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Genetic diversity and structure of the tree Manilkara zapota in a naturally fragmented tropical forest

  • Daniela A. Martínez-Natarén (a1) (a2), Víctor Parra-Tabla (a3) and Miguel A. Munguía-Rosas (a2)


Forest fragmentation, habitat loss and isolation may have a strong effect on biodiversity in tropical forests. This can include modification of the genetic diversity and structure of plant populations. In this study, we assessed the genetic diversity and structure of the tree Manilkara zapota in 15 naturally formed fragments of semi-evergreen tropical forest, as well as in an adjacent continuous forest for comparison. Forest fragments were scattered within a matrix of wetlands and were highly variable in terms of size and degree of isolation. The naturally fragmented populations of M. zapota had slightly less allelic diversity (Ar: 3.4) than those of the continuous forest (Ar: 3.6), when corrected for sample size. However, populations in the fragments and continuous forest had very similar heterozygosity levels (HE: 0.59 in both cases). Low levels of genetic differentiation were observed among populations (FST: 0.026) and genetic structure was not consistent with isolation by distance, indicating high levels of gene flow. Genetic diversity was not explained by fragment size or degree of isolation. The relatively high genetic diversity and low inter-population genetic differentiation observed in M. zapota may be the result of long-distance pollen and seed dispersal, as well as the high proximity among patches.


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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. Molecular Ecology 17:51775188.
AZEVEDO, V. C. R., VINSON, C. C. & CIAMPI, A. Y. 2005. Twelve microsatellite loci in Manilkara huberi (Ducke) Standl (Sapotaceae), an Amazonian timber species. Molecular Ecology Notes 5:1315.
BACLES, C. F. & JUMP, A. S. 2011. Taking a tree's perspective on forest fragmentation genetics. Trends in Plant Science 16:1318.
BARRETT, S. C. H. & KOHN, J. R. 1991. Genetic and evolutionary consequences of small population size in plants: implication for conservation. Pp. 330 in Falk, D. A. & Holsinger, K. E. (eds). Genetics and conservation of rare plants. Oxford University Press, New York.
BREED, M. F., OTTEWELL, K. M., GARDNER, M. G., MARKLUND, M. H., DORMONTT, E. E. & LOWE, A. J. 2015. Mating patterns and pollinator mobility are critical traits in forest fragmentation genetics. Heredity 115:108114.
BROOKFIELD, J. 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Molecular Ecology 5:453455.
BURGOS-SOLÍS, Y. & MONTIEL, S. 2016. Prospección alimentaria del mono araña (Ateles geoffroyi) en petenes del humedal costero de Campeche, México. Acta Zoológica Mexicana 32:404406.
CHASE, M. W. & HILLS, H. H. 1991. Silica gel: an ideal material for field preservation of leaf samples for DNA studies. Taxon 40:215220.
COMPS, B., GÖMÖRY, D., LETOUZEY, J., THIÉBAUT, B. & PETIT, R. J. 2001. Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European beech. Genetics 157:389397.
CORDEIRO, N. J., NDANGALASI, H. J., McENTEE, J. P. & HOWE, H. F. 2009. Disperser limitation and recruitment of an endemic African tree in a fragmented landscape. Ecology 90:10301041.
COUVET, D. 2002. Deleterious effects of restricted gene flow in fragmented populations. Conservation Biology 16:369376.
CRAWLEY, M. J. 2013. The R book. John Wiley and Sons, Chichester. 1051 pp.
CRESTE, S., NETO, A. T. & FIGUEIRA, A. 2001. Detection of single sequence repeat polymorphisms in denaturing polyacrylamide sequencing gels by silver staining. Plant Molecular Biology Report 19:299306.
DA SILVA, E. F., DE OLIVEIRA, C. A. M., LINS-E-SILVA, A. C. B. & RODAL, M. J. N. 2008. Diversity and genetic structure of natural fragmented populations of Tapirira guianensis Aubl. in Northeastern Brazil. Bioremediation, Biodiversity and Bioavailability 2: 3540.
DAYANANDAN, S., DOLE, J., BAWA, K. S. & KESSELI, R. 1999. Population structure delineated with microsatellite markers in fragmented populations of a tropical tree, Carapa guianensis (Meliaceae). Molecular Ecology 8:15851592.
DICK, C. W. 2001. Genetic rescue of remnant tropical trees by an alien pollinator. Proceedings of the Royal Society of London. Series B, Biological Sciences 268:23912396.
DOYLE, J. J. & DOYLE, J. L. 1987. A rapid procedure for DNA purification from small quantities of fresh leaf tissue. Phytochemical Bulletin 19:1115.
DURÁN, R. 1987. Lista florística de la región de los Petenes, Campeche, México. Biótica 12:199208.
ELLSTRAND, N. C. & ELAM, D. R. 1993. Population genetic consequences of small population size: implications for plant conservation. Annual Review of Ecology and Systematics 24: 217242.
EXCOFFIER, L. LAVAL, G. & SCHNEIDER, S. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1:4750.
FAHRIG, L. 2003. Effects of habitat fragmentation on biodiversity. Annual Review of Ecology Evolution and Systematics 34:487515.
GANZHORN, S. M., THOMAS, W. W., GAIOTTO, F. A. & LEWIS, J. D. 2015. Spatial genetic structure of Manilkara maxima (Sapotaceae), a tree species from the Brazilian Atlantic forest. Journal of Tropical Ecology 31:437447.
GONZÁLEZ-HERNÁNDEZ, D., GARCÍA-PÉREZ, E. & GUNTIN-MAREY, P. 2012. Genetic characterization of Manilkara zapota from Veracruz, Mexico, with SSR markers. Agrociencia 46:883–675.
GOUDET, J. 1995. FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86:485486.
GUTIÉRREZ-AYALA, L. V., TORRESCANO-VALLE, N. & ISLEBE, G. A. 2012. Reconstrucción paleoambiental del Holoceno tardío de la reserva Los Petenes, Península de Yucatán, México. Revista Mexicana de Ciencias Geológicas 29:749763.
HADDAD, N. M., BRUDVIG, L. A., CLOBERT, J., DAVIES, K. F., GONZALEZ, A., HOLT, R. D., LOVEJOY, T. E., SEXTON, J. O., AUSTIN, M. P., COLLINS, C. D., COOK, W. M., DAMSCHEN, E. I., EWERS, R. M., FOSTER, B. L., JENKINS, C. N., KING, A. J., LAURANCE, W. F., LEVEY, D. J., MARGULES, C. R., MELBOURNE, B. A., NICHOLLS, A. O., ORROCK, J. L., SON, D. -X. & TOWNSHEND, J. R. 2015. Habitat fragmentation and its lasting impact on Earth's ecosystems. Science Advances 1:e1500052.
HADLEY, A. S. & BETTS, M. G. 2012. The effects of landscape fragmentation on pollination dynamics: absence of evidence not evidence of absence. Biological Reviews 87:526544.
HAGLER, J. R., MUELLER, S., TEUBER, L. R., MACHTLEY, S. A. & VAN DEYNZE, A. 2011. Foraging range of honey bees, Apis mellifera, in alfalfa seed production fields. Journal of Insect Science 11:112.
HEATON, H. J., WHITKUS, R. & GÓMEZ-POMPA, A. 1999. Extreme ecological and phenotypic differences in the tropical tree chicozapote (Manilkara zapota (L.) P. Royen) are not matched by genetic divergence: a random amplified polymorphic DNA (RAPD) analysis. Molecular Ecology 8:627632.
HEITHAUS, E. R., FLEMING, T. H. & OPLER, P. A. 1975. Foraging patterns and resource utilization in seven species of bats in a seasonal tropical forest. Ecology 56:841854.
KALINOWSKI, S. T. 2004. Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conservation Genetics 5:539543.
KRAMER, A. T., ISON, J. L., ASHLEY, M. V. & HOWE, H. F. 2008. The paradox of forest fragmentation genetics. Conservation Biology 22:878885.
KREMER, A., RONCE, O., ROBLEDO-ARNUNCIO, J. J., GUILLAUME, F., BOHRER, G., NATHAN, R., BRIDLE, J. R., GOMULKIEWICZ, R., KLEIN, E. K., RITLAND, K., KUPARINEN, A., GERBER, S. & SCHUELER, S. 2012. Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecology Letters 15: 378392.
LAURANCE, W. F., NASCIMENTO, H. E., LAURANCE, S. G., ADRADE, A. C., FEARNSIDE, P. M., RIBEIRO, J. E. & CAPRETZ, R. L. 2006. Rain forest fragmentation and the proliferation of successional trees. Ecology 87:469482.
LEÓN, A., ARIAS-CASTRO, C., RODRÍGUEZ-MENDIOLA, M. A., MEZA-GORDILLO, R., GUTIÉRREZ-MICELI, F. A. & NIEH, J. C. 2015. Colony foraging allocation is finely tuned to food distance and sweetness even close to a bee colony. Entomologia Experimentalis et Applicata 155:4753.
LIEBERMAN, D., LIEBERMAN, M., HARTSHORN, G. & PERALTA, R. 1985. Growth rates and age-size relationships of tropical wet forest trees in Costa Rica. Journal of Tropical Ecology 1:97109.
LOVELESS, M. D. & HAMRICK, J. L. 1984. Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics 15:6595.
LOWE, A. J., BOSHIER, D., WARD, M., BACLES, C. F. E. & NAVARRO, C. 2005. Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity 95:255273.
LOWE, A. J., CAVERS, S., BOSHIER, D., BREED, M. F. & HOLLINGSWORTH, P. M. 2015. The resilience of forest fragmentation genetics – no longer a paradox – we were just looking in the wrong place. Heredity 115:9799.
MARTÍNEZ-NATARÉN, D. A., PARRA-TABLA, V., FERRER-ORTEGA, M. M. & CALVO-IRABIÉN, L. M. 2014. Genetic diversity and genetic structure in wild populations of Mexican oregano (Lippia graveolens H.B.K.) and its relationship with the chemical composition of the essential oil. Plant Systematics and Evolution 300: 535547.
MAS, J. F. & CORREA, J. 2000. Análisis de la fragmentación del paisaje en el área protegida Los Petenes, Campeche, México. Investigaciones Geográficas 43:4259.
MONTIEL, S., ESTRADA, A. & LEÓN, P. 2006. Bat assemblages in a naturally fragmented ecosystem in the Yucatan Peninsula, Mexico: species richness, diversity and spatio-temporal dynamics. Journal of Tropical Ecology 22:267276.
MUNGUÍA-ROSAS, M. A. & MONTIEL, S. 2014. Patch size and isolation predict plant species density in a naturally fragmented forest. PLoS ONE 9:e111742.
MUNGUÍA-ROSAS, M. A., JURADO-DZIB, S. G., MEZETA-COB, C. R., MONTIEL, S., ROJAS, A. & PECH-CANCHÉ, J. M. 2014. Continuous forest has greater taxonomic, functional and phylogenetic plant diversity than an adjacent naturally fragmented forest. Journal of Tropical Ecology 30:323333.
MURAWSKI, D. A. & HAMRICK, J. L. 1991. The effect of the density of flowering individuals on the mating systems of nine tropical tree species. Heredity 67:167174.
NASON, J. D. & HAMRICK, J. L. 1997. Reproductive and genetic consequences of forest fragmentation: two case studies of neotropical canopy trees. Journal of Heredity 88:264276.
O'FARRILL, G., CALMÉ, S. & GONZALEZ, A. 2006. Manilkara zapota: a new record of a species dispersed by tapirs. Tapir Conservation 15:3235.
PEAKALL, R. & SMOUSE, P. E. 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28:25372539.
PENNINGTON, T. D. 1991. The genera of Sapotaceae. Kew & New York Botanical Garden, New York. 307 pp.
PEREZ-CORTEZ, S. & REYNA-HURTADO, R. 2008. La dieta de los pecaríes (Pecari tajacu y Tayassu pecari) en la región de Calakmul, Campeche, México. Revista Mexicana de Mastozoología 12:1742.
PITHER, R. & KELLMAN, M. 2002. Tree species diversity in small, tropical riparian forest fragments in Belize, Central America. Biodiversity and Conservation 11:16231636.
RAYMOND, M. & ROUSSET, F. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86:248249.
REYNA-HURTADO, R., ROJAS-FLORES, E. & TANNER, G. W. 2009. Home range and habitat preferences of white-lipped peccaries (Tayassu pecari) in Calakmul, Campeche, Mexico. Journal of Mammalogy 90:11991209.
RICO-GRAY, V. 1982. Estudio de la vegetación de la zona costera inundable del noreste del estado de Campeche, México: los Petenes. Biótica 7:171190.
RICO-GRAY, V. & PALACIOS-RIOS, M. 1996. Salinidad y el nivel del agua como factores en la distribución de la vegetación en la ciénaga del NW de Campeche, México. Acta Botánica Mexicana 34: 5361.
RIVERA, A. & CALMÉ, S. 2006. Forest fragmentation and the changes in the feeding ecology of the black howler monkey (Alouatta pigra) in Calakmul region. Pp. 189213 in Estrada, A., Garber, P. A., Pavelka, M. S. M. & Luecke, L. (eds). New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation. Springer, New York.
ROUSSET, F. 2008. Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8:103106.
SALINAS-PEBA, L. & PARRA-TABLA, V. 2007. Phenology and pollination of Manilkara zapota in forest and homegardens. Forest Ecology and Management 248:136142.
SAUNDERS, D. A., HOBBS, R. J. & MARGULES, C. R. 1991. Biological consequences of ecosystem fragmentation: a review. Conservation Biology 15:1832.
SHAPCOTT, A. 2000. Conservation and genetics in the fragmented monsoon rainforest in the Northern Territory, Australia: a case study of three frugivore-dispersed species. Australian Journal of Botany 48:397407.
THOMPSON, K. M., CULLEY, T. M., ZUMBERGER, A. M. & LENTZ, D. L. 2015. Genetic variation and structure in the neotropical tree, Manilkara zapota (L) P. Royen (Sapotaceae) used by the ancient Maya. Tree Genetics and Genomes 11:113.
TISCHENDORF, L. & FAHRIG, L. 2000. On the usage and measurement of landscape connectivity. Oikos 90:719.
VAN OOSTERHOUT, C., HUTCHINSON, W. F., WILLS, D. P. & SHIPLEY, P. 2004. MICRO‐CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4:535538.
VRANCKX, G. U. Y., JACQUEMYN, H., MUYS, B. & HONNAY, O. 2012. Meta-analysis of susceptibility of woody plants to loss of genetic diversity through habitat fragmentation. Conservation Biology 26:228237.
WANG, H., SORK, V. L., WU, J. & GE, J. 2010. Effect of patch size and isolation on mating patterns and seed production in an urban population of Chinese pine (Pinus tabulaeformis Carr.). Forest Ecology and Management 260:965974.
WETERINGS, M. J. A., WETERINGS-SCHONCK, S. M., VESTER, H. F. M. & CALMÉ, S. 2008. Senescence of Manilkara zapota trees and implications for large frugivorous birds in the Southern Yucatan Peninsula, Mexico. Forest Ecology and Management 256: 16041611.
WHITE, G. M., BOSHIER, D. H. & POWELL, W. 2002. Increased pollen flow counteracts fragmentation in a tropical dry forest: an example from Swietenia humilis Zuccarini. Proceedings of the National Academy of Science USA 99:20382042.
WIBERG, R. A. W., SCOBIE, A. R., A'HARA, S. W., ENNOS, R. A. & COTTRELL, J. E. 2016. The genetic consequences of long term habitat fragmentation on a self-incompatible clonal plant, Linnaea borealis L. Biological Conservation 201: 405413.
YOUNG, A., BOYLE, T. & BROWN, T. 1996. The population genetic consequences of habitat fragmentation for plants. Trends in Ecology and Evolution 11:413418.
ZAR, J. H. 1984. Biostatistical analysis. Prentice-Hall, New Jersey. 324 pp.
ZHANG, X., SHI, M. M., SHEN, D. W. & CHEN, X. Y. 2012. Habitat loss other than fragmentation per se decreased nuclear and chloroplast genetic diversity in a monoecious tree. PLoS ONE 7: e39146.



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