Plant Ecology and Evolution 151(1): 61-76, doi: 10.5091/plecevo.2018.1343
Genetic variation and dispersal patterns in three varieties of Pinus caribaea (Pinaceae) in the Caribbean Basin
expand article infoVirginia Rebolledo Camacho‡, Lev Jardón Barbolla§, Ivón Ramírez Morillo|, Alejandra Vázquez-Lobo, Daniel Piñero#, Patricia Delgado¤
‡ Instituto de Investigaciones Forestales, Universidad Veracruzana, Parque Ecológico “El Haya”, Carretera antigua a Coatepec S/N, CP 91000 Xalapa, Veracruz, Mexico§ Centro de Investigaciones Interdisciplinarias en Ciencias y Humanidades, Universidad Nacional Autónoma de México, Torre II de Humanidades, 4º piso, Ciudad Universitaria, CP 04510 Ciudad de México, Mexico| Centro de Investigación Científica de Yucatán, A.C. Calle 43 #130 x 32 y 34, Colonia Chuburná de Hidalgo, CP 97205 Mérida, Yucatán, Mexico¶ Centro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos, Av. Universidad No. 1001, Colonia Chamilpa, CP 62209 Cuernavaca, Morelos, Mexico# Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Tercer Circuito Exterior S/N, Ciudad Universitaria, CP 04510 Ciudad de México, Mexico¤ Facultad de Agrobiología “Presidente Juárez”, Universidad Michoacana de San Nicolás de Hidalgo, Paseo de la Revolución esquina con Berlín S/N, Colonia Viveros, CP 60170 Uruapan, Michoacán, Mexico

Corresponding author: Patricia Delgado ( dvalerio@umich.mx )

© Botanic Garden Meise and Royal Botanical Society of Belgium.
all rights reserved
Citation: Rebolledo Camacho V, Jardón Barbolla L, Ramírez Morillo I, Vázquez-Lobo A, Piñero D, 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): 61-76. https://doi.org/10.5091/plecevo.2018.1343
Open Access
Abstract

Background – Pinus 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.

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

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.
  • 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].
  • 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
  • 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.
  • 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., 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.
  • 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., 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.
  • 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.
  • 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
  • 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. (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.
  • 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