Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-10T13:44:06.623Z Has data issue: false hasContentIssue false
  • English
  • Français

Gene flow and fine-scale spatial genetic structure in Cabralea canjerana (Meliaceae), a common tree species from the Brazilian Atlantic forest

Published online by Cambridge University Press:  15 March 2016

Arthur Tavares de Oliveira Melo  and
Edivani Villaron Franceschinelli
Arthur Tavares de Oliveira Melo*
Affiliation:
Plant Genetics and Breeding College of Agronomy, Federal University of Goiás, Campus II, CP 131, Goiânia, GO, 74690–900, Brazil
Edivani Villaron Franceschinelli
Affiliation:
Botany Department, Biological Sciences Institute, Federal University of Goiás, Goiânia, GO, Brazil
*
1Corresponding author. Email: arthurmelobio@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract:

The Atlantic forest is the biome most severely affected by deforestation in Brazil. Cabralea canjerana spp. canjerana is a dioecious tree species with widespread distribution in the Neotropical region. This species is considered a model to ascertain population ecology parameters for endangered plant species from the Atlantic forest. Fine-scale spatial genetic structure and pollen-mediated gene flow are crucial information in landscape genetics and evolutionary ecology. A total of 192 adults and 121 offspring were sampled in seven C. canjerana populations in the Southern Minas Gerais State, Brazil, to assess whether pollen-mediated gene flow is able to prevent spatial genetic structure within and among Atlantic forest fragments. Several molecular ecology parameters were estimated using microsatellite loci. High levels of genetic diversity (HE = 0.732) and moderate population structure (θ = 0.133) were recorded. No significant association between kinship and spatial distance amongst individuals within each population (Sp = 0.000109) was detected. Current pollen-mediated gene flow occurs mainly within forest fragments, probably due to short-distance flights of the pollinator of C. canjerana, and also the forest fragmentation may have restricted flight distance. The high levels of genetic differentiation found amongst the seven sites sampled demonstrated how habitat fragmentation affects the gene flow process in natural areas.

Keywords

Brazilfine-scale SGShabitat fragmentationmolecular ecologypollen dispersal
Type
Research Article
Information
Journal of Tropical Ecology , Volume 32 , Issue 2 , March 2016 , pp. 135 - 145
Copyright
Copyright © Cambridge University Press 2016 

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

AGUARI. 2001. Ações sociais para a preservação de fragmentos florestais na bacia do Rio Camanducaia. PROBIO/MMA, Camanducaia. 40 pp.Google Scholar
ALDRICH, P. R. & HAMRICK, J. L. 1998. Reproductive dominance of pasture trees in a fragmented tropical forest mosaic. Science 281:103–105.CrossRefGoogle Scholar
AULER, N. M. F., REIS, M. S., 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 25:329–338.Google Scholar
AUSTERLITZ, F. & SMOUSE, P. 2001. Two-generation analysis of pollen flow across a landscape. II. Relation between ФFT, pollen dispersal and inter female distance. Genetics 157:851–857.Google ScholarPubMed
BALDAULF, C., CIAMPI-GUILLARDI, M., AGUIRRA, T. J., CORRÊA, C. E., SANTOS, F. A. M., SOUZA, A. P. & SEBBENN, A. M. 2014. Genetic diversity, spatial genetic structure and realised seed and pollen dispersal of Himatanthus drasticus (Apocynaceae) in the Brazilian savanna. Conservation Genetics 15:1073–1083.Google Scholar
BARREIROS, H. D. S. & SOUZA, D. S. E. 1986. Notas geográficas e taxonômicas sobre Cabralea canjerana (Vell.) Mart. no Brasil (Meliaceae). Revista Brasileira de Biologia 46:17–26.Google Scholar
BITTENCOURT, J. V. M. & SEBBENN, A. M. 2008. Pollen movement within a continuous forest of wind-pollinated Araucaria angustifolia, inferred from paternity and TwoGener analysis. Conservation Genetics 9:855–868.CrossRefGoogle Scholar
CARDINALE, B. J., DUFFY, J. E., GONZALEZ, A. HOOPER, U., D., PERRINGS, C., VENAIL, P., NARWANI, A., MACE, G. M., TILMAN, D., WARDLE, D. A., KINZIG, A. P., DAILY, G. C., LOREAU, M., GRACE, J. B., LARIGAUDERIE, A., SRIVASTAVA, D. S. & NAEEM, S. 2012. Biodiversity loss and its impact on humanity. Nature Review 486:59–67.Google Scholar
CARMO, R. M. 2005. Biologia reprodutiva de Cabralea canjerana subsp. canjerana em fragmentos de Mata Atlântica do sul do estado Minas Gerais. Ph.D thesis, Universidade Federal de Minas Gerais, Brasil.Google Scholar
CLOUTIER, D., HARDY, O. J., CARON, H., CIAMPI, A. Y., DEGEN, B., KANASHIRO, M. & SCHOEN, D. J. 2007. Low inbreeding and high pollen dispersal distances in populations of two Amazonian Forest tree species. Biotropica 39:406–415.CrossRefGoogle Scholar
COCKERHAM, C. C. 1969. Variance of gene frequencies. Evolution 23:72–84.Google Scholar
COLOMBO, A. F. & JOLY, C. A. 2010. Brazilian Atlantic Forest lato sensu: the most ancient Brazilian forest, and a biodiversity hotspot, is highly threatened by climate change. Brazilian Journal of Biology 70:697–708.Google Scholar
CONTE, R., REIS, M. S., MANTOVANI, A. & VENCOVSKY, R. 2008. Genetic structure and mating system of Euterpe edulis Mart. populations: a comparative analysis using microsatellite and allozyme markers. Journal of Heredity 99:476–482.Google Scholar
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.Google Scholar
CORDEIRO, N. J. & HOWE, H. F. 2003. Forest fragmentation severs mutualism between seed dispersers and an endemic African tree. Proceedings of the National Academy of Sciences USA 100:14052–14054.Google Scholar
DICK, C. W., ETCHELECU, G. & AUSTERLITZ, F. 2003. Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Molecular Ecology 12:753–764.Google Scholar
DYER, R. J. & SORK, L. J. 2001. Pollen pool heterogeneity in shortleaf pine, Pinus schinata Mill. Molecular Ecology 10:859–866.Google Scholar
DYER, R. J., WESTFALL, R. D., SORK, V. L. & SMOUSE, P. E. 2004. Two-generation analysis of pollen flow across a landscape V: a stepwise approach for extracting factors contributing to pollen structure. Heredity 92:204–211.Google Scholar
FRANCESCHINELLI, E. V., VASCONCELOS, G. M. P., LANDAU, E. C., ONO, K. Y. & SANTOS, F. A. M. 2007. The genetic diversity of Myrciaria floribunda (Myrtaceae) in Atlantic forest fragments of different size. Journal of Tropical Ecology 23:361–367.Google Scholar
FRANCESCHINELLI, E. V., CARMO, R. M., SILVA-NETO, C. M. & MESQUITA-NETO, J. N. 2015a. Functional dioecy and moth pollination in Cabralea canjerana subsp. canjerana (Meliaceae). Darwiniana 3:96–107.Google Scholar
FRANCESCHINELLI, E. V., CARMO, R. M., SILVA-NETO, C. M., GONÇALVES, B. B. & BERGAMINI, L. 2015b. Reproductive success of Cabralea canjerana (Meliaceae) in Atlantic forest fragments, Brazil. Revista de Biologia Tropical 63:515–524.Google Scholar
FREELAND, J. R., BISS, P. & SILVERTOWN, J. 2011. Contrasting patterns of pollen and speed flow influence the spatial genetic structure of sweet vernal grass (Anthoxanthum odoratum) populations. Journal of Heredity 103:28–35.Google Scholar
FORTI, G., TAMBARUSSI, E. V., KAGEYAMA, P. Y., MORENO, M. A., FERRAZ, E. M., IBAÑES, B., VENCOVSKY, R., MORI, G. M. & SEBBENN, A. M. 2014. Low genetic diversity and intrapopulation spatial genetic structure of the Atlantic Forest tree, Esenbeckia leiocarpa Engl. (Rutaceae). Annals of Forest Research 57:165–174.Google Scholar
GARCIA, C., JORDANO, P. & GODOY, J. A. 2007. Contemporary pollen and seed dispersal in a Prunus mahaleb population: patterns in distance and direction. Molecular Ecology 16:1947–1955.Google Scholar
GHAZOUL, J. 2005. Pollen and seed dispersal among dispersed plants. Biological Review 80:413–443.Google Scholar
GOODMAN, S. J. 1997. Rst-Calc: a collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and a determining their significance. Molecular Ecology 6:881–885.Google Scholar
GUILLOT, G., ESTOUP, A., MORTIER, F. & COSSON, J. F. 2005a. A spatial statistical model for landscape genetics. Genetics 170:1261–1280.CrossRefGoogle ScholarPubMed
GUILLOT, G., MORTIER, F. & ESTOUP, A. 2005b. GENELAND: a computer package for landscape genetics. Molecular Ecology Notes 5:712–715.CrossRefGoogle Scholar
HAMILTON, M. B. & MILLER, J. R. 2002. Comparing relative rates of pollen and seed gene flow in the island model using nuclear and organelle measure of population structure. Genetics 162:1897–1909.Google Scholar
HARDY, O. J. & VEKEMANS, X. 2002. SPAGeDi: a versatile computer program to analyses spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2:618–620.CrossRefGoogle Scholar
HARDY, O. J., GONZALEZ-MARTINEZ, S. C., COLAS, B., FREVILLE, H., MIGNOT, A. & OLIVERI, I. 2004. Fine-scale genetic structure and gene dispersal in Centaurea corymbosa (Asteraceae). II. Correlated paternity within and among sibships. Genetics 168:1601–1614.Google Scholar
HARDY, O. J., MAGGIA, L., BANDOU, E., BREYNE, P., CARON, H., CHEVALLIER, M. H., DOLIGNEZ, A., DUTECH, C., KREMER, A., HALLÉ, C. L., TROISPOUX, V., VERON, V. & DEGEN, B. 2006. Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Molecular Ecology 15:559–571.Google Scholar
HEDRICK, P. W. 1999. Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318.Google Scholar
HOLSINGER, K. E. & WEIR, B. S. 2009. Genetics in geographically structured populations: defining, estimating and interpreting FST. Nature Review Genetics 10: 639–650.Google 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 82:1420–1425.Google Scholar
LOVELESS, M. D. & HAMRICK, J. L. 1984. Ecological determinants of genetic structure in plant populations. Annual Review of Ecological System 15:65–95.Google 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
LUIKART, G. & CORNUET, J. M. 1998. Empirical evaluation of a testing for identifying recently bottleneck populations from allele frequency data. Conservation Biology 12:228–237.Google Scholar
MELO, A. T. O., COELHO, A. S. G., PEREIRA, M. F., BLANCO, A. J. V. & FRANCESCHINELLI, E. V. 2014. High genetic diversity and strong spatial genetic structure in Cabralea canjerana (Vell.) Mart. (Meliaceae): implications to Brazilian Atlantic Forest tree conservation. Natureza & Conservação 12:129–133.Google Scholar
MELO, A. T. O., COELHO, A. S. G., PEREIRA, M. F., BLANCO, A. J. V. & FRANCESCHINELLI, E. V. 2015. Genética da conservação de Cabralea canjerana (Vell.) Mart. (Meliaceae) em fragmentos florestais de Mata Atlântica na APA Fernão Dias. Revista Árvore 39:365–374.Google Scholar
NEI, M. 1973. Analysis of gene diversity in subdivided population. Proceedings of the National Academy of Sciences USA 70:3321–3323.Google Scholar
PENNINGTON, T. D., STYLES, B. D. & TAYLOR, D. A. H. 1981. Meliaceae. Flora Neotropica 28:235–244.Google Scholar
PEREIRA, M. F., BANDEIRA, L. F., BLANCO, A. J. V., COELHO, A. S. G, CIAMPI, A. Y. & FRANCESCHINELLI, E. V. 2011. Isolation and characterization of microsatellite locis in Cabralea canjerana (Meliaceae). American Journal of Botany 98:1–3.Google Scholar
PIZO, M. A. & OLIVEIRA, P. S. 1998. Interaction between ants and seeds of a nonmyrmecochorous neotropical tree, Cabralea canjerana (Meliaceae), in the Atlantic forest of southeast Brazil. American Journal of Botany 85:669–674.Google 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 142:1141–1153.Google Scholar
RICKETTS, T. H. 2001. The matrix matters: effective isolation in fragmented landscapes. American Naturalist 158:87–99.Google Scholar
RITLAND, K. 2002. Extensions of models for the estimation of mating systems using n independent loci. Heredity 88:221–228.Google Scholar
ROBLEDO-ARNUNCIO, J. J. & GILL, L. 2005. Patterns of pollen dispersal in a small population of Pinus sylvestris L. revealed by total exclusion paternity analysis. Heredity 94:13–22.Google Scholar
ROBLEDO-ARNUNCIO, J. J., AUSTERLITZ, F. & SMOUSE, P. E. 2007. POLDISP: a software package for indirect estimation of contemporary pollen dispersal. Molecular Ecology Notes 7:763–766.Google Scholar
ROSAS, F. QUESADA, M., LOBO, A., J. & SORK, V. L. 2011. Effects of habitat fragmentation on pollen flow and genetic diversity of the endangered tropical tree Swietenia humilis (Meliaceae). Biological Conservation 144:3082–3088.Google Scholar
SALGUEIRO, F., FELIX, D., CALDAS, J. F., PINHEIRO, M. M. & MARGIS, R. 2004. Even population differentiation for maternal and biparental gene markers in Eugenia uniflora, a widely distributed species from the Brazilian coastal Atlantic rain forest. Diversity and Distributions 10:201–210.Google Scholar
SEBBENN, A. M., CARVALHO, A. C. M., FREITAS, M. L. M., MORAES, S. M. B., GAINO, A. P. S. C., DA, SILVA, M., J., JOLIVET, C. & MORAES, M. L. T. 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 106:134–145.Google Scholar
SEOANE, C. E. S., KAGEYAMA, P. Y. & SEBBEN, A. M. 2000. Forest fragmentation effects in population genetic structure of Esenbeckia leiocarpa Engl. (Guarantã). Scientia Forestalis 57:123–139.Google Scholar
SLOTTA, T. A. B., BRADY, L. & CHAO, S. 2008. High throughput tissue preparation for large-scale genotyping experiments. Molecular Ecology Resource 8:83–87.CrossRefGoogle ScholarPubMed
SMOUSE, P. E. & SORK, V. L. 2004. Measuring pollen flow in forest trees: an exposition of alternative approaches. Forest Ecology and Management 197:21–38.Google Scholar
SOKAL, R. R. 1979. Testing statistical significance of geographic variation patterns. Systematic Zoology 28:227–232.Google Scholar
STACY, E. A., HAMRICK, J. L., NASON, J. D., HUBBELL, S. P., FOSTER, R. B. & CONDIT, R. 1996. Pollen dispersal in low-density populations of three Neotropical tree species. American Naturalist 148:275–298.Google Scholar
TARAZI, R., MANTOVANI, A. & REIS, M. S. 2010. Fine-scale spatial genetic structure and allozymic diversity in natural populations of Ocotea catharinensis Mez (Lauraceae). Conservation Genetics 11:965–976.Google Scholar
VEKEMANS, X. & HARDY, O. J. 2004. New insights from fine-scale spatial genetic structure analyses in plant populations. Molecular Ecology 13:921–935.Google Scholar
VILARINHO, E. C., FERNANDES, O. A., HUNT, T. E. & CAIXETA, D. F. 2011. Movement of Spodoptera frugiperda adults (Lepidoptera: Noctuidae) in maize in Brazil. Florida Entomologist 94:480–488.Google Scholar
YOUNG, A., BOYLE, T. & BROWN, T. 2001. The population genetic consequences of habitat fragmentation for plants. Trends in Ecology and Evolution 11:413–418.Google Scholar
WANG, R., COMPTON, S. G. & CHEN, X. Y. 2011. Fragmentation can increase spatial genetic structure without decreasing pollen-mediated gene flow in a wind-pollinated tree. Molecular Ecology 20:4421–4432.Google Scholar
WEIR, B. S. & COCKERHAM, C. C. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370.Google Scholar
WHITE, G. M., BOSHIER, D. H. & POWELL, W. 2002. Increased pollen flow counteracts fragmentation in tropical dry forest: an example from Swietenia humilis Zuccarini. Proceedings of the National Academy of Sciences USA 99:2038–2042.Google Scholar