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Genetic variability of Araucaria angustifolia in the Argentinean Parana Forest and implications for management and conservation

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Genetic variability of Araucaria angustifolia populations in Argentina was moderate-to-low and reduced by logging. Some studied populations and the plantation are valuable gene pools for conservation and management.

Abstract

The main forces shaping genetic variability of woody species in fragmented forest are the geographical distribution and demographic history of populations. We conducted molecular analyses to evaluate how these factors have affected Araucaria angustifolia genetic variability in the Argentinean Parana Forest and to identify valuable gene pools for conservation and management purposes. Using 706 polymorphic AFLP (Amplified Fragment Length Polymorphism) markers, we analyzed nine native populations with different logging history and one plantation (312 individuals) of an uncertain origin. Average genetic diversity for the native populations was moderate-to-low (He = 0.128) in accordance with their marginal location within Araucaria’s range. In general, genetic diversity of populations decreases from east to west with increasing distances from the main area of species distribution on southern Brazil. Logging may have been responsible for further reduction of genetic variability in the more intensely exploited populations of the southern region and in some private fields. The moderate genetic differentiation among populations (ΦPT = 0.080) suggests an increase in the genetic structure of remnant populations because of fragmentation. UPGMA and Bayesian analyses agreed with the geographic location of populations. Populations from the southern Provincial Parks at Araucaria’s range edges grouped and differed genetically more from other populations. The highest genetic diversity of the plantation (He = 0.155) suggests that its individuals could have originated from seeds collected from different and/or highly variable sources of Brazil and the northeast of Argentina.

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References

  • Aguirre NC (2014) Diversidad genética de Pino Paraná (Araucaria angustifolia) en la Selva Paranaense: Análisis genómico mediante marcadores moleculares AFLPs. Thesis for Degree in Genetics, Facultad de Ciencias Exactas, Químicas y Naturales, Universidad de Morón, Buenos Aires, Argentina

  • 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 25:329–338

    Article  CAS  Google Scholar 

  • Behling H, Pillar VDP, 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

    Article  Google Scholar 

  • Bekessy SA, Allnutt TR, Premoli AC, Lara A, Ennos RA, Burgman MA, Cortes M, Newton AC (2002) Genetic variation in the vulnerable and endemic Monkey Puzzle tree, detected using RAPDs. Heredity 88:243–224

    Article  PubMed  CAS  Google Scholar 

  • Bertolini MP (2000) Documento Base para la Discusión del Plan de Manejo del Parque Provincial de la Araucaria. Ministerio de Ecología y Recursos Naturales Renovables de la Provincia de Misiones. Administración de Parques Nacionales—Delegación Regional Nordeste Argentino

  • Bittencourt JVM (2007) Proposta para conservação genética da Araucaria angustifolia. Pesq Flor Bras Colombo 55:87–93

    Google Scholar 

  • 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 99:580–591

    Article  PubMed  CAS  Google Scholar 

  • Bittencourt JVM, Sebbenn AM (2009) Genetic effects of forest fragmentation in high-density Araucaria angustifolia populations in Southern Brazil. Tree Genet Genomes 5:573–582

    Article  Google Scholar 

  • Bonin A, Ehrich D, Manel S (2007) Statistical analysis of amplified fragment length polymorphism data: a toolbox for molecular ecologists and evolutionists. Mol Ecol 16:3737–3758

    Article  PubMed  CAS  Google Scholar 

  • Cavers S, Navarro C, Lowe AJ (2004) Targeting genetic resource conservation in widespread species: a case of Cedrela odorata L. Forest Ecol Manage 197:285–294

    Article  Google Scholar 

  • Chebez JC, Hilgert N (2003) Brief history of conservation in the parana forest. In: Galindo-Leal C, de Gusmão Câmara I (eds) The Atlantic Forest of South America: biodiversity status, threats, and outlook. Island Press, Washington, pp 141–159

    Google Scholar 

  • Cohen KM, Finney SC, Gibbard PL, Fan JX (2013) The ICS International Chronostratigraphic Chart. Episodes 36:199–204

    Google Scholar 

  • Crisci JV, Katinas L, Posadas P (2000) Introducción a la teoría y práctica de la Biogeografía Histórica. Sociedad Argentina de Botánica, Buenos Aires, Argentina

    Google Scholar 

  • Crow JF, Aoki K (1984) Group selection for a polygenic behavioral trait: estimating the degree of population’s subdivision. Proc Natl Acad Sci USA 81:6073–6077

    Article  PubMed  CAS  Google Scholar 

  • de Lacerda AE, Biscaia R, Nimmo E, Sebbenn AM (2013) Modeling the long-term impacts of logging on genetic diversity and demography of. Hymenaea courbaril Forest Sci 59(1):15–26

    Article  Google Scholar 

  • de la Torre A, López C, Yglesias E, Cornelius JP (2008) Genetic (AFLP) diversity of nine Cedrela odorata populations in Madre de Dios, southern Peruvian Amazon. Forest Ecol Manage 255:334–339

    Article  Google Scholar 

  • Degen B, Blanc L, Caron H, Maggia L, Kremer A, Gourlet-Fleury S (2006) Impact of selective logging on genetic composition and demographic structure of four tropical tree species. Biol Conserv 131:386–401

    Article  Google Scholar 

  • del Fueyo G, Caccavaru MA, Dome EA (2008) Morphology and structure of the pollen cone and pollen grain of the Araucaria species from Argentina. Biocell 32:49–60

    PubMed  Google Scholar 

  • Di Bitetti MS, Placci G, Dietz LA (2003) Una Visión de Biodiversidad para la Ecorregión del Bosque Atlántico del Alto Paraná: Diseño de un Paisaje para la Conservación de la Biodiversidad y prioridades para las acciones de conservación. World Wildlife Fund, Washington, D.C.

    Google Scholar 

  • Earl DA, von Holdt BM (2012) Structure Harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Geneti Resour 4:359–361

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  PubMed Central  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fassola HE, Ferrere P, Muñoz D, Pahr N, Kuzdra H, Márquez S (1999) Observaciones sobre la producción de frutos y semillas en plantaciones de Araucaria angustifolia (Bert) O. K. (período 1993–1998). Informe Técnico N° 24 INTA EEA Montecarlo, Montecarlo, Misiones, Argentina

  • Fernández R, Fassola H, Moscovich F, Pinazo M, Pahr N (2005) Campo Manuel Belgrano Compromiso Público con la Conservación Genética de la Araucaria. Idia XXI Forestales Año 5(8):272–275

    Google Scholar 

  • Ferreira de Souza MI, Salgueiro F, Carnavale-Bottino M, Félix DB, Alves-Ferreira M, Bittencourt JVM, Margis R (2009) Patterns of genetic diversity in southern and southeastern Araucaria angustifolia (Bert.) O. Kuntze relict populations. Genet Mol Biol 32(3):546–556

    Article  CAS  Google Scholar 

  • Ferrero Klabunde GH (2012) Análise filogeográfica entre populações de Araucaria angustifolia. In: (Bert.) O. Kuntze em sua área de distribuição natural. Dissertação Grau de Mestre em Ciências. Programa de Pós-Graduação em Recursos Genéticos Vegetais da Universidade Federal de Santa Catarina, Santa Catarina, Brasil

    Google Scholar 

  • Finger A, Radespiel U, Habel JC, Kettle CJ (2014) Forest Fragmentation Genetics: What Can Genetics Tell Us About Forest Fragmentation? In: Kettle CJ, Koh LP (eds) Global Forest Fragmentation. Department of Environmental System Science, ETH Zurich, pp 50–68

    Google Scholar 

  • Finkeldey R, Hattemer HH (2007) Tropical forest genetics. Springer, Berlin

    Book  Google Scholar 

  • Gallo LA (2013) Domesticación y mejora de especies forestales nativas para la incertidumbre climática. Revista de Producción Forestal 7:39–42

    Google Scholar 

  • Gallo LA, Marchelli P, Chauchard L, Gonzalez Peñalba MG (2009) Knowing and doing: research leading to action in the conservation of forest genetic diversity of Patagonian Temperate Forests. Conserv Biol 23(4):895–898

    Article  PubMed  Google Scholar 

  • Gillies ACM, Navarro C, Lowe AJ, Newton AC, Hernández M, Wilson J, Cornelius JP (1999) Genetic diversity in Mesoamerican populations of mahogany (Swietenia macrophylla), assessed using RAPDs. Heredity 83:722–732

    Article  PubMed  Google Scholar 

  • Goya J, Sandoval M, Arturi M, Burns S, Russo F, Santacá M, Azcona M, Sañudo G (2012) Plan de Manejo Forestal del Campo Anexo Manuel Belgrano perteneciente a la EAA Montecarlo del INTA, Misiones. Laboratorio de Investigación de Sistemas Ecológicos y Ambientales (LISEA), Facultad de Ciencias Agrarias y Forestales. Universidad Nacional de La Plata, La Plata, Buenos Aires

    Google Scholar 

  • Hamrick JL, Godt MJW (1989) Allozyme diversity in plant species. In: Brown AHD, Clegg MT, Kahler AL, Weir BS (eds) Plant population genetics, breeding and genetic resources. Sinauer, Sunderland, pp 43–63

    Google Scholar 

  • Hamrick JL, Godt MJW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. New For 6:95–124

    Article  Google Scholar 

  • Holz S, Placci LG (2003) Socioeconomic roots of biodiversity loss in Misiones. In: Galindo L, De Gusmao Camara CI (eds) The Atlantic Forest of South America: Biodiversity Status, Threats and Outlook (State of the Hotspots, 1). Island Press, Center for Applied Biodiversity Science at Conservation International, Washington DC, pp 207–226

    Google Scholar 

  • Hueck K (1953) Distribiuçao e habitat natural do pinheiro do Paraná, Departamento de Botánica, Universidade deSão Pablo. São Pablo, Brasil

    Google Scholar 

  • Hueck K (1966) Die Wälder Südamerikas. Fischer Vlg., Stuttgart

    Google Scholar 

  • Inza MV, Zelener N, Fornes L, Gallo LA (2012) Effect of latitudinal gradient and impact of logging on genetic diversity of Cedrela lilloi along the Argentine Yungas Rainforest. Ecol Evol 2(11):2722–2736

    Article  PubMed  PubMed Central  Google Scholar 

  • IUCN (2018) IUCN red list of threatened species. https://www.iucnredlist.org. Version 2017.1. Accessed 16 Mar 2018

  • Izquierdo AE, Grau HR, Mitchell Aide T (2011) Implications of Rural-Urban Migration for Conservation of the Atlantic Forest and Urban Growth in Misiones, Argentina (1970–2030). Ambio 40:298–309

    Article  PubMed  Google Scholar 

  • Jump AS, Peñuelas JP (2007) Extensive spatial genetic structure revealed by AFLP but not SSR molecular markers in the wind-pollinated tree, Fagus sylvatica. Mol Ecol 16:925–936

    Article  PubMed  CAS  Google Scholar 

  • Khan IA, Procunier JD, Humphreys DG, Tranquilly G, Schlatter AR, Marcucci Poltri S, Frohberg R, Dubcovsky J (2000) Development of PCR-based markers for a high grain protein content gene from Triticum turgidum ssp. dicoccoides transferred to bread wheat. Crop Sci 40:518–524

    Article  CAS  Google Scholar 

  • Kranitz ML, Biffin E, Clark A, Hollingsworth ML, Ruhsam M et al (2014) Evolutionary diversification of new Caledonian Araucaria. PLoS One 9(10):e110308

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kremer A, Caron H, Cavers S, Colpaert N, Gheysen G, Gribel R, Lemes M, Lowe AJ, Margis R, Navarro C, Salgueiro F (2005) Monitoring genetic diversity in tropical trees with multilocus dominant markers. Heredity 95:274–280

    Article  PubMed  CAS  Google Scholar 

  • Latorre F, Alarcón P, Fassola H (2013) Distribución temporal y espacial del polen de Araucaria angustifolia (Araucariaceae) en Misiones, Argentina. Bol Soc Argent Bot 48(3–4):453–464

    Google Scholar 

  • Ledru MP, Salgado-Labouriau ML, Lorscheitter ML (1998) Vegetation dynamics in southern and central Brazil during the last 10000 year BP. Rev Palaeobot Palynol 99:131–142

    Article  Google Scholar 

  • Lowe AJ, Boshier D, Ward M, Bacles CFE, Navarro C (2005) Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity 95:255–273

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Mol Ecol 3:91–99

    Article  PubMed  CAS  Google Scholar 

  • Mac Donagh P, Rivero L (2005) ¿Es posible el uso sustentable de los Bosques de la Selva Misionera? In: Brown A, Martínez Ortiz U, Acerbi M, Corcuera J (eds) La situación ambiental argentina 2005, 1st edn. Fundación Vida Silvestre Argentina, Buenos Aires, Argentina, pp 210–217

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Mariette S, Chagné D, Lécier C, Pastuszka P, Raffin A, Plomion C, Kremer A (2001) Genetic diversity within and among Pinus pinaster populations: comparison between AFLP and microsatellite markers. Heredity 86:469–479

    Article  PubMed  CAS  Google Scholar 

  • Martin PR, McKay JK (2004) Latitudinal variation in genetic divergence of populations and the potential for future speciation. Evolution 58(5):938–945

    Article  PubMed  Google Scholar 

  • Medri C, Ruas PM, Higa AR, Murakami M, de Fátima Ruas C (2003) Effects of forest management on the genetic diversity in a population of Araucaria angustifolia (Bert.). O Kuntze Silvae Genet 52:202–205

    Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  PubMed Central  CAS  Google Scholar 

  • Newton AC, Allnutt TR, Gillies ACM, Lowe AJ, Ennos RA (1999) Molecular phylogeography, intraspecific variation and the conservation of tree species. Tree 14(4):140–145

    PubMed  CAS  Google Scholar 

  • Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155

    Article  PubMed  CAS  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX6: genetic analysis in Excel. Population genetics software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Placci LG (2000) El desmonte en Misiones: impactos y medidas de mitigación. In: Bertonatti C, Corcuera J (eds) Situación Ambiental Argentina 2000. Fundación Vida Silvestre Argentina, Buenos Aires, Argentina, pp 349–354

    Google Scholar 

  • Placci G, Di Bitetti M (2005) Situación ambiental en la ecorregión del Bosque Atlántico del Alto Paraná (Selva Paranaense). In: Brown A, Martínez Ortiz U, Acerbi M, Corcuera J (eds) La situación ambiental argentina 2005, 1st edn. Fundación Vida Silvestre Argentina, Buenos Aires, Argentina, pp 197–210

    Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pye MG, Gadek PA (2004) Genetic diversity, differentiation and conservation in Araucaria bidwilli (Araucariaceae), Australia’s Bunya pine. Conserv Genet 5:619–629

    Article  CAS  Google Scholar 

  • Pye MG, Henwood MJ, Gadek PA (2009) Differential levels of genetic diversity and divergence among populations of an ancient Australian rainforest conifer, Araucaria cunninghamii. Plant Syst Evol 277:173–185

    Article  Google Scholar 

  • Ragonese A, Castiglione J (1946) Los pinares de Araucaria angustifolia en la República. Argentina Boletín de la Sociedad Argentina de Botánica 1(2):126–147

    Google Scholar 

  • Rau MF (2005) Land Use Change and Natural Araucaria Forest Degradation Northeastern Misiones, Argentina.Dissertation to the Doctorate of the Faculty of Forestry, Albert-Ludwigs-University Freiburg in Breisgau, Germany

  • Rohlf FJ (1998) NTSYS-PC Numerical Taxonomy and Multivariate Analysis System version 2.0. Exeter Software, Setauket

  • Sarasola M, Zelener N, Fassola H, Pahr N, Fernandez R, Torales S (2011) Diversidad genética de Araucaria angustifolia (Bert.) O. Ktze. en una Reserva Forestal Argentina. Análisis de semillas 5:84–88

    Google Scholar 

  • SAyDS (2007) Primer Inventario Nacional de Bosques Nativos. Informe Regional Selva Misionera. Secretaría de Ambiente y Desarrollo Sustentable de la Nación, Buenos Aires, Argentina

    Google Scholar 

  • Sebbenn AM, Pontinha AAS, Giannotti E, Kageyama PY (2003) Genetic variation in provenance-progeny test of Araucaria angustifolia (Bert.) O. Ktze. in Saõ Paulo, Brazil. Silvae Genet 52:181–184

    Google Scholar 

  • Silveira Wrege M, Higa RCV, Miranda Britez R, Cordeiro Garrastazu M, de Sousa VA, Caramori PH, Radin B, Braga HJ (2009) Climate change and conservation of Araucaria angustifolia in Brazil. Unasylva 60(231–232):30–33

    Google Scholar 

  • Soldati MC, Fornes L, van Zonneveld M, Thomas E, Zelener N (2013) An assessment of the genetic diversity of Cedrela balansae (Meliaceae) in Northwestern Argentina by means of combined use of SSR and AFLP molecular markers. Biochem Syst Ecol 47:45–55

    Article  CAS  Google Scholar 

  • Sousa VA, Robinson IP, Hattemer HH (2004) Variation and population structure at enzyme gene loci in Araucaria angustifolia (Bert.) O. Ktze. Silvae Genet 53:12–19

    Article  Google Scholar 

  • 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 34:221–223

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Stefenon VM, Behling H, Gailing O, Finkeldey R (2008a) Evidences of delayed size recovery in Araucaria angustifolia populations after post-glacial colonization of highlands in Southeastern Brazil. An Acad Bras Cienc 80:433–443

    Article  PubMed  Google Scholar 

  • Stefenon VM, Gailing O, Finkeldey R (2008b) Genetic structure of plantations and the conservation of genetic resources of Brazilian pine (Araucaria angustifolia). For Ecol Manage 255:2718–2725

    Article  Google Scholar 

  • Stefenon VM, Steiner N, Guerra M, Nodari R (2009) Integrating approaches towards the conservation of forest genetic resources: a case study of Araucaria angustifolia. Biodivers Conserv 18:2433–2448

    Article  Google Scholar 

  • Vekemans X (2002) AFLP-SURV version 1.0. Distributed by the author. Laboratoire de Génétique et Ecologie Végétale, Université Libre de Bruxelles, Belgium

    Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Young AG, Boyle TJ (2000) Forest Fragmentation. In: Young A, Boshier D, Boyle TJ (eds) Forest conservation genetics: principles and practice. CSIRO, CABI, Australia, pp 123–134

    Chapter  Google Scholar 

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Acknowledgements

This research was financed by the National Institute of Agricultural Technology (INTA) (PNFOR 044331). We thank the EEA INTA Montecarlo’s technical teams, who participated in plant collection in Misiones. We also thank María de la Paz Sarasola and Andrea González for DNA extraction assistance. We acknowledge Martin Pinazo for providing information of the plantation from the Reserve Forest of Campo Anexo Manuel Belgrano (CAMB) and Julia Sabio y García for language editing.

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Inza, M.V., Aguirre, N.C., Torales, S.L. et al. Genetic variability of Araucaria angustifolia in the Argentinean Parana Forest and implications for management and conservation. Trees 32, 1135–1146 (2018). https://doi.org/10.1007/s00468-018-1701-4

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