of the Americas in 1492. Ann Assoc Am Geogr 82:369–385.  https://doi.org/10.1111/j.1467-8306.1992.tb01965.x CrossRefGoogle Scholar
  22. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus (Madison) 12:13–15Google Scholar
  23. Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20.  https://doi.org/10.18637/jss.v022.i04 CrossRefGoogle Scholar
  24. Duarte LDS, Dos-Santos MMG, Hartz SM, Pillar VD (2006) Role of nurse plants in Araucaria Forest expansion over grassland in South Brazil. Austral Ecol 31:520–528.  https://doi.org/10.1111/j.1442-9993.2006.01602.x CrossRefGoogle Scholar
  25. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and windows. Mol Ecol Resour 10:564–567.  https://doi.org/10.1111/j.1755-0998.2010.02847.x CrossRefPubMedGoogle Scholar
  26. 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.  https://doi.org/10.1007/s00424-009-0730-7 PubMedCentralCrossRefPubMedGoogle Scholar
  27. Ferreira DK, Nazareno AG, Mantovani A, Bittencourt R, Sebbenn AM, Reis MS (2012) Genetic analysis of 50-year old Brazilian pine (Araucaria angustifolia) plantations: implications for conservation planning. Conserv Genet 13:435–442.  https://doi.org/10.1007/s10592-011-0296-8 CrossRefGoogle Scholar
  28. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedCentralPubMedGoogle Scholar
  29. Gamache I, Jaramillo-Correa JP, Payette S, Bousquet J (2003) Diverging patterns of mitochondrial and nuclear DNA diversity in subarctic black spruce: imprint of a founder effect associated with postglacial colonization. Mol Ecol 12:891–901.  https://doi.org/10.1046/j.1365-294X.2003.01800.x CrossRefPubMedGoogle Scholar
  30. Gérardi S, Jaramillo-Correa JP, Beaulieu J, Bousquet J (2010) From glacial refugia to modern populations: new assemblages of organelle genomes generated by differential cytoplasmic gene flow in transcontinental black spruce. Mol Ecol 19:5265–5280.  https://doi.org/10.1111/j.1365-294X.2010.04881.x CrossRefPubMedGoogle Scholar
  31. Glaser B, Birk JJ (2012) State of the scientific knowledge on properties and genesis of anthropogenic dark earths in Central Amazonia (terra preta de Índio). Geochim Cosmochim Acta 82:39–51.  https://doi.org/10.1016/j.gca.2010.11.029 CrossRefGoogle Scholar
  32. Gribel R, Lemes MR, Bernardes LG, Pinto AE, Shepard GH (2007) Phylogeography of Brazil-nut tree (Bertholletia excelsa, Lecythidaceae): evidence of human influence on the species distribution. Association for Tropical Biology and Conservation Annual Meeting: Linking Tropical Biology with Human Dimensions 15–19 July 2007 Morelia, Mexico, p 281Google Scholar
  33. Guerra MP, Silveira V, Reis MS, Schneider L (2002) Exploração, manejo e conservação da araucária (Araucaria angustifolia). In: Lino CF, Simões LL (eds) Sustentável Mata Atlântica: A exploração de seus recursos florestais. Senac, São Paulo, pp 85–102Google Scholar
  34. Gugerli F, Sperisen C, Büchler U et al (2001) Haplotype variation in a mitochondrial tandem repeat of Norway spruce (Picea abies) populations suggests a serious founder effect during postglacial re-colonization of the western alps. Mol Ecol 10:1255–1263.  https://doi.org/10.1046/j.1365-294X.2001.01279.x CrossRefPubMedGoogle Scholar
  35. Hartl DL, Clark AG (2007) Principles of population genetics, 4th edn. Sinauer associates, SunderlandGoogle Scholar
  36. Höhn M, Gugerli F, Abran P, Bisztray G, Buonamici A, Cseke K, Hufnagel L, Quintela-Sabarís C, Sebastiani F, Vendramin GG (2009) Variation in the chloroplast DNA of Swiss stone pine (Pinus cembra L.) reflects contrasting post-glacial history of populations from the Carpathians and the alps. J Biogeogr 36:1798–1806.  https://doi.org/10.1111/j.1365-2699.2009.02122.x CrossRefGoogle Scholar
  37. Hueck K (1952) Verbreitung und Standortsansprüche der brasilianischen Araukarie (Araucaria angustiolia). Forstwissenschaftliches Cent 71:272–289CrossRefGoogle Scholar
  38. Hueck K (1953) Distribuição e habitat natural do Pinheiro do Paraná (Araucaria angustifolia). Bol da Fac Filos Ciências e Let Univ São Paulo 10:5–24CrossRefGoogle Scholar
  39. Iob G, Vieira EM (2008) Seed predation of Araucaria angustifolia (Araucariaceae) in the Brazilian Araucaria Forest: influence of deposition site and comparative role of small and “large” mammals. Plant Ecol 198:185–196.  https://doi.org/10.1007/s11258-007-9394-6 CrossRefGoogle Scholar
  40. Iriarte J, Behling H (2007) The expansion of Araucaria forest in the southern Brazilian highlands during the last 4000 years and its implications for the development of the Taquara/Itararé tradition. Environ Archaeol 12:115–127.  https://doi.org/10.1179/174963107x226390 CrossRefGoogle Scholar
  41. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, III. Academic Press, New York, pp 21–132Google Scholar
  42. Kaur D, Bhatnagar SP (1985) Fertilization and formation of neocytoplasm in Agathis robusta. Phytomorphology 34:56–60Google Scholar
  43. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefPubMedGoogle Scholar
  44. Ladio AH (2001) The maintenance of wild edible plant gathering in a Mapuche community of Patagonia. Econ Bot 55:243–254.  https://doi.org/10.1007/BF02864562 CrossRefGoogle Scholar
  45. Levis C, Costa FRC, Bongers F et al (2017) Persistent effects of pre-Columbian plant domestication on Amazonian forest composition. Science (80- ) 355:925–931.  https://doi.org/10.1126/science.aal0157 CrossRefGoogle Scholar
  46. Levis C, Flores BM, Moreira PA, Luize BG, Alves RP, Franco-Moraes J, Lins J, Konings E, Peña-Claros M, Bongers F, Costa FRC, Clement CR (2018) How people domesticated Amazonian forests. Front Ecol Evol 5:e111.  https://doi.org/10.3389/fevo.2017.00171 CrossRefGoogle Scholar
  47. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452.  https://doi.org/10.1093/bioinformatics/btp187 CrossRefPubMedGoogle Scholar
  48. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  49. Mantovani A, Morellato LPC, Reis MS (2006) Internal genetic structure and outcrossing rate in a natural population of Araucaria angustifolia (Bert.) O. Kuntze. J Hered 97:466–472.  https://doi.org/10.1093/jhered/esl031 CrossRefPubMedGoogle Scholar
  50. Marchelli P, Baier C, Mengel C, Ziegenhagen B, Gallo LA (2010) Biogeographic history of the threatened species Araucaria araucana (Molina) K. Koch and implications for conservation: a case study with organelle DNA markers. Conserv Genet 11:951–963.  https://doi.org/10.1007/s10592-009-9938-5 CrossRefGoogle Scholar
  51. Medina-Macedo L, Sebbenn AM, Lacerda AEB, Ribeiro JZ, Soccol CR, Bittencourt JVM (2015) High levels of genetic diversity through pollen flow of the coniferous Araucaria angustifolia: a landscape level study in southern Brazil. Tree Genet Genomes 11:1–14.  https://doi.org/10.1007/s11295-014-0814-1 CrossRefGoogle Scholar
  52. Meng L, Chen G, Li Z, Yang Y, Wang Z, Wang L (2015) Refugial isolation and range expansions drive the genetic structure of Oxyria sinensis (Polygonaceae) in the Himalaya-Hengduan Mountains. Sci Rep 5:10396.  https://doi.org/10.1038/srep10396 CrossRefPubMedCentralPubMedGoogle Scholar
  53. Mogensen HL (1996) The hows and whys of cytoplasmic inheritance in seed plants. Am J Bot 83:383.  https://doi.org/10.2307/2446172 CrossRefGoogle Scholar
  54. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  55. Noelli FS (2000) A ocupação humana na região Sul do Brasil: arqueologia, debates e perspectivas 1872-2000. Rev USP 0(44):218–269CrossRefGoogle Scholar
  56. Ornelas JF, Ruiz-Sánchez E, Sosa V (2010) Phylogeography of Podocarpus matudae (Podocarpaceae): pre-quaternary relicts in northern Mesoamerican cloud forests. J Biogeogr 37:2384–2396.  https://doi.org/10.1111/j.1365-2699.2010.02372.x CrossRefGoogle Scholar
  57. Owens JN, Catalano GL, Morris SJ, Aitken-Christie J (1995) The reproductive riology of kauri (Agathis australis). II. Male gametes, fertilization, and cytoplasmic inheritance. Int J Plant Sci 156:404–416.  https://doi.org/10.1086/297262 CrossRefGoogle Scholar
  58. Paise G, Vieira EM (2005) Produção de frutos e distribuição espacial de angiospermas com frutos zoocóricos em uma Floresta Ombrófila Mista no Rio Grande do Sul, Brasil. Brazilian J Bot 28:615–625CrossRefGoogle Scholar
  59. Paludo GF, Duarte RI, Bernardi AP, Mantovani A, Reis MS (2016a) The size of Araucaria angustifolia (Bertol.) Kuntze entering into reproductive stages as a basis for seed management projects. Rev Árvore 40:695–705.  https://doi.org/10.1590/0100-67622016000400013 CrossRefGoogle Scholar
  60. Paludo GF, Lauterjung MB, Reis MS, Mantovani A (2016b) Inferring population trends of Araucaria angustifolia (Araucariaceae) using a transition matrix model in an old-growth forest. South For J For Sci 78:137–143.  https://doi.org/10.2989/20702620.2015.1136506 CrossRefGoogle Scholar
  61. Patreze CM, Tsai SM (2010) Intrapopulational genetic diversity of Araucaria angustifolia (Bertol.) Kuntze is different when assessed on the basis of chloroplast or nuclear markers. Plant Syst Evol 284:111–122.  https://doi.org/10.1007/s00606-009-0238-9 CrossRefGoogle Scholar
  62. Peakall R, Ebert D, Scott LJ, Meagher PF, Offord CA (2003) Comparative genetic study confirms exceptionally low genetic variation in the ancient and endangered relictual conifer, Wollemia nobilis (Araucariaceae). Mol Ecol 12:2331–2343.  https://doi.org/10.1046/j.1365-294X.2003.01926.x CrossRefPubMedGoogle Scholar
  63. Peres CA, Baider C (1997) Seed dispersal, spatial distribution and population structure of Brazilnut trees ( Bertholletia excelsa) in southeastern Amazonia. J Trop Ecol 13:595–616.  https://doi.org/10.1017/S0266467400010749 CrossRefGoogle Scholar
  64. Quiroga MP, Pacheco S, Malizia LR, Premoli AC (2012) Shrinking forests under warming: evidence of Podocarpus parlatorei (pino del cerro) from the subtropical Andes. J Hered 103:682–691.  https://doi.org/10.1093/jhered/ess031 CrossRefPubMedGoogle Scholar
  65. R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
  66. Reis MS, Ladio A, Peroni N (2014) Landscapes with Araucaria in South America: evidence for a cultural dimension. Ecol Soc 19:43.  https://doi.org/10.5751/ES-06163-190243 CrossRefGoogle Scholar
  67. Reitz R, Klein RM (1966) Araucariáceas. In: Reitz R (ed) Flora Ilustrada Catarinense. Herbário Barbosa Rodrigues, Itajaí, p 62Google Scholar
  68. Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153.  https://doi.org/10.1016/j.biocon.2009.02.021 CrossRefGoogle Scholar
  69. Rossetto M, Ens EJ, Honings T, Wilson PD, Yap JYS, Costello O, Round ER, Bowern C (2017) From songlines to genomes: prehistoric assisted migration of a rain forest tree by Australian aboriginal people. PLoS One 12:e0186663.  https://doi.org/10.1371/journal.pone.0186663 CrossRefPubMedCentralPubMedGoogle Scholar
  70. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedCentralPubMedGoogle Scholar
  71. Rull V, Montoya E (2014) Mauritia flexuosa palm swamp communities: natural or human-made? A palynological study of the gran Sabana region (northern South America) within a neotropical context. Quat Sci Rev 99:17–33.  https://doi.org/10.1016/j.quascirev.2014.06.007 CrossRefGoogle Scholar
  72. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74:5463–5467CrossRefPubMedCentralPubMedGoogle Scholar
  73. Schlögl PS, de Souza AP, Nodari RO (2007) PCR-RFLP analysis of non-coding regions of cpDNA in Araucaria angustifolia (Bert.) O. Kuntze. Genet Mol Biol 30:423–427.  https://doi.org/10.1590/S1415-47572007000300020 CrossRefGoogle Scholar
  74. Scott LJ, Shepherd MJ, Nikles DG, Henry RJ (2005) Low efficiency of pseudotestcross mapping design was consistent with limited genetic diversity and low heterozygosity in hoop pine (Araucaria cunninghamii, Araucariaceae). Tree Genet Genomes 1:124–134.  https://doi.org/10.1007/s11295-005-0022-0 CrossRefGoogle Scholar
  75. Shepard GH, Ramirez H (2011) “Made in Brazil”: human dispersal of the Brazil nut (Bertholletia excelsa, Lecythidaceae) in ancient Amazonia. Econ Bot 65:44–65.  https://doi.org/10.1007/s12231-011-9151-6 CrossRefGoogle Scholar
  76. Sinclair WT, Morman JD, Ennos RA (1999) The postglacial history of scots pine (Pinus sylvestris L.) in western Europe: evidence from mitochondrial DNA variation. Mol Ecol 8:83–88.  https://doi.org/10.1046/j.1365-294X.1999.00527.x CrossRefGoogle Scholar
  77. Sousa VA, Sebbenn AM, Hattemer HH, Ziehe M (2005) Correlated mating in populations of a dioecious Brazilian conifer, Araucaria angustifolia (Bert.) O. Ktze. For Genet 12:107–119Google Scholar
  78. Souza AF, Forgiarini C, Longhi SJ, Brena DA (2008) Regeneration patterns of a long-lived dominant conifer and the effects of logging in southern South America. Acta Oecol 34:221–232.  https://doi.org/10.1016/j.actao.2008.05.013 CrossRefGoogle Scholar
  79. Stefenon VM, Gailing O, Finkeldey R (2007) Genetic structure of Araucaria angustifolia (Araucariaceae) populations in Brazil: implications for the in situ conservation of genetic resources. Plant Biol 9:516–525.  https://doi.org/10.1055/s-2007-964974 CrossRefPubMedGoogle Scholar
  80. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedCentralPubMedGoogle Scholar
  81. Thomas P (2013) Araucaria angustifolia. The IUCN Red List of Threatened Species 2013: e.T32975A2829141.  https://doi.org/10.2305/IUCN.UK.2013-1.RLTS.T32975A2829141.en
  82. Thomas E, Alcázar Caicedo C, McMichael CH et al (2015) Uncovering spatial patterns in the natural and human history of Brazil nut (Bertholletia excelsa) across the Amazon Basin. J Biogeogr 42:1367–1382.  https://doi.org/10.1111/jbi.12540 CrossRefGoogle Scholar
  83. Vieira EM, Ribeiro JF, Iob G (2011) Seed predation of Araucaria angustifolia (Araucariaceae) by small rodents in two areas with contrasting seed densities in the Brazilian Araucaria forest. J Nat Hist 45:843–854.  https://doi.org/10.1080/00222933.2010.536265 CrossRefGoogle Scholar
  84. Vieira-da-Silva C, Reis MS (2009) Produção de pinhão na região de Caçador, SC: Aspectos da obtenção e sua importância para comunidades locais. Ciência Florest 19:363–374CrossRefGoogle Scholar
  85. Vieira-da-Silva C, Martins G, Steiner N et al (2011) Araucaria angustifolia. In: Coradin L, Reis A, Siminski A (eds) Espécies nativas da flora brasileira de valor econômico atual ou potencial: plantas para o futuro – Região Sul. Ministério do Meio Ambiente, Brasília, pp 134–150Google Scholar
  86. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution (N Y) 38:1358–1370Google Scholar
  87. Yang Y-X, Wang M-L, Liu Z-L, Zhu J, Yan MY, Li ZH (2016) Nucleotide polymorphism and phylogeographic history of an endangered conifer species Pinus bungeana. Biochem Syst Ecol 64:89–96.  https://doi.org/10.1016/j.bse.2015.11.016 CrossRefGoogle Scholar
  88. Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall, Upper Saddle RiverGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Miguel Busarello Lauterjung
    • 1
    Email author
  • Alison Paulo Bernardi
    • 1
  • Tiago Montagna
    • 1
  • Rafael Candido-Ribeiro
    • 1
  • Newton Clóvis Freitas da Costa
    • 1
  • Adelar Mantovani
    • 2
  • Maurício Sedrez dos Reis
    • 1
  1. 1.Núcleo de Pesquisas em Florestas Tropicais (NPFT)Universidade Federal de Santa CatarinaFlorianópolisBrazil
  2. 2.Uso e Conservação dos Recursos Florestais (UCRF)Universidade do Estado de Santa CatarinaLagesBrazil

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