Genetic variation of four tropical tree species in the Selva El Ocote Biosphere Reserve, Chiapas, Mexico
DOI:
https://doi.org/10.21829/abm128.2021.1847Keywords:
conservation genetics, ITS, natural protected area, semi-evergreen forest, tropical forestAbstract
Background and Aims: Genetic variation of tree species is poorly understood for tropical forests of Mexico. The objective was to analyze the genetic diversity of Brosimum alicastrum (Moraceae) and Sapium macrocarpum (Euphorbiaceae), successionally intermediate species and dispersed by animal (zoochory), and Cecropia peltata (Cecropiaceae) and Heliocarpus appendiculatus (Malvaceae), early successional or pioneer, zoochory and anemochory dispersal syndrome, respectively, of the semi-evergreen forest of the Selva El Ocote Biosphere Reserve (REBISO), Chiapas, Mexico.
Methods: Two DNA regions of the ribosomal nuclear gene, ITS 1-2 and ITS 3-4, were amplified as genetic markers. DNA was extracted from leaves or cambium of trees of the chosen species from three locations (or subpopulations) in the REBISO. From concatenated sequences (578 bp), the estimators of genetic diversity were obtained.
Key results: Eight haplotypes were recorded in B. alicastrum, 12 in S. macrocarpum, five in H. appendiculatus and six in C. peltata. The highest values for most of the diversity estimators were observed in S. macrocarpum (π = 0.047, Hd = 0.79, s = 10), and the lowest differentiation between subpopulations was also recorded in this species (Φst = 0.22). In contrast, H. appendiculatus and C. peltata presented lower values but greater differentiation between the subpopulations (Φst ~ 0.80).
Conclusions: Overall, the highest level of genetic diversity was recorded for S. macrocarpum, a successionally intermediate species and with zoochorous dispersal syndrome. Less variation was observed within species and greater differentiation in successionally pioneer species, H. appendiculatus and C. peltata. The genetic variation observed fits well a neutral evolutionary model; therefore, the pattern of genetic variation probably was driven by random evolutionary processes. However, the dispersal syndrome and successional affinity influence spatial distribution of genetic diversity.
Downloads
References
Álvarez-Buylla, E. R. y A. Garay-Arroyo. 1994. Population genetic structure of Cecropia obtusifolia, a tropical pioneer tree. Evolution 48(2): 437-453. DOI: https://doi.org/10.1111/j.1558-5646.1994.tb01322.x DOI: https://doi.org/10.1111/j.1558-5646.1994.tb01322.x
Álvarez, I. y J. F. Wendel. 2003. Ribosomal ITS sequences and plant phylogenetic inference. Molecular Phylogenetics and Evolution 29(3): 417-434. DOI: https://doi.org/10.1016/s1055-7903(03)00208-2 DOI: https://doi.org/10.1016/S1055-7903(03)00208-2
Angrizani, R. C., L. A. S. Contim y M. R. Lemes. 2013. Development and characterization of microsatellite markers for the endangered Amazonian Tree Aniba rosaeodora (Lauraceae). Applications in Plant Sciences 1(9): 1200516. DOI: https://doi.org/10.3732/apps.1200516 DOI: https://doi.org/10.3732/apps.1200516
Benson, D. A., M. Cavanaugh, K. Clark, I. Karsh-Mizrachi, D. J. Lipman, J. Ostell, E. W. Sayers. 2013. GenBank. Nucleic Acids Research 41 (D1): D36-D42. DOI: https://doi.org/10.1093/nar/gks1195 DOI: https://doi.org/10.1093/nar/gks1195
Berg, C. C. 1972. Brosimum alicastrum Sw. subsp. alicastrum. Flora Neotropica 7: 170-171.
Berg, C., P. F. Rosselli y D. Davidson. 2005. Cecropia. Flora Neotropica 94: 1-230.
Castilla, A. R., N. Pope, R. Jaffé y S. Jha. 2016. Elevation, not deforestation, promotes genetic differentiation in a pioneer tropical tree. PloS ONE 11(6): e0156694. DOI: https://doi.org/10.1371/journal.pone.0156694 DOI: https://doi.org/10.1371/journal.pone.0156694
Chávez-Pesqueira, M. y J. Núñez-Farfán. 2016. Genetic diversity and structure of wild populations of Carica papaya in northern Mesoamerica inferred by nuclear microsatellites and chloroplast markers. Annals of Botany 118(7): 1293-1306. DOI: https://doi.org/10.1093/aob/mcw183 DOI: https://doi.org/10.1093/aob/mcw183
China Plant BOL Group, L. De-Zhu, G. Lian-Ming, L. Hong-Tao, H. Wang, G. Xue-Jun, L. Jian-Quan, C. Zhi-Duan, Z. Shi-Liang, C. Shi-Lin, Y. Jun-Bo, F. Cheng-Xin, Z. Chun-Xia, Y. Hai-Fei, Z. Ying-Jie, S. Yong-Shuai, C. Si-Yun, Z. Lei, W. Kun, Y. Tuo y D. Guang-Wen. 2011. Comparative analysis of a large dataset indicates that internal transcribed spacer (ITS) should be incorporated into the core barcode for seed plants. Proceedings of the National Academy of Sciences 108(49): 19641-19646. DOI: https://doi.org/10.1073/pnas.1104551108 DOI: https://doi.org/10.1073/pnas.1104551108
CONABIO. 2020. EncicloVida. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO). Cd. Mx., México. http://www.enciclovida.mx (consultado diciembre de 2020).
Corander, J., P. Waldmann y M. J. Sillanpää. 2003. Bayesian Analysis of genetic differentiation between populations. Genetics 163(1): 367-374. DOI: https://doi.org/10.1093/genetics/163.1.367 DOI: https://doi.org/10.1093/genetics/163.1.367
Cornelis, B., P. Franco y D. W. Davidson. 2005. Cecropia. Flora Neotropica 94: 1-230.
Cortés-Flores, J., K. B. Hernández-Esquivel, A. González-Rodríguez y G. Ibarra-Manríquez. 2017. Flowering phenology, growth forms, and pollination syndromes in tropical dry forest species: Influence of phylogeny and abiotic factors. American Journal of Botany 104(1): 39-49. DOI: https://doi.org/10.3732/ajb.1600305 DOI: https://doi.org/10.3732/ajb.1600305
Cramer, J. M., R. C. G. Mesquita y G. B. Williamson. 2007. Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees. Biological Conservation 137(3): 415-423. DOI: https://doi.org/10.1016/j.biocon.2007.02.019 DOI: https://doi.org/10.1016/j.biocon.2007.02.019
Cruz-Salazar, B., L. Ruiz-Montoya, N. Ramírez-Marcial y M. García-Bautista. 2021. Relationship between genetic variation and diversity of tree species in tropical forests in the El Ocote Biosphere Reserve, Chiapas, Mexico. Tropical Conservation Science 14: 1-14. DOI: https://doi.org/10.1177/1940082920978143 DOI: https://doi.org/10.1177/1940082920978143
Dakwa, K. B., B. Opoku y J. Toku. 2020. The role of size and number of forest patches in the conservation of bird species in a fragmented landscape. Ostrich 91(4): 292-298. DOI: https://doi.org/10.2989/00306525.2020.1792569 DOI: https://doi.org/10.2989/00306525.2020.1792569
Dalling, J. W. 2002. Ecología de las semillas. In: Guariguatta M. R. y G. H. Kattan (eds.). Ecología y conservación de bosques neotropicales. LUR Ediciones. Cartago, Costa Rica. Pp. 299-328.
Doyle, J. J. y J. L. Doyle. 1987. Isolation of DNA from small amounts of plant tissues. BRL Focus 12(1): 13-15.
Eguiarte, L. E., N. Perez y D. Piñero. 1992. Genetic structure, outcrossing rate and heterosis in Astrocaryum mexicanum (tropical palm): implications for evolution and conservation. Heredity 69: 217-228. DOI: https://doi.org/10.1038/hdy.1992.119 DOI: https://doi.org/10.1038/hdy.1992.119
Excoffier, L., G. Laval y S. Schneider. 2005. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1: 47-50. DOI: https://doi.org/10.1177/117693430500100003 DOI: https://doi.org/10.1177/117693430500100003
FAO. 2014. The state of the world´s forest genetic resources. Commission on genetic resources for food and agriculture-Food and Agriculture Organization of the United Nations (FAO). Rome, Italy. http://www.fao.org/3/a-i3825e.pdf (consultado mayo de 2021).
Feres, J. M. Guidugli M. C., M. A. Mestriner, Sebbenn A. M., Ciampi A. Y. y A. L. Alzate-Marin. 2009. Microsatellite diversity and effective population size in a germoplasm bank of Hymenaea courbaril var. stilbocarpa (Leguminosae), an endangered tropical tree: recommendations for conservation. Genetic Resources and Crop Evolution 56: 797-807. DOI: https://doi.org/10.1007/s10722-008-9402-2 DOI: https://doi.org/10.1007/s10722-008-9402-2
Figueroa-Esquivel, E. M., F. Puebla-Olivares, L. E. Eguiarte y J. Núñez-Farfán. 2010. Genetic structure of a bird-dispersed tropical tree (Dendropanax arboreus) in a fragmented landscape in Mexico. Revista Mexicana de Biodiversidad 81(3): 789-800. DOI: https://doi.org/10.22201/ib.20078706e.2010.003.649 DOI: https://doi.org/10.22201/ib.20078706e.2010.003.649
Figueroa, J.A. y C. Vázquez-Yanes. 2002. Efecto de la calidad de la luz sobre la germinación de semillas en el árbol pionero tropical Heliocarpus appendiculatus (Tiliaceae). Revista de Biología Tropical 50(1): 31-36.
Flamenco-Sandoval, A., M. Martínez Ramos y O. R. Masera. 2007. Assessing implications of land-use and land-cover change dynamics for conservation of a highly diverse tropical rain forest. Biological Conservation 138(1-2): 131-145. DOI: https://doi.org/10.1016/j.biocon.2007.04.022 DOI: https://doi.org/10.1016/j.biocon.2007.04.022
Frankham, R. 1995. Conservation genetics. Annual Review of Genetics 29: 305-327. DOI: https://doi.org/10.1146/annurev.ge.29.120195.001513 DOI: https://doi.org/10.1146/annurev.ge.29.120195.001513
Galindo-González, J. 1998. Dispersión de semillas por murciélagos: su importancia en la conservación y regeneración del bosque tropical. Acta Zoológica Mexicana (N.S.) 73: 57-74. DOI: https://doi.org/10.21829/azm.1998.73731727
Gamba, D. y N. Muchhala. 2020. Global patterns of population genetic differentiation in seed plants. Molecular Ecology 29(18): 3413-3428. DOI: https://doi.org/10.1111/mec.15575 DOI: https://doi.org/10.1111/mec.15575
Garay-Arroyo, A. y E. R. Álvarez-Buylla. 1997. Isozyme variation in a tropical pioneer tree species (Cecropia obtusifolia, Moraceae) with high contents of secondary compounds. Biotropica 29(3): 280-290. DOI: https://doi.org/10.1111/j.1744-7429.1997.tb00429.x DOI: https://doi.org/10.1111/j.1744-7429.1997.tb00429.x
Gelmi-Candusso, T. A., E. W. Heymann y K. Heer. 2017. Effects of zoochory on the spatial genetic structure of plant populations. Molecular Ecology 26(21): 5896-5910. DOI: https://doi.org/10.1111/mec.14351 DOI: https://doi.org/10.1111/mec.14351
GenBank. 2021. National Center for Biotechnology Information, U.S. National Library of Medicine. Rockville Pike, MD, USA. http://www.ncbi.nlm.nih.gov/genbank/.
Gómez-Pompa, A. 1971. Posible papel de la vegetación secundaria en la evolución de la flora tropical. Biotropica 3(2): 125-135. DOI: https://doi.org/10.2307/2989816 DOI: https://doi.org/10.2307/2989816
González-Espinosa, M., J. A. Meave, F. Lorea-Hernández, G. Ibarra-Manríquez y A. C. Newton. 2011. The red list of Mexican cloud forest trees. Fauna and Flora International. Cambridge, UK. 124 pp.
Guariguatta, M. R. y R. Ostertag. 2002. Sucesión secundaria. In: M. Guariguatta y G. Kattan (eds.). Ecología y conservación de Bosques Neotropicales. LUR Press. Cartago, Costa Rica. Pp. 559-624
Hamrick, J. L. 2004. Response of forest trees to global environmental changes. Forest Ecology and Management 197(1-3): 323-335. DOI: https://doi.org/10.1016/j.foreco.2004.05.023 DOI: https://doi.org/10.1016/j.foreco.2004.05.023
Hamrick, J. L. y M. J. W Godt. 1996. Effects of life history traits on genetic diversity in plant species. Philosophical Transaction of Royal Society of London, Series B: Biological Sciences 351(1345): 1291-1298. DOI: https://doi.org/10.1098/rstb.1996.0112 DOI: https://doi.org/10.1098/rstb.1996.0112
Hamrick, J. L., W. M. J. Godt y S. L. Sherman-Broyles. 1992. Factors influencing levels of genetic diversity in woody plant species. New Forests 6(1-4): 95-124. DOI: https://doi.org/10.1007/BF00120641 DOI: https://doi.org/10.1007/BF00120641
Howe, H. F. 2016. Making dispersal syndromes and networks useful in tropical conservation and restoration. Global Ecology and Conservation 6: 152-178. DOI: https://doi.org/10.1016/j.gecco.2016.03.002 DOI: https://doi.org/10.1016/j.gecco.2016.03.002
Hughes, A. R., B. D. Inouye, M. T. J. Johnson, N. Underwood y M. Vellend. 2008. Ecological consequences of genetic diversity. Ecology Letters 11(6): 609-623. DOI: https://doi.org/10.1111/j.1461-0248.2008.01179.x DOI: https://doi.org/10.1111/j.1461-0248.2008.01179.x
Ibarra-Manríquez, G. y G. Cornejo-Tenorio. 2010. Diversidad de frutos de los árboles del bosque tropical perennifolio de México. Acta Botanica Mexicana 90: 51-104. DOI: https://doi.org/10.21829/abm90.2010.299 DOI: https://doi.org/10.21829/abm90.2010.299
Kamm, U., F. Gugerli, P. Rotach, P. Edwards y R. Holderegger. 2010. Open areas in a landscape enhance pollen-mediated gene flow of a tree species: evidence from northern Switzerland. Landscape Ecology 25(6): 903-911. DOI: https://doi.org/10.1007/s10980-010-9468-z DOI: https://doi.org/10.1007/s10980-010-9468-z
Laborde, J. e I. Corrales-Ferrayola. 2012. Direct seeding of Brosimum alicastrum Sw. (Moraceae) and Enterolobium cyclocarpum (Jacq.) Griseb. (Mimosaceae) in different habitats in the dry tropics of central Veracruz. Acta Botanica Mexicana 100: 107-134. DOI: https://doi.org/10.21829/abm100.2012.33 DOI: https://doi.org/10.21829/abm100.2012.33
Lasso, E., J. W. Dalling y E. Bermingham. 2011. Strong spatial genetic structure in five tropical Piper species: should the Baker-Federov hypothesis be revived for tropical shrubs? Ecology and Evolution 1(4): 502-516. DOI: https://doi.org/10.1002/ece3.40 DOI: https://doi.org/10.1002/ece3.40
Lobova, T. A., S. A. Mori, F. Blanchard, H. Peckham y P. Charles-Dominique. 2003. Cecropia as a food resource for bats in French Guiana and the significance of fruit structure in seed dispersal and longevity. American Journal of Botany 90(3): 38-403. DOI: https://doi.org/10.3732/ajb.90.3.388 DOI: https://doi.org/10.3732/ajb.90.3.388
Loveless, M. D. y J. L. Hamrick. 1984. Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics 15: 65-95. DOI: https://doi.org/10.1146/annurev.es.15.110184.000433 DOI: https://doi.org/10.1146/annurev.es.15.110184.000433
Lozano, U. F., V. W. Herrera y G. Viera. 2011. Desarrollo inicial de Aniba rosaeodora Ducke en claros artificiales de bosque primario, Amazonia Central brasilera. Ingenierias y Amazonia 4(1): 5-18.
Maldonado Méndez, M. L., D. A. Rodríguez Trejo, E. Guízar Nolazco, J. Velázquez Martínez y S. Náñez Jiménez. 2009. Reducción en riqueza de especies arbóreas por incendios en la Reserva Selva El Ocote, Chiapas. Revista de Ciencia Forestal en México 34(106): 127-148.
Manzanilla-Quiñones U., y O. A. Aguirre-Calderón. 2017. Zonificación climática actual y escenarios de cambio climático para la Reserva de la Biosfera Selva El Ocote en Chiapas, México. In: Ruiz-Montoya, L., G. Álvarez-Gordillo, N. Ramírez-Marcial y B. Cruz-Salazar (eds.). Vulnerabilidad social y biológica ante el cambio climático en la Reserva de la Biosfera Selva El Ocote. El Colegio de la Frontera Sur. San Cristóbal de Las Casas, Chiapas, México. Pp. 25-66.
Martínez-Orea, Y., A. S. Castillo y C. P. Guadarrama. 2009. La dispersión de frutos y semillas y la dinámica de comunidades. Ciencias 96: 38-41.
McCarthy, C. 1998. Chromas v. 1.45. School of Health Science, Griffith University Queensland. Queensland, Australia.
Mendoza-Arroyo, G. E., A. Morón-Ríos, M. González-Espinosa, J. A. Alayón-Gamboa y P. A. Macario-Mendoza. 2020. La superviviencia y desarrollo de plántulas de Brosimum alicastrum (Moraceae) y Psidum sartorianum (Myrtaceae) difieren en condiciones de inundación. Acta Botanica Mexicana 127: e1548. DOI: https://doi.org/10.21829/abm127.2020.1548 DOI: https://doi.org/10.21829/abm127.2020.1548
Muller-Landau, H. C. y B. D. Hardesty. 2005. Seed dispersal of woody plants in tropical forests: concepts, examples and future directions. In: Burslem, D., M. A. Pinard y S. D. Hartley (ed.). Biotic interactions in the tropics: Their role in the maintenance of species diversity. Cambridge University Press. Edinburg, UK. Pp. 268-300. DOI: https://doi.org/10.1017/cbo9780511541971.012 DOI: https://doi.org/10.1017/CBO9780511541971.012
Muñoz-Alonso, L. A., J. Nieblas-Camacho, M. A. Chau-Cortez, A. B. González-Navarro, J. López-Pérez y J. Pérez-López. 2017. Diversidad de anfibios y reptiles en la Reserva de la Biosfera Selva El Ocote: su vulnerabilidad ante la fragmentación y el cambio climático. In: Ruiz-Montoya, L., G. Álvarez-Gordillo, N. Ramírez-Marcial y B. Cruz-Salazar (eds.). Vulnerabilidad social y biológica ante el cambio climático en la Reserva de la Biosfera Selva El Ocote. El Colegio de la Frontera Sur. San Cristóbal de Las Casas, Chiapas, México. Pp. 395-488.
Nason, J. D. 2002. La estructura genética de las poblaciones de árboles. In: Guariguatta, M. R., G. H. Kattan (eds.). Ecología y conservación de bosques neotropicales. LUR Ediciones. Cartago, Costa Rica. Pp. 299-328.
Nassar, J. M., A. E García y J. A. González. 2011. Patrones de diversidad genética en especies arbóreas de bosques secos fragmentados en Venezuela. Interciencia 36(12): 914-922.
Nathan, R. y H. C. Muller-Landau. 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology and Evolution 15(7): 278-285. DOI: https://doi.org/10.1016/s0169-5347(00)01874-7 DOI: https://doi.org/10.1016/S0169-5347(00)01874-7
Nei, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York, USA. 512 pp. DOI: https://doi.org/10.7312/nei-92038
Ornelas, J. F., E. Gándara, A. A. Vásquez-Aguilar, S. Ramírez-Barahona, A. E. Ortiz-Rodriguez, C. González, M. T. Mejía Saules y E. Ruiz-Sanchez. 2016. A mistletoe tale: postglacial invasion of Psittacanthus schiedeanus (Loranthaceae) to Mesoamerican cloud forests revealed by molecular data and species distribution modeling. BMC Evolutionary Biology 16: 78. DOI: https://doi.org/10.1186/s12862-016-0648-6 DOI: https://doi.org/10.1186/s12862-016-0648-6
Pennington, T. y J. Sarukhán. 2005. Árboles tropicales de México: manual para la identificación de las principales especies. Segunda edición. Fondo de Cultura Económica. Cd. Mx., México. 523 pp.
Piñero, D., J. Caballero, D. Cabrera, C. E. Canteros, A. Casas, A. Castañeda, A. Castillo, R. Cerritos, O. Chassin-Noria, P. Colunga-GarcíaMarin, P. Delgado. P. Díaz-Jaimes. L. E. Eguiarte, A. E. Escalante, B. Espinoza, A. Fleury, S. Flores Ramírez, G. Fragoso, J. González-Astorga, V. I. Villanueva, E. Martínez, F. Martinez, J. Martínez-Castillo, A. Mastretta Yanes, R. Medellín, L. Medrano-González, F. Molina-Freaner, B. Morales Vela, A. Murguía Vega, E. P. de la Cruz, M. R. Reyes-Montes, M. R. Robles Saavedra, G. Rodríguez-Arellanes, L. Rojas Bracho, R. Romero-Martínez, Jorge H. Sahaza-Cardona, R. Salas Lizana, E. Sciutto, C. S. Baker, Y. Schramm Urrutia, C. Silva, V. Souza, M. L. Taylor, J. Urbán Ramírez, Manuel Uribe-Alcocer, M. J. Vázquez Cuevas, E. Vázquez-Domínguez, A. P. Vovides, A. Wegier, A. Zaldívar Riverón y G. Zúiga. 2008. La diversidad genética como instrumento para la conservación y el aprovechamiento de la biodiversidad: estudios en especies mexicanas. In: Piñero, D. (ed.). Capital Natural de México, volumen I: Conocimiento actual de la biodiversidad. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. Cd. Mx., México. Pp. 437-483.
Plomion, C., G. Leprovost y A. Stokes. 2001. Wood formation in trees. Plant Physiology 127(4): 1513-1523. DOI: https://doi.org/10.1104/pp.010816 DOI: https://doi.org/10.1104/pp.010816
Polzin, T. y S. V. Daneshmand. 2003. On Steiner trees and minimum spanning trees in hypergraphs. Operations Research Letters 31(1): 12-20. DOI: https://doi.org/10.1016/S0167-6377(02)00185-2 DOI: https://doi.org/10.1016/S0167-6377(02)00185-2
Qin, Y., M. Li, Y. Cao, Y. Gao y W. Zhang. 2017. Molecular thresholds of ITS2 and their implications for molecular evolution and species identification in seed plants. Scientific Reports 7(1): 17316. DOI: https://doi.org/10.1038/s41598-017-17695-2 DOI: https://doi.org/10.1038/s41598-017-17695-2
Quezada Moreno, W. F., W. D. Quezada Torres e I. Gallardo Aguilar. 2016. Plantas mucilaginosas en la clarificación del jugo de la caña de azúcar. Centro Azúcar 43(2): 1-11. DOI: https://doi.org/10.5377/ribcc.v2i1.5677
Ramírez-Marcial, N., M. Martínez-Icó, A. Luna-Gómez, C. Buet y N. E. Taylor-Aquino. 2017. Diversidad local y regional de árboles en la Reserva de la Biosfera Selva El Ocote, Chiapas. In: Ruiz-Montoya, L., G. Álvarez-Gordillo, N. Ramírez-Marcial y B. Cruz-Salazar (eds.). Vulnerabilidad social y biológica ante el cambio climático en la Reserva de la Biosfera Selva El Ocote. El Colegio de la Frontera Sur. San Cristóbal de Las Casas, Chiapas, México. Pp. 255-308.
Ricker, M., I. Ramírez-Krauss, G. Ibarra-Manríquez, E. Martínez, C. H. Ramos, G. González-Medellín, G. Gómez-Rodríguez, J. L. Palacio-Prieto y H. M. Hernández. 2007. Optimizing conservation of forest diversity: a country-wide approach in Mexico. Biodiversity and Conservation 16(6): 1927-1957. DOI: https://doi.org/10.1007/s10531-006-9112-z DOI: https://doi.org/10.1007/s10531-006-9112-z
Rodríguez-Correa, H., A. González-Rodríguez y K. Oyama. 2017. Perspectivas de la ecología molecular en un país megadiverso. Revista Mexicana de Biodiversidad 88: 3-13. DOI: https://doi.org/10.1016/j.rmb.2017.10.002 DOI: https://doi.org/10.1016/j.rmb.2017.10.002
Rosas-Guerrero, V., R. Aguilar, S. Martén-Rodríguez, L. Ashworth, M. Lopezaraiza-Mikel, J. M. Bastida y M. Quesada. 2014. A quantitative review of pollination syndromes: do floral traits predict effective pollinators? Ecology Letters 17(3): 388-400. DOI: https://doi.org/10.1111/ele.12224 DOI: https://doi.org/10.1111/ele.12224
Rozas, J., J. Sánchez-DelBarrio, X. Messeguer y R. Rozas. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19(18): 2496-2497. DOI: https://doi.org/10.1093/bioinformatics/btg359 DOI: https://doi.org/10.1093/bioinformatics/btg359
Rzedowski, J. 2006. Vegetación de México. 1ra. Edición digital. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. Cd. Mx., México. https://www.biodiversidad.gob.mx/publicaciones/librosDig/pdf/VegetacionMx_Cont.pdf (consultado mayo de 2021).
SEMARNAT. 2001. Programa de manejo de la Reserva de la Biosfera Selva El Ocote, México. Secretaría de Medio Ambiente y Recursos Naturales. Ocozocoautla de Espinosa, Chiapas, México. 144 pp. http://centro.paot.org.mx/documentos/ine/prog_manejo_selva_ocote.pdf (consultado mayo de 2021).
SEMARNAT. 2010. NORMA Oficial Mexicana NOM-059-SEMARNAT-2010, Protección ambiental-Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. Secretaría del Medio Ambiente y Recursos Naturales. Diario Oficial de la Federación. Cd. Mx., México. http://dof.gob.mx/nota_detalle.php?codigo=5173091&fecha=30/12/2010 (consultado mayo de 2021).
Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3): 585-595. DOI: https://doi.org/10.1093/genetics/123.3.585 DOI: https://doi.org/10.1093/genetics/123.3.585
Thompson, J., T. Gibson, F. Plewniak, F. Jeanmougin y D. Higgins. 1997. The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25(24): 4876-4882. DOI: https://doi.org/10.1093/nar/25.24.4876 DOI: https://doi.org/10.1093/nar/25.24.4876
Turner, I. M. 2004. The ecology of trees in the tropical rain forest. Cambridge University Press. Cambridge, UK. 298 pp. DOI: https://doi.org/10.1017/CBO9780511542206 DOI: https://doi.org/10.1017/CBO9780511542206
Vellend, M. 2005. Species diversity and genetic diversity: parallel processes and correlated patterns. The American Naturalist 166(2):199-215. DOI: https://doi.org/10.1086/431318 DOI: https://doi.org/10.1086/431318
Vera-Maloof, F. Z., L. Ruiz-Montoya. y N. Ramírez Marcial. 2019. Does the genetic diversity of Macuilillo, Oreopanax xalapensis (Araliaceae), change along successional gradients of the Montane Cloud Forest? Tropical Conservation Science 12: 1-11. DOI: https://doi.org/10.1177/1940082919872923 DOI: https://doi.org/10.1177/1940082919872923
Vibrans, H. 2009. Malezas de México. Comisión Nacional de Uso y Conocimiento de la Biodiversidad, Ciudad de México, México. http://www.conabio.gob.mx/malezasdemexico/tiliaceae/heliocarpus-appendiculatus/fichas/ficha.htm#9.%20Referencias (consultado mayo de 2021).
White, T. J., T. Bruns, S. Lee y J. Taylor. 1990. A Guide to Methods and Applications: Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M. A., D. H. Gelfand, J. J. Sninsky y T. H. White (eds.). PCR protocols: a guide to methods and applications. Academic Press. New York, USA. Pp. 315-322 DOI: https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Published
How to Cite
-
Abstract12410
-
PDF (Español)669
-
XML (Español)47
-
EPUB (Español)305
Issue
Section
License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Authors who publish in this journal accept the following conditions:
In accordance with copyright legislation, Acta Botanica Mexicana recognizes and respects the moral rights of authors, as well as the ownership of the patrimonial right, which will be assigned to the journal for its dissemination in open access. Acta Botanica Mexicana does not charge authors for sending and processing articles for publication.
All the texts published by Acta Botanica Mexicana - without exception- are distributed under the Creative Commons 4.0 Attribution-Non Commercial License (CC BY-NC 4.0 International), which allows third parties to use what is published whenever they mention the authorship of the work and the first publication in this journal.
The authors can make other independent and additional contractual agreements for the non-exclusive distribution of the version of the article published in Acta Botanica Mexicana (for example, include it in an institutional repository or publish it in a book) as long as they clearly indicate that the work was published for the first time in Acta Botanica Mexicana
As a consequence, the copyeditors will request you, together with the galley review, to issue your Letter-Transfer of Ownership of Copyright form of the first publication duly completed and signed by the author(s). This letter should be sent by email in pdf file to the email: acta.botanica@inecol.mx (Letter-Transfer of Ownership of Copyright).


