Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-22T19:25:07.041Z Has data issue: false hasContentIssue false

Spatial genetic structure of Manilkara maxima (Sapotaceae), a tree species from the Brazilian Atlantic forest

Published online by Cambridge University Press:  25 June 2015

S. M. Ganzhorn*
Affiliation:
Louis Calder Center – Biological Field Station, and Department of Biological Sciences, Fordham University, Armonk, NY, 10504, USA The New York Botanical Garden, Bronx, NY, 10458, USA
W. W. Thomas
Affiliation:
The New York Botanical Garden, Bronx, NY, 10458, USA
F. A. Gaiotto
Affiliation:
Departamento de Ciências Biológicas – Universidade Estadual de Santa Cruz (UESC), Ilhéus, BA, 45662–900, Brazil
J. D. Lewis
Affiliation:
Louis Calder Center – Biological Field Station, and Department of Biological Sciences, Fordham University, Armonk, NY, 10504, USA
*
1Corresponding author. Email: [email protected]

Abstract:

Habitat fragmentation may lead to spatial genetic structuring of plant populations, but the magnitude of this effect differs among species. In this study, the effects of fragmentation on spatial genetic structure of Manilkara maxima, an ecologically important tree species endemic to the Atlantic forest of southern Bahia, Brazil, were examined. To address this issue, 222 individuals were sampled across two large-forest sites (200 and 400 ha) and one site comprising eight small fragments (5, 10 and 25 ha) roughly 35 y old. Five microsatellite loci were used. In general, M. maxima exhibited limited genetic structuring within and across the sites examined. At the landscape scale, genetic structure was not shaped by isolation by distance. Within individual sites, weak to moderate genetic structure was observed for both adults and saplings, which represented pre- and post-fragmentation, respectively. Sapling genetic structure did not clearly vary among the study sites, suggesting fragmentation has not affected spatial genetic structure. High levels of migration were observed, which would help maintain genetic connectivity. Taken together, these results suggest M. maxima, a long-lived tree that naturally occurs in low densities, may have limited spatial genetic structuring both within and across forest patches.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

AGUILAR, R., ASHWORTH, L., GALETTO, L. & AIZEN, M. A. 2006. Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecology Letters 9:968980.CrossRefGoogle ScholarPubMed
AGUINAGALDE, I., HAMPE, A., MOHANTY, A., MARTÍN, J. P., DUMINIL, J. & PETIT, R. J. 2005. Effects of life-history traits and species distribution on genetic structure at maternally inherited markers in European trees and shrubs. Journal of Biogeography 32:329339.CrossRefGoogle Scholar
AULER, N. M. F., REIS, M. S. D., GUERRA, M. P. & NODARI, R. O. 2002. The genetics and conservation of Araucaria angustifolia: I. Genetic structure and diversity of natural populations by means of non-adaptive variation in the state of Santa Catarina, Brazil. Genetics and Molecular Biology 25:329338.CrossRefGoogle Scholar
AZEVEDO, V., VINSON, C. & CIAMPI, A. 2005. Twelve microsatellite loci in Manilkara huberi (Ducke) Standl. (Sapotaceae), an Amazonian timber species. Molecular Ecology Notes 5:1315.CrossRefGoogle Scholar
AZEVEDO, V. C. R., KANASHIRO, M., CIAMPI, A. Y. & GRATTAPAGLIA, D. 2007. Genetic structure and mating system of Manilkara huberi (Ducke) A. Chev., a heavily logged Amazonian timber species. Journal of Heredity 98:646654.CrossRefGoogle Scholar
BACLES, C. F. & JUMP, A. S. 2011. Taking a tree's perspective on forest fragmentation genetics. Trends in Plant Science 16:1318.CrossRefGoogle ScholarPubMed
BARTON, N. & SLATKIN, M. 1986. A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Heredity 56:409415.CrossRefGoogle Scholar
BENARD, M. F. & MCCAULEY, S. J. 2008. Integrating across life-history stages: consequences of natal habitat effects on dispersal. American Naturalist 171:553567.CrossRefGoogle ScholarPubMed
BONNET, E. & VAN DE PEER, Y. 2002. zt: a software tool for simple and partial Mantel tests. Journal of Statistical Software 7:112.CrossRefGoogle Scholar
BROOKFIELD, J. 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Molecular Ecology 5:453455.CrossRefGoogle ScholarPubMed
CHASE, M. W. & HILLS, H. H. 1991. Silica gel: an ideal material for field preservation of leaf samples for DNA studies. Taxon 40:215220.CrossRefGoogle Scholar
CHOO, J., JUENGER, T. & SIMPSON, B. 2012. Consequences of frugivore-mediated seed dispersal for the spatial and genetic structures of a neotropical palm. Molecular Ecology 21:10191031.CrossRefGoogle ScholarPubMed
CHUNG, M. Y., EPPERSON, B. K. & CHUNG, M. 2003. Genetic structure of age classes in Camellia japonica (Theaceae). Evolution 57:6273.CrossRefGoogle ScholarPubMed
COLPAERT, N., CAVERS, S., BANDOU, E., CARON, H., GHEYSEN, G. & LOWE, A. J. 2005. Sampling tissue for DNA analysis of trees: trunk cambium as an alternative to canopy leaves. Silvae Genetica 54:265269.CrossRefGoogle Scholar
CONNELL, J. H. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forests. Pp. 298310 in den Boer, P. J. & Gradwell, G. R. (eds.). Dynamics of populations. Pudoc, Wageningen.Google Scholar
DUMINIL, J., FINESCHI, S., HAMPE, A., JORDANO, P., SALVINI, D., VENDRAMIN, G. G. & PETIT, R. J. 2007. Can population genetic structure be predicted from life-history traits? American Naturalist 169:662672.CrossRefGoogle ScholarPubMed
EXCOFFIER, L. & SLATKIN, M. 1998. Incorporating genotypes of relatives into a test of linkage disequilibrium. American Journal of Human Genetics 62:171180.CrossRefGoogle ScholarPubMed
EXCOFFIER, L., LAVAL, G. & SCHNEIDER, S. 2005. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1:4750.Google Scholar
FAO. 2012. State of the World's forests. Food and Agriculture Organization of the United Nations, Rome.Google Scholar
FUCHS, E. J. & HAMRICK, J. L. 2010. Spatial genetic structure within size classes of the endangered tropical tree Guaiacum sanctum (Zygophyllaceae). American Journal of Botany 97:12001207.CrossRefGoogle ScholarPubMed
GANZHORN, S., PEREZ-SWEENEY, B., THOMAS, W., GAIOTTO, F. & LEWIS, J. 2015. Effects of fragmentation on density and population genetics of a threatened tree species in a biodiversity hotspot. Endangered Species Research 26:189199.CrossRefGoogle Scholar
GUO, S. W. & THOMPSON, E. A. 1992. Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361372.CrossRefGoogle ScholarPubMed
HAMRICK, J. L. & NASON, J. D. 1996. Consequences of dispersal in plants. Pp. 203236 in Rhodes, O. E., Chesser, R. K. & Smith, M. H. (eds.). Population dynamics in ecological space and time. University of Chicago Press, Chicago.Google Scholar
HAMRICK, J. L., GODT, M. J. W. & SHERMAN-BROYLES, S. L. 1992. Factors influencing levels of genetic diversity in woody plant species. New Forests 6:95124.CrossRefGoogle Scholar
HAMRICK, J. L., MURAWSKI, D. A. & NASON, J. D. 1993. The influence of dispersal mechanisms on genetic structure of tropical tree populations. Vegetatio 107/108:281297.CrossRefGoogle Scholar
HARDY, O. J. & VEKEMANS, X. 2002. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2:618620.CrossRefGoogle Scholar
HARDY, O. J., MAGGIA, L., BANDOU, E., BREYNE, P., CARON, H., CHEVALLIER, M.-H., DOLIGEZ, A., DUTECH, C., KREMER, A., LATOUCHE-HALLÉ, C., TROISPOUX, V., VERON, V. & DEGEN, B. 2006. Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Molecular Ecology 15:559571.CrossRefGoogle ScholarPubMed
HEUERTZ, M., VEKEMANS, X., HAUSMAN, J. F., PALADA, M. & HARDY, O. J. 2003. Estimating seed vs. pollen dispersal from spatial genetic structure in the common ash. Molecular Ecology 12:24832495.CrossRefGoogle ScholarPubMed
HUBBELL, S. 2004. Two decades of research on the BCI forest dynamics plot. Pp. 830 in Losos, E. C. & Leigh, E. G. (eds.). Tropical forest diversity and dynamism: findings from a large-scale plot network. University of Chicago Press, Chicago.Google Scholar
ISMAIL, S., GHAZOUL, J., RAVIKANTH, G., KUSHALAPPA, C. & KETTLE, C. 2012. Does long-distance pollen dispersal preclude inbreeding in tropical trees? Fragmentation genetics of Dysoxylum malabaricum in an agro-forest landscape. Molecular Ecology 21:54845496.CrossRefGoogle Scholar
JANZEN, D. H. 1970. Herbivores and the number of tree species in tropical forests. American Naturalist 104:501528.CrossRefGoogle Scholar
JARDIM, J. G. 2003. Uma caracterização parcial da vegetação na região Sul da Bahia, Brasil. In Prado, P. I., Landau, E. C., Moura, R. T., Pinto, L. P. S., Fonseca, G. A. B. & Alger, K. (eds.). Corredor de Biodiversidade de Mata Atlântica do Sul da Bahia, Brasil. Instituto de Estudos Sócio-Ambientais do Sul da Bahia e Conservation International do Brasil. CD-ROM.Google Scholar
KALISZ, S., NASON, J. D., HANZAWA, F. M. & TONSOR, S. J. 2001. Spatial population genetic structure in Trillium grandiflorum: the roles of dispersal, mating, history, and selection. Evolution 55:15601568.Google ScholarPubMed
KRAMER, A. T., ISON, J. L., ASHLEY, M. V. & HOWE, H. F. 2008. The paradox of forest fragmentation genetics. Conservation Biology 22:878885.CrossRefGoogle ScholarPubMed
LAN, G. Y., ZHU, H., CAO, M., HU, Y., WANG, H., DENG, X., ZHOU, S., CUI, J., HUANG, J., HE, Y., LIU, L., XU, H. & SONG, J. 2009. Spatial dispersion patterns of trees in a tropical rainforest in Xishuangbanna, southwest China. Ecological Research 24:11171124.CrossRefGoogle Scholar
LANDAU, E. C., HIRSCH, A. & MUSINSKY, J. 2008. Vegetation cover and land use in the Atlantic coastal forest of southern Bahia, Brazil, based on satellite imagery: a comparison among municipalities. Pp. 221244 in Thomas, W. W. (ed.). The Atlantic coastal forest of northeastern Brazil. The New York Botanical Garden Press, New York.Google Scholar
LEVENE, H. 1949. On a matching problem arising in genetics. Annals of Mathematical Statistics 20:9194.CrossRefGoogle Scholar
LOISELLE, B. A., SORK, V. L., NASON, J. & GRAHAM, C. 1995. Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). American Journal of Botany 82:14201425.CrossRefGoogle Scholar
MANTEL, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Research 27:209220.Google Scholar
MENDONÇA, J. R., CARVALHO, A. M. D., SILVA, L. A. M. & THOMAS, W. W. 1994. 45 anos de desmatamento no sul da Bahia, remanescentes da Mata Atlântica – 1945, 1960, 1974, 1990. Projecto Mata Atlântica Nordeste, Centro de Pesquisas do Cacau, Ilhéus.Google Scholar
MORAES, R. C. S., VIVAS, C. V., OLIVEIRA, F. A., MENEZES, I. P. P., BERG, C. V. D. & GAIOTTO, F. A. 2013. Microsatellite markers for an endemic Atlantic forest tree, Manilkara multifida (Sapotaceae). AoB Plants 5: plt006.CrossRefGoogle ScholarPubMed
MOREIRA, P. A., FERNANDES, G. W. & COLLEVATTI, R. G. 2009. Fragmentation and spatial genetic structure in Tabebuia ochracea (Bignoniaceae) a seasonally dry neotropical tree. Forest Ecology and Management 258:26902695.CrossRefGoogle Scholar
MORI, S. A. & SILVA, L. A. M. 1979. The herbarium of the “Centro de Pesquisas do Cacau” at Itabuna, Brazil. Brittonia 31:177196.CrossRefGoogle Scholar
MORI, S. A., BOOM, B. M., CARVALHO, A. M. D. & SANTOS, T. S. D. 1983. Southern Bahian moist forests. Botanical Review 49:155232.CrossRefGoogle Scholar
MYERS, N., MITTERMEIER, R. A., MITTERMEIER, C. G., DA FONSECA, G. A. B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853856.CrossRefGoogle ScholarPubMed
PEAKALL, R. & SMOUSE, P. E. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6:288295.CrossRefGoogle Scholar
PENNINGTON, T. D. 1990. Sapotaceae. Monograph 52. Flora Neotropica. New York Botanical Garden Press, New York.Google Scholar
PENNINGTON, T. D. 2004. Sapotaceae. Pp. 390421 in Kubitzki, K. (ed.). The families and genera of vascular plants, volume IV, flowering plants, dicotyledons: Celastrales, Oxidales, Rosales, Cornales, Ericales. Springer-Verlag, Berlin.Google Scholar
RAYMOND, M. & ROUSSET, F. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86:248249.CrossRefGoogle Scholar
RIBEIRO, M. C., METZGER, J. P., MARTENSEN, A. C., PONZONI, F. J. & HIROTA, M. M. 2009. The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142:11411153.CrossRefGoogle Scholar
ROCHA, C. F. A. 1976. Diagnostico socioeconômico da região cacaueira: Volume 5. Recursos hídricos. Comissão Executiva do Plano da Lavoura Cacaueira and the Instituto Interamericano de Ciências Agricolas-OEA, Ilhéus.Google Scholar
ROUSSET, F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:12191228.CrossRefGoogle ScholarPubMed
ROUSSET, F. 2008. genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources 8:103106.CrossRefGoogle ScholarPubMed
SEBBENN, A., CARVALHO, A., FREITAS, M., MORAES, S., GAINO, A., DA SILVA, J., JOLIVET, C. & MORAES, M. 2011. Low levels of realized seed and pollen gene flow and strong spatial genetic structure in a small, isolated and fragmented population of the tropical tree Copaifera langsdorffii Desf. Heredity 106:134145.CrossRefGoogle Scholar
SEOANE, C. E. S., KAGEYAMA, P. Y. & SEBBENN, A. M. 2000. Forest fragmentation in population genetic structure of Esenbeckia leiocarpa Engl. (Guarantã). Scientia Forestalis 57:123139.Google Scholar
SEOANE, C. E. S., KAGEYAMA, P. Y., RIBEIRO, A., MATIAS, R., REIS, M., BAWA, K. & SEBBENN, A. M. 2005. Efeitos da fragmentação florestal sobre a imigração de sementes ea estrutura genética temporal de populações de Euterpe edulis Mart. Revista do Instituto Florestal 17:2343.CrossRefGoogle Scholar
SILVA, E. F. D., 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.Google Scholar
SMOUSE, P. E., PEAKALL, R. & GONZALES, E. 2008. A heterogeneity test for fine-scale genetic structure. Molecular Ecology 17:33893400.CrossRefGoogle ScholarPubMed
THOMAS, W. W. & BARBOSA, M. R. D. V. 2008. Natural vegetation types in the Atlantic coastal forest of northeast Brazil. Pp. 620 in Thomas, W. W. (ed.). The Atlantic coastal forest of northeastern Brazil. The New York Botanical Garden Press, New York.Google Scholar
TONSOR, S. J., KALISZ, S., FISHER, J. & HOLTSFORD, T. P. 1993. A life-history based study of population genetic structure: seed bank to adults in Plantago lanceolata. Evolution 47:833843.Google ScholarPubMed
TURNER, I. M. 1996. Species loss in fragments of tropical rain forest: a review of the evidence. Journal of Applied Ecology 33:200209.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 4:535538.CrossRefGoogle Scholar
VAN OOSTERHOUT, C., WEETMAN, D. & HUTCHINSON, W. 2006. Estimation and adjustment of microsatellite null alleles in nonequilibrium populations. Molecular Ecology Notes 6:255256.CrossRefGoogle Scholar
VEKEMANS, X. & HARDY, O. J. 2004. New insights from fine-scale spatial genetic structure analyses in plant populations. Molecular Ecology 13:921935.CrossRefGoogle ScholarPubMed
VRANCKX, G., 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.CrossRefGoogle ScholarPubMed
WELDEN, C. W., HEWETT, S. W., HUBBELL, S. P. & FOSTER, R. B. 1991. Sapling survival, growth, and recruitment: relationship to canopy height in a neotropical forest. Ecology 72:3550.CrossRefGoogle Scholar
WRIGHT, S. 1940. Breeding structure of populations in relation to speciation. American Naturalist 74:232248.CrossRefGoogle Scholar
ZHOU, H.-P. & CHEN, J. 2010. Spatial genetic structure in an understorey dioecious fig species: the roles of seed rain, seed and pollen-mediated gene flow, and local selection. Journal of Ecology 98:11681177.CrossRefGoogle Scholar