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Low genetic diversity and high differentiation among relict populations of the neotropical gymnosperm Podocarpus sellowii (Klotz.) in the Atlantic Forest

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Abstract

Podocarpus sellowii (Podocarpaceae) is one of only a few gymnosperms native to Brazil and the sole species of the genus found in the northeastern region of that country. It has a very restricted distribution in this region, with only three known populations in highland forests (called Brejos de Altitude), which apparently have been isolated from each other since the Pleistocene. Due to this long-term isolation and the fact that these populations have few adult individuals and suffer great anthropogenic pressure, low genetic variability is expected, compromising their long-term viability. The present work assessed the genetic variability and structure of northeastern populations of P. sellowii to investigate the role of Pleistocene glaciations on the genetic relationships between them and to propose strategies for their conservation by analyzing the SSR and ISSR markers of adult and juvenile individuals. Low genetic diversity was found with both markers, associated with a high differentiation of the Brejo de Baturité population in relation to the others—suggesting their isolation at different points in time, probably during the Pleistocene. Actions directed towards increasing the genetic diversity of these populations will be needed, such as planting seedlings with high genetic variability—but the high degrees of differentiation observed between the populations must be taken into account.

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References

  • Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188

    Article  PubMed  Google Scholar 

  • Andrade IM, Mayo SJ, Van Der Berg C, Fay MF, Chester M, Lexer C, Kirkup D (2007) A preliminary study of genetic variation in populations of Monstera adansonii var. klotzschiana (Araceae) from North-East Brazil, estimated with AFLP molecular markers. Ann Bot 100:1143–1154

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Andrade-Lima D (1971) Flora de Pernambuco. Podocarpaceae. XXI Congresso Nacional Sociedade Botânica do Brasil. Ciência e Cultura 23:337

    Google Scholar 

  • Andrade-Lima D (1982) Present-day forest refuges in Northeastern Brazil. In: Prance GT (ed) Biological diversification in the tropics. Plenum Press, New York, pp 245–251

    Google Scholar 

  • Araújo FS, Gomes VS, Silveira AP, Figueiredo MA, Oliveira RF, Bruno MMA, Lima-Verde LW, Silva EF, Otutumi AT, Ribeiro KA (2007) Efeito da variação topoclimática na fisionomia e estrutura da vegetação da serra de Baturité, Ceará. In: Oliveira TS, Araújo FS (eds) Diversidade de Conservação da biota na Serra de Baturité, Ceará. Edições UFC, Coelce, Fortaleza, pp 73–136

  • Auler AS, Wang X, Edwards RL, Cheng H, Cristalli PS, Smart PL, Richards DA (2004) Quaternary ecological and geomorphic changes associated with rainfall events in presently Semi-arid Northeastern Brazil. J Quat Sci 19:693–701

    Article  Google Scholar 

  • Behling H, Arz HW, Pätzold J, Wefer G (2000) Late Quaternary vegetational and climate dynamics in Northeastern Brazil, inferences from marine core GeoB 3104-1. Quat Sci Rev 19:981–994

    Article  Google Scholar 

  • Bizoux JP, Daïnou K, Bourland N, Hardy OJ, Heuertz M, Mahy G, Doucet JL (2009) Spatial genetic structure in Milicia excelsa (Moraceae) indicates extensive gene dispersal in a low-density wind-pollinated tropical tree. Mol Ecol 18:4398–4480

    Article  CAS  PubMed  Google Scholar 

  • Bornet B, Branchard M (2001) Nonanchored inter simple sequence repeat (ISSR) markers: reproducible and specific tools for genome fingerprinting. Plant Mol Biol Rep 19:209–215

    Article  CAS  Google Scholar 

  • Cabanne GS, d’Horta FM, Sari EHR, Santos FR, Miyaki CY (2008) Nuclear and mitochondrial phylogeography of the Atlantic Forest endemic Xiphorhynchus fuscus (Aves: Dendrocolaptidae): biogeography and systematics implications. Mol Phylogenet Evol 49:760–773

    Article  CAS  PubMed  Google Scholar 

  • Carnaval AC, Bates JM (2007) Amphibian DNA shows marked genetic structure and tracks Pleistocene climate change in Northeastern Brazil. Evolution 61–12:2942–2957

    Article  Google Scholar 

  • Carnaval AC, Moritz C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest. J Biogeogr 35:1187–1201

    Article  Google Scholar 

  • Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT, Moritz C (2009) Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science 323:785–789

    Article  CAS  PubMed  Google Scholar 

  • Chase MW, Hills HH (1991) Silica gel: an ideal material for field preservation of leaf samples for DNA studies. Taxon 40:215–220

    Article  Google Scholar 

  • Creste S, Tulmann Neto A, Figueira A (2001) Detection of simple sequence repeat polymorphisms in denaturing polyacrylamide sequencing gels by silver staining. Plant Mol Biol Rep 19:299–306

    Article  CAS  Google Scholar 

  • da Silva JMC, Castelletti CHM (2003) Status of the biodiversity of the Atlantic Forest of Brazil. In: Galindo-Leal C, Câmara IG (eds) The Atlantic Forest of South America: biodiversity status, threats, and outlook. Center for Applied Biodiversity Science and Island Press, Washington, DC, pp 43–59

    Google Scholar 

  • de Oliveira PE, Barreto AMF, Suguio K (1999) Late Pleistocene/Holocene climatic and vegetational history of the Brazilian caatinga: the fossil dunes of the middle São Francisco River. Palaeogeogr Palaeoclimatol Palaeoecol 152:319–337

    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  CAS  PubMed  Google Scholar 

  • 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 Res 10:564–567

    Article  Google Scholar 

  • Félix LP, Carvalho R (2002) Diversidade de Orquídeas no Estado de Pernambuco. In: Tabarelli M, Silva JMC (eds) Diagnóstico da biodiversidade de Pernambuco, vol 1. Massangana, Recife, pp 207–217

    Google Scholar 

  • Figueiredo MA, Fernandes A, Nepomuceno VAG (1990) Refúgio florístico de Podocarpus na Serra de Baturité—Ceará. XIV Reunião Nordestina de Botânica, Recife

    Google Scholar 

  • Gonçalves FR (2008) Estrutura genética em populações naturais de Podocarpus sellowii Klotzsch (Podocarpaceae) na região do Alto Rio Grande, Sul de Minas Gerais. Dissertação de mestrado. Lavras: UFLA, p 72

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html. Updated from Goudet (1995)

  • Haffer J (1969) Speciation in Amazonian forest birds. Science 165:131–137

    Article  CAS  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hardy OJ, Charbonnel N, Fréville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    Article  CAS  PubMed  Google Scholar 

  • Hokanson SC, Szewc-McFadden AK, Lamboy WF, McFerson JR (1998) Microsatellite (SSR) markers reveal genetic identities, genetic diversity and relationships in a Malus x domestica borkh. core subset collection. Theor Appl Genet 97:671–683

    Article  CAS  Google Scholar 

  • Hoorn C, Wesselingh FP, ter Steege H, Bermudez MA, Mora A, Sevink J, Sanmartín I, Sanchez-Meseguer A, Anderson CL, Figueiredo JP, Jaramillo C, Riff D, Negri FR, Hooghiemstra H, Lundberg J, Stadler T, Säarkinen T, Antonelli A (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330:927–931

    Article  CAS  PubMed  Google Scholar 

  • Ledru MP, Salatino MLF, Ceccantini G, Salatino A, Pinheiro F, Pintaud JC (2007) Regional assessment of the impact of climatic change on the distribution of a tropical conifer in the lowlands of South America. Divers Distrib 13:761–777

    Article  Google Scholar 

  • Lima TV, Barbosa DCA (1998) Levantamento da distribuição espacial de plantas jovens não estabelecidas e estabelecidas de Podocarpus sellowii Klotzsch, em Serra dos Cavalos, Caruaru—PE. Trabalho técnico, Imprensa Universitária, UFRPE, Recife, p 32

  • Lima-Verde LW, Gomes VS (2007) Plantas nativas da serra de Baturité, Ceará, com potencial ornamental. In: Oliveira TS, Araújo FS (eds) Diversidade de Conservação da biota na Serra de Baturité, Ceará. Edições UFC, Coelce, Fortaleza, pp 295–315

    Google Scholar 

  • Maldonado-Coelho M (2012) Climatic oscillations shape the phylogeographical structure of Atlantic Forest fire-eyes (Aves: Thamnophilidae). Biol J Linn Soc 105:900–924

    Article  Google Scholar 

  • Marquardt PE, Echt CS, Epperson BK, Pubanz DM (2007) Genetic structure, diversity, and inbreeding of eastern white pine under different management conditions. Can J For Res 37:2652–2662

    Article  CAS  Google Scholar 

  • Mellik R, Lowe A, Allen C, Hill RS, Rossetto M (2012) Palaeodistribution modeling and genetic evidence highlight differential post-glacial range shifts of a rain forest conifer distributed across a latitudinal gradient. J Biogeogr. doi:10.1111/j.1365-2699.2012.02747.x

    Google Scholar 

  • Miller MP (1997) Tools for population genetic analysis (TFPGA) 1.3: a Windows program for the analysis of allozyme and molecular population genetic data. Computer software distributed by author

  • Mori GM, Zucchi MI, Sampaio I, Souza AP (2010) Microsatellites for the mangrove tree Avicenia germinans (Acanthaceae): tools for hybridization and mating system studies. Am J Bot 97:e79–e81

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Oliveira TS, Figueiredo MA, Nogueira RS, Sousa SC, Souza SSG, Romero RE, Tavares RC (2007) Histórico dos impactos antrópicos e aspectos geoambientais da serra de Baturité, Ceará. In: Oliveira TS, Araújo FS (eds) Diversidade de Conservação da biota na Serra de Baturité, Ceará. Edições UFC; COELCE, Fortaleza, pp 21–27

    Google Scholar 

  • Ott J (1992) Strategies for characterizing highly polymorphic marker in human gene mapping. AJHG 51:283–290

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Perrier X, Jacquemoud-Collet JP (2006) DARwin software. http://darwin.cirad.fr/darwin. Acesso em: 30 Jun 2006

  • Perrier X, Flori A, Bonnot F (2003) Data Analysis Methods. In: Hamon P, Seguin M, Perrier X, Glasmann JC (eds) Genetic diversity of cultivated tropical plants. Enfield Science Publishers, Montpellier, pp 43–76

    Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Quiroga MP, Premoli AC (2007) Genetic patterns in Podocarpus parlatorei reveal the long-term persistence of cold-tolerant elements in the southern Yungas. J Biogeogr 34:447–455

    Article  Google Scholar 

  • Raymond R, Rousset F (1995) GENEPOP version 1.2: population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Ribas CC, Aleixo A, Nogueira ACR, Miyaki CY, Cracraft J (2012) A paleobiogeographic model for biotic diversification within Amazonia over the past three million years. Proc R Soc B 279:681–689

    Article  PubMed Central  PubMed  Google Scholar 

  • Rungis D, Bérubé Y, Zhang J, Ralph S, Ritland CE, Ellis BE, Douglas C, Bohlmann J, Ritland K (2004) Robust simple sequence repeat markers for spruce (Picea spp.) from expressed sequence tags. Theor Appl Genet 109:1283–1294

    Article  CAS  PubMed  Google Scholar 

  • Santos AMM, Cavalcanti DR, Silva JMC, Tabarelli M (2007) Biogeographical relationships among tropical forests in north-eastern Brazil. J Biogeogr 34:437–446

    Article  Google Scholar 

  • Silva FAB (2011) First record of Coprophanaeus bellicosus (Olivier) (Coleoptera, Scarabaeidae) in a “Brejo de Altitude” forest in northeastern Brazil: a historical biogeographical approach. Rev Bras Entomol 55:615–617

    Article  Google Scholar 

  • Siqueira-Filho JA (2002) Bromélias em Pernambuco: Diversidade e aspectos conservacionistas. In: Tabarelli M, Silva JMC (eds) Diagnóstico da biodiversidade de Pernambuco. Massangana, Recife, pp 219–228

    Google Scholar 

  • Su Y, Wang T, Deng F (2010) Contrasting genetic variation and differentiation on Hainan Island and the Chinese mainland populations of Dacrycarpus imbricatus (Podocarpaceae). Biochem Syst Ecol 38:576–584

    Article  CAS  Google Scholar 

  • Tabarelli M, Santos AMM (2004) Uma breve descrição sobre a história natural dos brejos nordestinos. In: Porto KC, Cabral JJP, Tabarelli M (eds) Brejos de altitude em Pernambuco e Paraíba: História Natural, Ecologia e Conservação. Brasília. Ministério do Meio Ambiente, p 324

  • Thomas E, van Zonneveld M, Loo J, Hodgkin T, Galluzzi G, van Etten J (2012) Present spatial diversity patterns of Theobroma cacao L. in the neotropics reflect genetic differentiation in pleistocene refugia followed by human-influenced dispersal. PLoS ONE 7:e47676

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vanzolini P, Williams EE (1970) South American anoles: geographic differentiation and evolution of the Anolis crysolepis species group (Sauria, Iguanidae). Arq Zool São Paulo 19:1–298

    Article  Google Scholar 

  • Wang X, Auler AS, Edwards RL, Cheng H, Cristalli PS, Smart PL, Richards DA, Shen C (2004) Wet periods in Northeastern Brazil over the past 210 kyr linked to distant climate anomalies. Nature 432:740–743

    Article  CAS  PubMed  Google Scholar 

  • Whitmore TC, Prance G (1987) Biogeography and quaternary history in Tropical America. Oxford Science Publications/Clarendon Press, Oxford

    Google Scholar 

  • Youens-Clark K, Buckler E, Casstevens T, Chen C, Declerck G, Derwent P, Dharmawardhana P, Jaiswal P, Kersey P, Karthikeyan AS, Lu J, McCouch SR, Ren L, Spooner W, Stein JC, Thomason J, Wei S, Ware D (2011) Gramene database in 2010: updates and extensions. Nucleic Acids Res 39(Database issue):D1085–D1094

  • Zellinger B, Akimcheva S, Puizina J, Schirato M, Riha K (2007) Ku suppresses formation of telomeric circles and alternative telomere lengthening in Arabidopsis. Mol Cell 27:163–169

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank the Laboratório de Análise Genética e Molecular of the Universidade Estadual de Campinas (UNICAMP) for support and infrastructure during the development of the SSR markers; to the MSc. Luiz Wilson Lima-Verde for his valuable help during the field work; the CNPq (National Council for Scientific and Technological Development) for the fellowship to LD; and PROPESQ/UFPE for financial support.

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Correspondence to Andrea Pedrosa-Harand.

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Liliane G. Dantas and Tiago Esposito have contributed equally to this work.

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Dantas, L.G., Esposito, T., de Sousa, A.C.B. et al. Low genetic diversity and high differentiation among relict populations of the neotropical gymnosperm Podocarpus sellowii (Klotz.) in the Atlantic Forest. Genetica 143, 21–30 (2015). https://doi.org/10.1007/s10709-014-9809-y

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