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From keystone species to conservation: conservation genetics of wax palm Ceroxylon quindiuense in the largest wild populations of Colombia and selected neighboring ex situ plant collections

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Abstract

The cloud forest of the Andean Region contains a high biodiversity. Unfortunately, human land use has caused most of the forest to become fragmented, negatively impacting many species due to the reduction of and constant change within the local habitat. In Colombia, these fragmentation triggers can include agriculture, livestock, and corridors for tourism. Conservation strategies focusing on keystone species could have more impact and better results to recover ecosystem dynamics. The wax palm Ceroxylon quindiuense (C. quindiuense) is an endemic and keystone species in cloud forests with a distribution across the three cordilleras of Colombia. Despite its ecological, economic and social importance, most forests of C. quindiuense are endangered; the most severely affected residing in small isolated populations in Central Cordillera. Nevertheless, these populations seem to retain a high genetic diversity. Because of this, the goal of conservation strategies should focus on retaining genetic diversity instead of increasing it. Because it can take as long as 80 years for C. quindiuense to reach maturity, our approach entails the introduction of juveniles (around 30 years) with genetic profiles similar to wild populations in order to augment population size, connect isolated populations, and avoid outbreeding. We evaluated the genetic makeup of three neighboring ex situ collections of living palms and compared them with the genetic profile of three wild populations of Central Cordillera. Multivariate analysis was used to assess patterns of genetic similarity and assign individuals to infer genetic clusters between collections and wild populations. Expected heterozygosity (He) of ex situ collections was lower (0.56) than wild populations (0.63), and the percentage of private alleles was higher in the wild populations (25%) than ex situ collections (10%). Collections Milan and Botanic Garden show genetic similarity with the Cocora and La Linea populations while the Toche and Roso collections were the most genetically distinct among the ones studied. Our results are that conservation programs should consider each population as a different evolutionary unit and protect them as such.

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References

  • Abbo S, Berger J, Turner NC (2003) Viewpoint: evolution of cultivated chickpea: four bottlenecks limit diversity and constrain adaptation. Funct Plant Biol 30:1081–1087

    PubMed  Google Scholar 

  • Anthelme F, Lincango J, Gully C, Duarte N, Montúfar R (2011) How anthropogenic disturbances affect the resilience of a keystone palm tree in the threatened Andean cloud forest? Biol Conserv 144:1059–1067

    Google Scholar 

  • Armenteras D, Cadena VC, Moreno RP (2007) Evaluación del estado de los bosques de niebla y de la meta 2010 en Colombia. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá

    Google Scholar 

  • Armenteras D, Espelta J, Rodríguez N, Retana J (2017) Deforestation dynamics and drivers in different forest types in Latin America: Three decades of studies (1980–2010). Global Environ Change 46:139–147

    Google Scholar 

  • Bernal R, Sanín MJ (2013) Los palmares de Ceroxylon quindiuense (Arecaceae) en el Valle de Cocora, Quindío: perspectivas de un ícono escénico de Colombia. Colomb For 16:67–79

    Google Scholar 

  • Bernal R, Galeano G, Sanín MJ (2015) Plan de conservación, manejo y uso sostenible de la palma de cera del Quindío (Ceroxylon quindiuense), Árbol Nacional de Colombia. Ministerio de Ambiente y Desarrollo Sostenible; Universidad Nacional de Colombia, Bogotá, D.C., Colombia

  • Blouin MS, Parsons M, Lacaille V, Lotz S (1996) Use of microsatellite loci to classify individuals by relatedness. Mol Ecol 5:393–401

    CAS  PubMed  Google Scholar 

  • Bruijnzeel L, Kappelle M, Mulligan M, Scatena F (2010) Tropical mountain cloud forest: state of knowledge and sustainability perspectives in a changing world. In: Bruijnzeel L, Kappelle M, Mulligan M, Scatena F (eds) Tropical mountain cloud forests: science for Conservation and Management. Cambridge University Press, Cambridge, p 768

    Google Scholar 

  • Brummit N, Lughada EI (2003) Biodiversity: where’s hot and where’s not. Conserv Biol 17:1442–1444

    Google Scholar 

  • Bubb P, May I, Miles L, Sayer J (2004) Cloud forest agenda. UNEP-WCMC, Cambridge

    Google Scholar 

  • Castro-Nuñez A, Mertz O, Casanova AB, Sosa CC, Lee S (2017) Land related grievances shape tropical forest-cover in areas affected by armed-conflict. Appl Geogr 85:39–50

    Google Scholar 

  • Cibrian-Jaramillo A, Daly AC, Brenner E, Desalle R, Marler TE (2010) When north and south don’t mix: genetic connectivity of a recently endangered oceanic cycad, Cycas micronesica in Guam using EST-microsatellites. Mol Ecol 19(12):2364–2379

    CAS  PubMed  Google Scholar 

  • Cibrian-Jaramillo A, Hird A, Oleas N, Ma H, Meerow AW, Francisco-Ortega J, Griffith MP (2013) What is the conservation value of a plant in a botanic garden? Using indicators to improve management of ex situ collections. Bot Rev 79(4):559–577

    Google Scholar 

  • Doumenge C, Gilmour D, Pérez MR, Blockhus J (1995) Tropical montane cloud forests: conservation status and management issues. In: Tropical montane cloud forests. Springer, New York, NY.

    Google Scholar 

  • Etisham-Ul-Haq M, Allnutt TR, Smith-Ramirez C, Gardner MF, Armesto JJ, Newton AC (2001) Patterns of genetic variation in and ex situ populations of the threatened Chilean Vine Berberidopsis corallina, detected using RAPD markers. Ann Bot 87:813–821

    CAS  Google Scholar 

  • Etter A, Van Wyngaarden W (2000) Patterns of landscape transformation in Colombia, with emphasis in the Andean region. Ambio 29(7):432–439

    Google Scholar 

  • Excoffier L, Heckel G (2006) Computer programs for population genetics data analysis: a survival guide. Nat Rev Genet 7:745

    CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HE (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

    PubMed  Google Scholar 

  • Fenster CB, Galloway LF (2000) Population differentiation in an annual legume: genetic architecture. Evolution 54:1157–1172

    CAS  PubMed  Google Scholar 

  • Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618

    PubMed  Google Scholar 

  • Frankham R, Ballou JD, Eldridge MD, Lacy RC, Ralls K, Dudash MR, Fenster ChB (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475

    PubMed  Google Scholar 

  • Frankham R, Bradshaw CJ, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, red list criteria and population viability analysis. Biol Cons 170:56–63

    Google Scholar 

  • Frantz AC, Pourtois T, Heuertz M, Schley L, Flamand MC, Krier A, Bertouille S, Chaumont F, Burke T (2006) Genetic structure and assignment tests demonstrate illegal translocation of red deer (Cervus elaphus) into a continuous population. Mol Ecol 15:3191–3203

    CAS  PubMed  Google Scholar 

  • Gaitán E (2003) Obtención y uso de secuencias microsatélites GA/CA en estudios de diversidad genética en las especies de palmas colombianas Ceroxylon sasaimae, Ceroxylon alpinum y Attalea amygdalina. Dissertation, Universidad Nacional de Colombia, Palmira, Colombia

  • Galeano G, Bernal R (2005) Palmas. In: Calderón E, Galeano G, García N (eds) Libro Rojo de las Plantas de Colombia, 2nd edn. Palmas, Frailejones y Zamias. Serie de Libros Rojos de Especies Amenazadas de Colombia, Bogotá, Colombia, pp 59–224

  • Galili T (2015) dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering. Bioinformatics 31:3718–3720

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on GST and D: forget GST but not all of statistics! Mol Ecol 19:3845–3852

    PubMed  Google Scholar 

  • Godefroid S, Piazza C, Rossi G, Buord S, Stevens AD, Aguraiuja R, Cowell C, Weekley C, Vogg G, Iriondo J, Jhonson I, Dixon B, Gordon D, Magnannon S, Valentin B, Bjureke K, Kopman R, Vicens M, Virevaire M, Vanderborght T (2011) How successful are plant species reintroductions? Biol Conserv 144:672–682

    Google Scholar 

  • Goerner A, Gloaguen R, Makeschin F (2007) Monitoring of the Ecuadorian mountain rainforest with remote sensing. J Appl Remote Sens 1:3172–3178. https://doi.org/10.1117/1.2784111

    Article  Google Scholar 

  • González-Rivillas N, Bohorquez A, Gutierrez JP, Merchan VHG (2018) Diversity and population genetic structure of the wax palm Ceroxylon quindiuense in the Colombian Coffee Region. BioRxiv, 443960

  • Griffith MP, Lewis C, Francisco-Ortega J (2011) Palm conservation at a botanic garden: a case study of the keys thatch palm. Palms 55(2):93–101

    Google Scholar 

  • Griffith MP, Calonje M, Meerow AW, Tut F, Kramer AT, Hird A, Magellan TM, Husby ChE (2015) Can a botanic garden cycad collection capture the genetic diversity in a wild population? Int J Plant Sci 176(1):1–10

    Google Scholar 

  • Guerrant E, Havens K, Vitt P (2014) Sampling for effective ex situ plant conservation. Int J Plant Sci 175(1):11–20

    Google Scholar 

  • Hare MP, Allen SK Jr, Bloomer P, Camara MD, Carnegie RB, Murfree J, Luckenbach M, Meritt D, Morrison C, Paynter K, Reece KS, Rose CG (2006) A genetic test for recruitment enhancement in Chesapeake Bay oysters, Crassostrea virginica, after population supplementation with a disease tolerant strain. Conserv Genet 7:717–734

    Google Scholar 

  • Hoban S, Schlarbaum S (2014) Optimal sampling of seeds from plant populations for ex situ conservation of genetic biodiversity, considering realistic population structure. Biol Conserv 177:90–99

    Google Scholar 

  • Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18(3):147–155

    Google Scholar 

  • IUCN (1987). living organisms. IUCN Position Statement. The IUCN Red List of Threatened Species. Version 2015-4. <www.iucnredlist.org>. Accessed 27 Feb 2016

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    PubMed  PubMed Central  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    PubMed  Google Scholar 

  • Jost L (2009) D vs. GST: response to Heller and Siegismund (2009) and Ryman and Leimar (2009). Mol Ecol 18:2088–2091

    Google Scholar 

  • Kashimshetty Y, Pelikan S, Rogstad SH (2015) Variable gene dispersal conditions and spatial deforestation patterns can interact to affect tropical tree conservation outcomes. PLoS ONE 10:e0127745

    PubMed  PubMed Central  Google Scholar 

  • Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: an R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788. https://doi.org/10.1111/2041-210X.12067

    Article  Google Scholar 

  • Kraemer P, Gerlach G. (2013) Package ‘Demerelate’. R software. https://cran.r-project.org/web/packages/Demerelate/Demerelate.pdf. Accessed 24 Dec 2015

  • Krishnan S, Ranker TA, Davis AP, Rakotomalala JJ (2013) The study of genetic diversity patterns of Coffea commersoniana, an endangered coffee species from Madagascar: a model for conservation of other littoral forest species. Tree Genet Genomes 9(1):179–187

    Google Scholar 

  • LaBastille A, Pool D (1978) On the need for a system of cloud-forest parks in Middle America and the Caribbean. Environ Conserv 5(3):183–190

    Google Scholar 

  • Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952

    Google Scholar 

  • Li Q, He T, Xu Z (2005a) Genetic evaluation of the efficacy of in situ and ex situ conservation of Parashorea chinensis (Dipterocarpaceae) in southwestern China. Biochem Genet 43:387–406

    CAS  PubMed  Google Scholar 

  • Li YY, Chen YX, Zhang X, Wu TY, Ping LUH, Cai YW (2005b) Genetic differences between wild and artificial populations of Metasequoia glyptostroboides: implications for species recovery. Conserv Biol 19:224–231

    Google Scholar 

  • Liu MH, Chen XY, Zhang X, Shen DW (2008) A population genetic evaluation of ecological restoration with the case study on Cyclobalanopsis myrsinaefolia (Fagaceae). Plant Ecol 197:31–41

    Google Scholar 

  • Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142

    PubMed  Google Scholar 

  • Maschinski J, Haskins KE, Raven PH (2012) Plant reintroduction in a changing climate. Island Press, Washington, pp 1–432

    Google Scholar 

  • McKay JK, Christian CE, Harrison S, Rice KJ (2005) How local is local?—a review of practical and conceptual issues in the genetics of restoration. Restor Ecol 13:432–440

    Google Scholar 

  • Menges ES (2008) TURNER REVIEW No. 16. Restoration demography and genetics of plants: when is a translocation successful? Aust J Bot 56:187–196

    Google Scholar 

  • Menges ES, Stacy AS, Carl WW (2016) Adaptive introductions: how multiple experiments and comparisons to wild populations provide insights into requirements for long-term introduction success of an endangered shrub. Plant Divers 38(5):238–246

    PubMed  PubMed Central  Google Scholar 

  • Miao YC, Su RJ, Zhang ZJ, Lang XD, Liu WD, Li SF (2015) Microsatellite markers indicate genetic differences between cultivated and natural populations of endangered Taxus yunnanensis. Bot J Linn Soc 177:450–461

    Google Scholar 

  • Mijangos JL, Pacioni C, Spencer P, Craig MD (2015) Contribution of genetics to ecological restoration. Mol Ecol 24(1):22–37

    PubMed  Google Scholar 

  • Namoff S, Husby C, Francisco-Ortega J, Noblick L, Lewis C, Griffith P (2010) How well does a botanical garden collection of a rare palm capture the genetic variation in a wild population? Biol Conserv 143:1110–1117

    Google Scholar 

  • Nei M, Feldman MW (1972) Identity of genes by descent within and between populations under mutation and migration pressures. Theor Popul Biol 3:460–465

    CAS  PubMed  Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Pence VC (2011) Evaluating cost for the in vitro propagation and preservation of endangered plants. In vitro Cellular & Developmental Biology 47(1):176–187

    Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org. Accessed 27 Nov 2015

  • Ralls K, Ballou JD, Dudash MR, Eldridge MD, Fenster ChB, Lacy RC, Sunnucks P, Frankham R (2017) Call for a paradigm shift in the genetic management fo fragment populations. Conserv Lett 11:e12412

    Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9221

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raven P, Havens K (2014) Ex situ plant conservation and cryopreservation: breakthroughs in tropical plant conservation. Int J Plant Sci 175(1):1–2

    Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17(1):230–237

    Google Scholar 

  • Rice KJ, Emery NC (2003) Managing microevolution: restoration in the face of global change. Front Ecol Environ 9:469–478

    Google Scholar 

  • Robert A, Couvet D, Sarrazin F (2007) Integration of demographic and genetics in population restorations. Ecoscience 14(4):463–471

    Google Scholar 

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

    Google Scholar 

  • Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    PubMed  Google Scholar 

  • Ruber L, Meyer A, Sturmbauer C, Verheyen E (2001) Population structure in two sympatric species of the Lake Tanganyika cichlid tribe Eretmodini: evidence for introgression. Mol Ecol 10:1207–1225

    CAS  PubMed  Google Scholar 

  • Sanín MJ (2013) Estudios ecológicos y evolutivos en Ceroxylon (palmae: ceroxyloideae). Dissertation. Universidad Nacional de Colombia

  • Sanín MJ, Galeano G (2011) A revision of the Andean wax palms, Ceroxylon (Arecaceae). Phytotaxa 34:1–64

    Google Scholar 

  • Sanín MJ, Anthelme F, Pintaud JC, Galeano G, Bernal R (2013) Juvenile resilience and adult longevity explain residual populations of the Andean Wax Palm Ceroxylon quindiuense after Deforestation. PLoS ONE 8:74139

    Google Scholar 

  • Sanín MJ, Zapata JP, Pintaud JC, Galeano G, Bohórquez A, Tohme J, Hansen MM (2017) Up and down the blind alley: population divergence with scant gene flow in an endangered tropical lineage of Andean palms (Ceroxylon quindiuense clade: Ceroxyloideae). J Hered. https://doi.org/10.1093/jhered/esx006

    Article  PubMed  Google Scholar 

  • Santos AS, Cazetta E, Dodonov P, Faria D, Gaiotto FA (2016) Landscape-scale deforestation decreases gene flow distance of a keystone tropical palm, Euterpe edulis Mart (Arecaceae). Ecol Evol 6:6586–6598

    PubMed  PubMed Central  Google Scholar 

  • Svenning JC (1998) The effect of land-use on the local distribution of palm species in an Andean rain forest fragment in northwestern Ecuador. Biodivers Conserv 7:1529–1537

    Google Scholar 

  • Svenning JC, Harlev D, Sorensen MM, Balslev H (2009) Topographic and spatial controls of palm species distributions in a mountain rain forest, southern Ecuador. Biodivers Conserv 18:219–228

    Google Scholar 

  • Szczecińska M, Sramko G, Wołosz K, Sawicki J (2016) Genetic diversity and population structure of the rare and endangered plant species Pulsatilla patens (L.) Mill in East Central Europe. PLoS One 11(3):e0151730

    PubMed  PubMed Central  Google Scholar 

  • Walters C (2004) Principles for preserving germplasm in gene banks. In: Guerrant EO, Havens K, Maunder M (eds) Ex situ plant conservation: supporting species survival in the wild. Island Press, Washington, pp 113–138

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6):1358–1370

    CAS  PubMed  Google Scholar 

  • Wright S (1969) Evolution and the Genetics of populations, 2nd edn. The theory of gene frequencies. The University of Chicago Press, Chicago

    Google Scholar 

  • Yokogawa M, Kaneko S, Takahashi Y, Isagi Y (2013) Genetic consequences of rapid population decline and restoration of the critically endangered herb Polemonium kiushianum. Biol Conserv 157:401–408

    Google Scholar 

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Acknowledgements

This research was funded by Corporación Autónoma Regional del Quindío-CRQ, Colombia. We would like to thank Adriana Bohórquez, Patricia Zapata and Janeth Gutierrez for the big support during the lab work at the International Center for Tropical Agriculture (CIAT) and Johan Carvajal for his big help during the field work. Additionally, we would like to thank the reviwers for their comments that considerable improved this manuscript. Finally, we would like to thank Danny McSweeney, Chitra Naidu, Alicia Knudson and Allan Carrillo-Baltodano for their valuable feedback and improving the English of the manuscript.

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Authors and Affiliations

  1. Molecular and Cellular Biology Graduate Program, University of Massachusetts, 240 French Hall, Amherst, MA, USA

    Katherine Chacón-Vargas

  2. Grupo de Evolución, Ecología y Conservación (EECO), Programa de Biología, Universidad del Quindío, Carrera 15 Calle 12N, Armenia, Quindío, Colombia

    Katherine Chacón-Vargas & Víctor Hugo García-Merchán

  3. Facultad de Ciencias y Biotecnología, Universidad CES, Calle 10 A No. 22 – 04, Medellín, Colombia

    María José Sanín

  4. Department of Food Sciences, University of Massachusetts, 102 Holdsworth Way, Amherst, MA, 01003, USA

    Katherine Chacón-Vargas

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  1. Katherine Chacón-Vargas
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Chacón-Vargas, K., García-Merchán, V.H. & Sanín, M.J. From keystone species to conservation: conservation genetics of wax palm Ceroxylon quindiuense in the largest wild populations of Colombia and selected neighboring ex situ plant collections. Biodivers Conserv 29, 283–302 (2020). https://doi.org/10.1007/s10531-019-01882-w

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