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

Published online by Cambridge University Press:  22 August 2017

Daniela A. Martínez-Natarén ,
Víctor Parra-Tabla  and
Miguel A. Munguía-Rosas
Daniela A. Martínez-Natarén
Affiliation:
CONACyT Laboratorio de Ecología Terrestre, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (Cinvestav), Km 6, Antigua carretera a Progreso, Mérida 97310, México
Víctor Parra-Tabla
Affiliation:
Departamento de Ecología Tropical, Universidad Autónoma de Yucatán, Km. 15.5, Carretera Mérida-Xmatkuil, Mérida 97315, México
Miguel A. Munguía-Rosas*
Affiliation:
Laboratorio de Ecología Terrestre, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (Cinvestav), Km 6, Antigua carretera a Progreso, Mérida 97310, México
*
*Corresponding author. Email: [email protected]
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Abstract:

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.

Keywords

forest fragmentationgene flowgenetic diversityManilkara zapotapatch spatial configurationYucatan Peninsula
Type
Research Article
Information
Journal of Tropical Ecology , Volume 33 , Issue 4 , July 2017 , pp. 285 - 294
Copyright
Copyright © Cambridge University Press 2017 

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References

LITERATURE CITED

ACOSTA-LUGO, E., ALONZO-PARRA, D., ANDRADE-HERNÁNDEZ, M., CASTILLO-TZAB, D., CHABLÉ-SANTOS, J., DURÁN, R., ESPADAS-MANRIQUE, C., FERNÁNDEZ-STOHANZLOVA, I., FRAGA, J., GALICIA, E., GÓNZALEZ-ITURBE, J. A., HERRERA-SILVEIRA, J., SOSA-ESCALANTE, J., VILLALOBOS-ZAPATA, G. J. & TUN-DZUL, F. 2010. Plan de Conservación de la Eco-región Petenes-Celestún-Palmar. Pronatura Península de Yucatán, Mérida. 177 pp.Google Scholar
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 17:5177–5188.CrossRefGoogle ScholarPubMed
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 5:13–15.CrossRefGoogle Scholar
BACLES, C. F. & JUMP, A. S. 2011. Taking a tree's perspective on forest fragmentation genetics. Trends in Plant Science 16:13–18.CrossRefGoogle ScholarPubMed
BARRETT, S. C. H. & KOHN, J. R. 1991. Genetic and evolutionary consequences of small population size in plants: implication for conservation. Pp. 3–30 in Falk, D. A. & Holsinger, K. E. (eds). Genetics and conservation of rare plants. Oxford University Press, New York.CrossRefGoogle Scholar
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 115:108–114.CrossRefGoogle ScholarPubMed
BROOKFIELD, J. 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Molecular Ecology 5:453–455.CrossRefGoogle ScholarPubMed
BURGOS-SOLÍS, Y. & MONTIEL, S. 2016. Prospección alimentaria del mono araña (Ateles geoffroyi) en petenes del humedal costero de Campeche, México. Acta Zoológica Mexicana 32:404–406.CrossRefGoogle Scholar
CHASE, M. W. & HILLS, H. H. 1991. Silica gel: an ideal material for field preservation of leaf samples for DNA studies. Taxon 40:215–220.CrossRefGoogle Scholar
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 157:389–397.CrossRefGoogle ScholarPubMed
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 90:1030–1041.CrossRefGoogle Scholar
COUVET, D. 2002. Deleterious effects of restricted gene flow in fragmented populations. Conservation Biology 16:369–376.CrossRefGoogle Scholar
CRAWLEY, M. J. 2013. The R book. John Wiley and Sons, Chichester. 1051 pp.Google Scholar
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 19:299–306.CrossRefGoogle Scholar
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: 35–40.Google Scholar
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 8:1585–1592.CrossRefGoogle ScholarPubMed
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 268:2391–2396.CrossRefGoogle ScholarPubMed
DOYLE, J. J. & DOYLE, J. L. 1987. A rapid procedure for DNA purification from small quantities of fresh leaf tissue. Phytochemical Bulletin 19:11–15.Google Scholar
DURÁN, R. 1987. Lista florística de la región de los Petenes, Campeche, México. Biótica 12:199–208.Google Scholar
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: 217–242.CrossRefGoogle Scholar
EXCOFFIER, L. LAVAL, G. & SCHNEIDER, S. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1:47–50.CrossRefGoogle Scholar
FAHRIG, L. 2003. Effects of habitat fragmentation on biodiversity. Annual Review of Ecology Evolution and Systematics 34:487–515.CrossRefGoogle Scholar
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 31:437–447.CrossRefGoogle Scholar
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.Google Scholar
GOUDET, J. 1995. FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86:485–486.CrossRefGoogle Scholar
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 29:749–763.Google Scholar
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.CrossRefGoogle ScholarPubMed
HADLEY, A. S. & BETTS, M. G. 2012. The effects of landscape fragmentation on pollination dynamics: absence of evidence not evidence of absence. Biological Reviews 87:526–544.CrossRefGoogle Scholar
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 11:1–12.Google ScholarPubMed
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 8:627–632.CrossRefGoogle Scholar
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 56:841–854.CrossRefGoogle Scholar
KALINOWSKI, S. T. 2004. Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conservation Genetics 5:539–543.CrossRefGoogle Scholar
KRAMER, A. T., ISON, J. L., ASHLEY, M. V. & HOWE, H. F. 2008. The paradox of forest fragmentation genetics. Conservation Biology 22:878–885.CrossRefGoogle ScholarPubMed
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: 378–392.CrossRefGoogle ScholarPubMed
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 87:469–482.CrossRefGoogle ScholarPubMed
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 155:47–53.CrossRefGoogle Scholar
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 1:97–109.CrossRefGoogle Scholar
LOVELESS, M. D. & HAMRICK, J. L. 1984. Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics 15:65–95.CrossRefGoogle Scholar
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 95:255–273.CrossRefGoogle ScholarPubMed
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 115:97–99.CrossRefGoogle ScholarPubMed
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: 535–547.CrossRefGoogle Scholar
MAS, J. F. & CORREA, J. 2000. Análisis de la fragmentación del paisaje en el área protegida Los Petenes, Campeche, México. Investigaciones Geográficas 43:42–59.Google Scholar
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 22:267–276.CrossRefGoogle Scholar
MUNGUÍA-ROSAS, M. A. & MONTIEL, S. 2014. Patch size and isolation predict plant species density in a naturally fragmented forest. PLoS ONE 9:e111742.CrossRefGoogle Scholar
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 30:323–333.CrossRefGoogle Scholar
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 67:167–174.CrossRefGoogle Scholar
NASON, J. D. & HAMRICK, J. L. 1997. Reproductive and genetic consequences of forest fragmentation: two case studies of neotropical canopy trees. Journal of Heredity 88:264–276.CrossRefGoogle Scholar
O'FARRILL, G., CALMÉ, S. & GONZALEZ, A. 2006. Manilkara zapota: a new record of a species dispersed by tapirs. Tapir Conservation 15:32–35.Google Scholar
PEAKALL, R. & SMOUSE, P. E. 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28:2537–2539.CrossRefGoogle ScholarPubMed
PENNINGTON, T. D. 1991. The genera of Sapotaceae. Kew & New York Botanical Garden, New York. 307 pp.Google Scholar
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 12:17–42.CrossRefGoogle Scholar
PITHER, R. & KELLMAN, M. 2002. Tree species diversity in small, tropical riparian forest fragments in Belize, Central America. Biodiversity and Conservation 11:1623–1636.CrossRefGoogle Scholar
RAYMOND, M. & ROUSSET, F. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86:248–249.CrossRefGoogle Scholar
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 90:1199–1209.CrossRefGoogle Scholar
RICO-GRAY, V. 1982. Estudio de la vegetación de la zona costera inundable del noreste del estado de Campeche, México: los Petenes. Biótica 7:171–190.Google Scholar
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: 53–61.CrossRefGoogle Scholar
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. 189–213 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.CrossRefGoogle Scholar
ROUSSET, F. 2008. Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8:103–106.CrossRefGoogle ScholarPubMed
SALINAS-PEBA, L. & PARRA-TABLA, V. 2007. Phenology and pollination of Manilkara zapota in forest and homegardens. Forest Ecology and Management 248:136–142.CrossRefGoogle Scholar
SAUNDERS, D. A., HOBBS, R. J. & MARGULES, C. R. 1991. Biological consequences of ecosystem fragmentation: a review. Conservation Biology 15:18–32.CrossRefGoogle Scholar
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 48:397–407.CrossRefGoogle Scholar
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 11:1–13.CrossRefGoogle Scholar
TISCHENDORF, L. & FAHRIG, L. 2000. On the usage and measurement of landscape connectivity. Oikos 90:7–19.CrossRefGoogle Scholar
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 4:535–538.CrossRefGoogle Scholar
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 26:228–237.CrossRefGoogle ScholarPubMed
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 260:965–974.CrossRefGoogle Scholar
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: 1604–1611.CrossRefGoogle Scholar
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 99:2038–2042.CrossRefGoogle Scholar
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: 405–413.CrossRefGoogle Scholar
YOUNG, A., BOYLE, T. & BROWN, T. 1996. The population genetic consequences of habitat fragmentation for plants. Trends in Ecology and Evolution 11:413–418.CrossRefGoogle ScholarPubMed
ZAR, J. H. 1984. Biostatistical analysis. Prentice-Hall, New Jersey. 324 pp.Google Scholar
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.CrossRefGoogle Scholar