Genetic variation and dispersal patterns in three varieties of Pinus caribaea (Pinaceae) in the Caribbean Basin
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Keywords

Pinus caribaea varieties
genetic variation
microsatellites
lineage divergence
migration routes
Caribbean Basin

How to Cite

Rebolledo Camacho, V., Jardón Barbolla, L., Ramírez Morillo, I., Vázquez-Lobo, A., Piñero, D. and Delgado, P. (2018) “Genetic variation and dispersal patterns in three varieties of Pinus caribaea (Pinaceae) in the Caribbean Basin”, Plant Ecology and Evolution, 151(1), pp. 61-76. doi: 10.5091/plecevo.2018.1343.

Abstract

BackgroundPinus caribaea Morelet comprises three varieties of tropical pines distributed in the Caribbean Basin: P. caribaea var. hondurensis, var. caribaea, and var. bahamensis. The insular and continental distribution of these varieties, as well as the geological processes in the region, have been important factors for analysing evolutionary processes implicated in the diversification of these lineages. In this study, we evaluate the genetic and geographic structure within and between these three varieties in order to infer the possible origin and dispersal routes of these taxa.
Methods – We used six polymorphic nuclear microsatellites (nSSR) in fifteen representative populations of the three pine varieties, sampled throughout their natural range in Central America, Cuba and the Bahamas islands.
Results – The varieties contain similar levels of genetic variation (mean He = 0.571), with several populations out of Hardy-Weinberg equilibrium, and significant levels of inbreeding (0.097–0.184, P ≤ 0.05). A slight but significant genetic differentiation was found between the varieties (RST = 0.088) and populations (RST= 0.082), and genetic differentiation increased with geographic distance (r2 = 0.263). Distance and Bayesian BAPS analyses generated seven groups; two represented by the two island varieties and the remainder by the Central American populations of var. hondurensis. Migration rate estimates between pairs of groups ranged from M = 0.47 to M = 20.16. Estimates were generally higher from the continent to islands, with the highest migration rate estimated from a continental genetic group to the Cuba island group of var. hondurensis (M = 20.16).
Conclusions – This study supports the hypothesis of a recent origin of these pine taxa through the migration of an ancestor from Central America, where the historical demography is associated with events of colonization, expansion and contraction of populations. The genetic variation and differentiation suggest that the three varieties are divergent lineages that currently share allelic variants, indicating that their speciation has not yet completed.

https://doi.org/10.5091/plecevo.2018.1343
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References

Adams D.C., Jackson F.J. (1997) A phylogenetic analysis of the southern pines (Pinus subsecc. Australes Loudon): biogeographical and ecological implications. Proceedings of the Biological Society of Washington 110: 681–692.

Al-Rabab’ah M.A. (2003) Evolutionary dynamic of Pinus taeda L. in the late Quaternary: an interdisciplinary approach. PhD thesis, Texas A & M University, College Station, Texas, USA.

Al-Rabab’ah M.A., Williams C.G. (2004) An ancient bottleneck in the Lost Pines of central Texas. Molecular Ecology 13: 1075–1084. https://doi.org/10.1111/j.1365-294X.2004.02142.x

Avise J.C. (2009) Phylogeography: retrospect and prospect. Journal of Biogeography 36: 3–15. https://doi.org/10.1111/j.1365-2699.2008.02032.x

Beerli P. (1998) Estimation of migration rates and population sizes in geographically structured populations. In: Carvalho G.R. (ed.) Advances in Molecular Ecology: 39–54. IOS Press, Amsterdam.

Beerli P. (2008) Migrate version 3.4.2, a maximum likelihood and Bayesian estimator of gene flow using the coalescent. Available at http://popgen.sc.fsu.edu/oldversions/3.x/3.4/ [accessed 16 Nov. 2017].

Beerli P., Palczewski M. (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185: 313–326. https://doi.org/10.1534/genetics.109.112532

Bohonak A.J. (2002) IBD (Isolation by Distance): a program for analysis of isolation by distance. Journal of Heredity 93: 153–154. https://doi.org/10.1093/jhered/93.2.153

Boys J., Cherry M., Dayanandan S. (2005) Microsatellite analysis reveals genetically distinct populations of red pine (Pinus resinosa, Pinaceae). American Journal of Botany 92: 833–841. https://doi.org/10.3732/ajb.92.5.833

Budde K.B., González-Martínez S.C., Navascués M., Burgarella C., Mosca E., Lorenzo Z, Zabal-Aguirre M., Vendramin G.G., Verdú M., Pausas J.G., Heuertz M. (2017) Increased fire frequency promotes stronger spatial genetic structure and natural selection at regional and local scales in Pinus halepensis Mill. Annals of Botany 119: 1061–1072. https://doi.org/10.1093/aob/mcw286

Corander J., Sirén J., Arjas E. (2008) Bayesian spatial modeling of genetic population structure. Computational Statistics 23: 111–129. https://doi.org/10.1007/s00180-007-0072-x

Cornuet J.-M., Luikart G. (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001–2014.

Dakin E.E., Avise J.C. (2004) Microsatellite null alleles in parentage analysis. Heredity 93: 504–509. https://doi.org/10.1038/sj.hdy.6800545

Delgado P., Cuenca A., Escalante A.E., Molina-Freaner F., Piñero D. (2002) Comparative genetic structure in pines: evolutionary and conservation consequences. Revista Chilena de Historia Natural 75: 27–37.

Delgado P., Piñero D., Rebolledo V., Jardón L., Chi F. (2011) Genetic variation and demographic contraction of the remnant populations of Mexican Caribbean pine (Pinus caribaea var. hondurensis: Pinaceae). Annals of Forest Science 68: 121–128. https://doi.org/10.1007/s13595-011-0013-2

De-Lucas A.I., González-Martínez S.C., Vendramin G.G., Hidalgo E., Heuertz M. (2009) Spatial genetic structure in continuous and fragmented populations of Pinus pinaster Aiton. Molecular Ecology 18: 4564–4576. https://doi.org/10.1111/j.1365-294X.2009.04372.x

Dvorak W.S., Jordon A.P., Hodge G.P., Romero J.L. (2000a) Assessing evolutionary relationships of pines in the Oocarpae and Australes subsections using RAPD markers. New Forests 20: 163–192. https://doi.org/10.1023/A:1006763120982

Dvorak W.S., Gutiérrez E.A., Hodge G.R., Romero J.L., Stock J., Rivas O. (2000b) Pinus caribaea var. hondurensis. In: CAMCORE Cooperative (eds) Conservation and testing of tropical and subtropical forest tree species: 12–33. North Carolina State University.

Dvorak W.S., Hamrick J.L., Gutiérrez E.A. (2005) The origin of Caribbean pine in the seasonal swamps of the Yucatán. International Journal of Plant Science 166: 985–994. https://doi.org/10.1086/449314

Dvorak W.S., Potter K.M., Hipkins V.D., Hodge G.R. (2009) Genetic diversity and gene exchange in Pinus oocarpa, a Mesoamerican pine with resistance to the pitch canker fungus (Fusarium circinatum). International Journal of Plant Science 170: 609–626. https://doi.org/10.1086/597780

Echt C.S., May-Marquardt P., Hseih M., Zahorchak R. (1996) Characterization of microsatellite markers in eastern white pine. Genome 39: 1102–1108. https://doi.org/10.1139/g96-138

Eckenwalder J.F. (2009) Conifers of the world: the complete reference. Portland (OR), Timber Press.

El Mousadik A., Petit R.J. (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theoretical and Applied Genetics 92: 832–839. https://doi.org/10.1007/BF00221895

Elsik G.C., Minihan T.V., Hall E.S., Scarpa M.A., Williams G.C. (2000) Low-copy microsatellite markers for Pinus taeda L. Genome 43: 550–555. https://doi.org/10.1139/g00-002

ESRI (1992–2000) ArcView version 3.2. Redlands, CA.

Excoffier L., Lischer H.E. (2010) Arlequin suite version 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x

Farjon A. (1996) Biodiversity of Pinus (Pinaceae) in Mexico: speciation and palaeo-endemism. Botanical Journal of the Linnean Society 121: 365–384. https://doi.org/10.1111/j.1095-8339.1996.tb00762.x

Farjon A., Styles B.T. (1997) Pinus (Pinaceae). Flora Neotropical Monograph 75. New York, New York Botanical Garden.

Farjon A. (2005) Pines, drawings and descriptions of the genus Pinus. 2nd Ed. Leiden & Boston, Brill.

Farjon A. (2013) Pinus caribaea var. hondurensis. The IUCN Red List of Threatened Species 2013: e.T20364366A20405060. https://doi.org/10.2305/IUCN.UK.2013-1.RLTS.T20364366A20405060.en

Flores L.C., López U.J., Vargas H.J.J. (2005) Indicadores reproductivos en poblaciones naturales de Picea mexicana Martínez. Agrociencia 39:117–126.

Francis J. K. (1992) Pinus caribaea Morelet. Caribbean pine. SO-ITF-SM-53. USDA Forest Service, Southern Forest Experiment Station. New Orleans & Los Angeles, Institute of Tropical Forestry.

Furlan R. de A., Mori E.S., Tambarussi E.V., Bueno de Moraes C., de Jesús F.A., Zimback L. (2007) Estrutura genética de populacões de melhoramento de Pinus caribaea var. hondurensis por meio de marcadores microssatélites. Bragantia 66: 553–563. https://doi.org/10.1590/S0006-87052007000400004

Gernandt D.S., Geada López G., Ortiz García S., Liston A. (2005) Phylogeny and classification of Pinus. Taxon 54: 29–42. https://doi.org/10.2307/25065300

Gernandt D.S., Pérez-de la Rosa J.A. (2014) Biodiversidad de Pinophyta (coníferas) en México. Revista Mexicana de Biodiversidad Suppl. 85: S126–S133. https://doi.org/10.7550/rmb.32195

Guo W.S., Thompson A.E. (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48: 361–372. https://doi.org/10.2307/2532296

Hartl D.L., Clark A.G. (1997) Principles of population genetics. 3rd Ed. Sunderland (MA), Sinauer Associates.

Hedges S.B. (1996a) The origin of West Indian amphibians and reptiles. In: Powell R., Henderson R.W. (eds) Contributions to West Indian herpetology: a tribute to Albert Schwartz: 9–128. Ithaca, Society for the Study of Amphibians and Reptiles.

Hedges S.B. (1996b) Historical biogeography of West Indian vertebrates. Annual Review of Ecology and Systematics 27: 163–196. https://doi.org/10.1146/annurev.ecolsys.27.1.163

Hernández-León S., Gernandt D.S., Pérez de la Rosa J.A., Jardón-Barbolla L. (2013) Phylogenetic relationships and species delimitation in Pinus Section Trifoliae inferred from plastid DNA. Plos One 8: e70501. https://doi.org/10.1371/journal.pone.0070501

Iturralde-Vinent M.A. (2004–2005) La Paleogeografía del Caribe y sus implicaciones para la biogeografía histórica. Revista del Jardín Botánico Nacional 25–26: 49–78.

Iturralde-Vinent M.A. (2006) Meso-Cenozoic Caribbean paleogeography: implications for historical biogeography of the region. International Geology Review 48: 791–827. https://doi.org/10.2747/0020-6814.48.9.791

IUCN (2016) The IUCN Red List of Threatened Species, version 2016.3. Available from http://www.iucnredlist.org [accessed 11 May 2017].

Jardón-Barbolla L., Delgado-Valerio P., Geada-López G., Vázquez-Lobo A., Piñero D. (2011) Phylogeography of Pinus subsection Australes in the Caribbean Basin. Annals of Botany 107: 229–241. https://doi.org/10.1093/aob/mcq232

Karhu A. (2001) Evolution and applications of pine microsatellites. Oulu, Oulu University Press.

Karhu A., Vogl C., Moran G.F., Bell J.C., Savolainen O. (2006) Analysis of microsatellite variation in Pinus radiata reveals effects of genetic drift but no recent bottlenecks. Journal of Evolutionary Biology 19: 167–175. https://doi.org/10.1111/j.1420-9101.2005.00982.x

Krupkin A.B, Liston A., Strauss S.H. (1996) Phylogenetic analysis of the hard pines (Pinus subgenus Pinus, Pinaceae) from chloroplast DNA restriction site analysis. American Journal of Botany 83: 489–498.

Ledig F.T. (1998) Genetic variation in Pinus. In: Richardson (ed.) Ecology and biogeography of Pinus: 251–280. Cambridge, Cambridge University Press.

Leyden B.W. (1984) Guatemalan forest synthesis after Pleistocene aridity. Proceedings of National Academy of Sciences of the United States of America 81: 4856–4859.

Ma X.F., Szmidt A.E., Wang X.R. (2006) Genetic structure and evolutionary history of a diploid hybrid pine Pinus densata inferred from the nucleotide variation at seven gene loci. Molecular Biology and Evolution 23: 807–816. https://doi.org/10.1093/molbev/msj100

Mantel N. (1967) The detection of disease clustering and a generalized regression approach. Cancer Research 27: 209–220.

Mariette S., Chagné D., Lézier 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.

Marrero A., Renda A., Calzadilla E. (1998) Comportamiento de Pinus caribaea var. caribaea Morelet en diferentes tipos de suelos. Revista Cuba Forestal 1: 39–40.

Matheson A.C., Bell J.C., Barnes R.D. (1989) Breeding systems and genetic structure in some Central America pine populations. Silvae Genetica 38: 107–113.

Millar C.I. (1993) Impact of the Eocene on the evolution of Pinus L. Annals of Missouri Botanical Garden 80: 471–498. https://doi.org/10.2307/2399795

Mirov N.T. (1967) The genus Pinus. New York, The Ronald Press Company.

Moonlight P.W., Richardson J.E., Tebbitt M.C. Thomas D.C., Hollands R. Peng C.-I., Hughes M. (2015) Continental-scale diversification patterns in a megadiverse genus: the biogeography of Neotropical Begonia. Journal of Biogeography 42: 1137–1149. https://doi.org/10.1111/jbi.12496

Naydenov K.D., Alexandrov A., Matevski V., Vasilevski K., Naydenov M.K., Gyuleva V., Carcaillet C., Wahid N., Kamary S. (2014) Range-wide genetic structure of maritime pine predates the last glacial maximum: evidence from nuclear DNA. Hereditas 151: 1–13. https://doi.org/10.1111/j.1601-5223.2013.00027.x

Nei M., Tajima F., Tateno Y. (1983) Accuracy of estimated phylogenetic trees from molecular data. II Gene frequency data. Journal of Molecular Evolution 19: 153–170. https://doi.org/10.1007/BF02300753

Nikles D.G. (1966) Comparative variability and relationships of Caribbean Pine (Pinus caribaea Mor.) and Slash Pine (Pinus elliottii Engelm.) PhD thesis, College of Natural Resources, North Carolina State University, Raleigh, North Carolina, USA.

Okoro O.O. (1984) Influence of flowering habit of Pinus caribaea var. hondurensis Barr. et Golf. on seed yield. Nigerian Journal of Forest 13: 36–42.

Perry J. (1991) The pines of Mexico and Central America. Portland, Oregon Timber Press.

Petit J.R., Duminil J., Fineschi S., Hampe A., Salvini D., Vendramin GG. (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Molecular Ecology 14: 689–701. https://doi.org/10.1111/j.1365-294X.2004.02410.x

Pindell J., Kennan L., Stanek K.P., Maresch W.V., Draper G. (2006) Foundations of Gulf of Mexico and Caribbean evolution: eight controversies resolved. Geologica Acta 4: 303–341.

Piry S., Luikart G., Cornuet J.-M. (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity 90:502–503. https://doi.org/10.1093/jhered/90.4.502

QGIS Development Team (2017) QGIS version 2.14.21. Available from https://www.qgis.org/en/site/ [accessed 2 Jul. 2017].

Rajora O.P., Rahman M.H., Buchert G.P., Dancik B.P. (2000) Microsatellite DNA analysis of genetic effects of harvesting in old-growth eastern white pine (Pinus strobus) in Ontario, Canada. Molecular Ecology 9: 339–348. https://doi.org/10.1046/j.1365-294x.2000.00886.x

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

Sánchez M. (2012) Conservation genetics and biogeography of the Caribbean pine (Pinus caribaea var. bahamensis) in the Bahamas archipelago. PhD thesis, Birkbeck University of London, UK.

Sánchez M., Ingrouille M.J., Cowan R.S., Hamilton M.A., Fay M.F. (2014) Spatial structure and genetic diversity of natural populations of the Caribbean pine, Pinus caribaea var. bahamensis (Pinaceae), in the Bahaman archipelago. Botanical Journal of the Linnean Society 174: 359–383. https://doi.org/10.1111/boj.12146

Schlötterer C. (2000) Evolutionary dynamics of microsatellite DNA. Chromosoma 109: 365–371. https://doi.org/10.1007/s004120000089

Schuchert C. (1935) Historic geology of the Antillean-Caribbean region. New York, John Wiley & Sons Inc.

Shepherd M., Cross M., Maguire T.L., Dieters M.J., Williams C.G., Henry R.J. (2002) Transpecific microsatellites for hard pines. Theoretical and Applied Genetics 104: 819–827. https://doi.org/10.1007/s00122-001-0794-z

Slatkin M. (1977) Gene flow and genetic drift in a species subject to frequent local extinctions. Theoretical Population Biology 12: 253–262. https://doi.org/10.1016/0040-5809(77)90045-4

Slatkin M. (1995) A measure of population subdivision based on microsatellite allele frequency. Genetics 139: 457–462.

Sokal R.R., Rohlf FJ. (1995) Biometry: the principles and practice of statistics in biological research. New York, W.H. Freeman & Co.

Szpiech Z.A., Jakobsson M., Rosenberg N.A. (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24: 2498–2504. https://doi.org/10.1093/bioinformatics/btn478

Takezaki N., Nei M. (1996) Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144: 389–399.

Takezaki N., Nei M., Tamura K. (2010) POPTREE2: software for constructing population trees from allele frequency data and computing other population statistics with Windows interface. Molecular Biology and Evolution 27: 747–752. https://doi.org/10.1093/molbev/msp312

Tsuda Y., Chen J., Stocks M., Lascoux M., Kӓllman T., Sonstebo J. H., Parducci L., Semerikov V., Sperisen C., Politov D., Ronkainen T., Vӓliranta M., Vendramin G.G., Tollefsrud M.M., Lascoux M. (2016) The extent and meaning of hybridization and introgression between Siberian spruce (Picea obovata) and Norway spruce (P. abies): cryptic refugia as stepping stones to the west? Molecular Ecology 25: 277–2789. https://doi.org/10.1111/mec.13654

Van W.G. (2002) Pinus caribaea Morelet. In: CAB International (eds) Pines of silvicultural importance: 3–50. Wallingford, UK, CABI Publishing.

van Oosterhout C., Hutchinson W.F., Wills D.P.M., Shipley P. (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x

Vázquez-Lobo A. (1996) Evolución de hongos endófitos del género Pinus L.: implementación de técnicas moleculares y resultados preliminares. PhD Thesis, Facultad de Ciencias, UNAM, México.

Wang M.L., Barkley N.A., Jenkins T.M. (2009) Microsatellite markers in plants and insects. Part I: applications of biotechnology. Genes, Genomes and Genomics 3: 54–67.

Williams C.G., Elsik C.G., Barnes R.D. (2000) Microsatellite analysis of Pinus taeda L. in Zimbabwe. Heredity 84: 261–268.

Willyard A., Syring J., Gernandt D.S., Liston A., Cronn R. (2007) Fossil calibration of molecular divergence infers a moderate mutation rate and recent radiations for Pinus. Molecular Biology and Evolution 24: 90–101. https://doi.org/10.1093/molbev/msl131

Wright S. (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19: 395–420. https://doi.org/10.2307/2406450

Zheng Y.Q., Ennos R.A. (1999) Genetic variability and structure of natural and domesticated populations of Caribbean pine (Pinus caribaea Morelet). Theoretical and Applied Genetics 98: 765–771. https://doi.org/10.1007/s001220051133

Zinck JWE., Rajora OP. (2016) Post-glacial phylogeography and evolution of a wide-ranging highly-exploited keystone forest tree, eastern white pine (Pinus strobus) in North America: single refugium, multiple routes. BMC Evolutionary Biology 16: 1–17. https://doi.org/10.1186/s12862-016-0624-1

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