How Do Gap Dynamics And Colonization Of A Human Disturbed Area Affect Genetic Diversity And Structure Of A Pioneer Tropical Tree Species?

Pioneer tree species exhibit life-cycle characteristics and population structures that are mainly affected by natural or human disturbances. In primary forests, demographic dynamics of pioneer species may resemble those defined for a metapopulation. In early successional forests, the patterns of establishment, survival and reproduction are mainly determined by microclimate and biota modifications of the site after the human disturbance. The aim of this study was to investigate how the ecological processes and the population genetic factors associated with disturbances can affect the genetic diversity and structure of populations of a pioneer tree species: Croton floribundus Spreng. (Euphorbiaceae). Nuclear and chloroplast microsatellite markers were examined in plants of two size classes sampled in four gaps of primary forest and four sub-areas of early successional forest. Despite presenting similar genetic diversity levels, the genetic diversity was distributed differently between forests. The combined effects of seed dispersal and colonizations (and extinctions) were determinants of the fine-scale genetic structure of C. floribundus. The main finding was that human disturbances seem to boost the influence of founder effects in populations of a species with limited seed dispersal. Results suggested that gene flow by pollen was responsible for maintaining the genetic diversity within populations of C. floribundus in both forests, but in the early successional forest, gene flow by seeds was equally important. We conclude that gap dynamics, colonization, and pollen and seed dispersal affect the genetic diversity and structure of the pioneer species depending mainly on the number of colonizers, the number of source populations, the gene flow rates, and the level of human disturbance.3443852Alvarez-Buylla, E.R., Density dependence and patch dynamics in tropical rain forests: matrix models and applications to a tree species (1994) Am. Nat., 143, pp. 155-191Alvarez-Buylla, E.R., Garay, A.A., Population genetic structure of Cecropia obtusifolia, a tropical pioneer tree species (1994) Evolution, 48, pp. 437-453Alvarez-Buylla, E.R., Chaos, A., Piñero, D., Garay, A.A., Demographic genetics of a pioneer tropical tree species: patch dynamics, seed dispersal and seed banks (1996) Evolution, 50, pp. 1155-1166Ashley, M.V., Plant parentage, pollination, and dispersal: how DNA microsatellites have altered the landscape (2010) Crit. Rev. Plant Sci., 29 (3), pp. 148-161Born, C., Hardy, O.J., Chevallier, M.H., Ossari, S., Attéké, C., Wickings, E.J., Hossaert-Mckey, M., Small-scale spatial genetic structure in the Central African rainforest tree species Aucoumea klaineana: a stepwise approach to infer the impact of limited gene dispersal, population history and habitat fragmentation (2008) Mol. Ecol., 17, pp. 2041-2050Born, C., Kjellberg, F., Chevallier, M.H., Vignes, H., Dikangadissi, J.T., Sanguie, J., Wickings, E.J., Hossaert-McKey, M., Colonization processes and the maintenance of genetic diversity: insights from a pioneer rainforest tree, Aucoumea klaineana (2008) Proc. R. Soc. Bot., 275, pp. 2171-2179Brokaw, N.V.L., Gap-phase regeneration of three pioneer tree species in a tropical forest (1987) J. Ecol., 75, pp. 9-19Cavallari, M.M., Gimenes, M.A., Billot, C., Torres, R.B., Zucchi, M.I., Cavalheiro, A.J., Bouvet, J., Population genetic relationships between Casearia sylvestris (Salicaceae) varieties occurring sympatrically and allopatrically in different ecosystems in south-east Brazil (2010) Ann. Bot., 106, pp. 627-636Cavers, S., Navarro, C., Hopkins, R., Ennos, R.A., Lowe, A.J., Regional and population-scale influences on genetic diversity partitioning within costarican populations of the pioneer tree Vochysia ferruginea Mart (2005) Silvae Genet., 54, pp. 258-264Clark, L.V., Jasieniuk, M., POLYSAT: an R package for polyploid microsatellite analysis (2011) Mol. Ecol. Res., 11 (3), pp. 562-566Danciguer, L., Aspectos da regeneração de duas espécies arbóreas em um fragmento florestal do sudeste brasileiro (1996), MSc Thesis, University of Campinas, BrazilDavies, S.J., Cavers, S., Finegan, B., Navarro, C., Lowe, A.J., Genetic consequences of multigenerational and landscape colonisation bottlenecks for a neotropical forest pioneer tree, Vochysia ferruginea (2010) Tropical Plant Biol., 3, pp. 14-27Davies, S.J., Cavers, S., Finegan, B., White, A., Breed, M.F., Lowe, A.J., Pollen flow in fragmented landscapes maintains genetic diversity following stand-replacing disturbance in a neotropical pioneer tree (2013), Vochysia ferruginea Mart. Heredity, in pressDegen, B., SGS: Spatial Genetic Software (2000), http://software.bfh-inst2.de, Computer program and user's manual (04.09.14)Degen, B., Petit, R., Kremer, A., SGS - Spatial Genetic Software: a computer program for analysis of spatial genetic and phenotypic structures of individuals and populations (2001) J. Hered., 92, pp. 447-448Degen, B., Bandou, E., Caron, H., Limited pollen dispersal and biparental inbreeding in Symphonia globulifera in French Guiana (2004) Heredity, 93, pp. 585-591Doyle, J.J., Doyle, J.L., Isolation of plant DNA from fresh tissue (1990) Focus, 12, pp. 13-15Dufresne, F., Stift, M., Vergilino, R., Mable, B.K., Recent progress and challenges in population genetics of polyploid organisms: an overview of current state-of-the-art molecular and statistical tools (2014) Mol. Ecol., 23, pp. 40-69Earl, D.A., vonHoldt, B.M., STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method (2012) Conserv. Genet. Res., 4, pp. 359-361Ellstrand, N.C., Elam, D.R., Population genetic consequences of small population sizes: implication for plant conservation (1993) Annu. Rev. Ecol. Syst., 24, pp. 217-242Evanno, G., Regnaut, S., Goudet, J., Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study (2005) Mol. Ecol., 14, pp. 2611-2620Excoffier, L., Lischer, H.E.L., Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows (2010) Mol. Ecol. Res., 10, pp. 564-567Excoffier, L., Smouse, P.E., Quattro, J.M., Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data (1992) Genetics, 131, pp. 479-491Falush, D., Stephens, M., Pritchard, J.K., Inference of population structure using multilocus genotype data: dominant markers and null alleles (2007) Mol. Ecol. Notes, 7, pp. 574-578Fields, P.D., McCauley, D.E., McAssey, E.V., Taylor, D.R., Patterns of cyto-nuclear linkage disequilibrium in Silene latifolia: genomic heterogeneity and temporal stability (2014) Heredity, 112, pp. 99-104Franceschinelli, E.V., Kesseli, R., Population structure and gene flow of the Brazilian shrub Helicteres brevispira (1999) Heredity, 82, pp. 355-363Gandolfi, S., Leitão-Filho, H.F., Bezerra, C.L.F., Levantamento florístico e caráter sucessional das espécies arbustivo-arbóreas de uma Floresta Mesófila Semidecídua no município de Guarulhos, SP (1995) Rev. Bras. Biol., 55, pp. 753-767Guicking, D., Fiala, B., Kröger-Kilian, T., Mohamed, M., Weising, K., High gene flow in two thrips-pollinated South-East Asian pioneer trees: genetic diversity and population structure of Macaranga hypoleuca and M. beccariana (Euphorbiaceae) (2013) Bot. J. Linn. Soc., 173, pp. 606-621Hamrick, J.L., Response of forest trees to global environmental changes (2004) For. Ecol. Manage., 197, pp. 323-335Hamrick, J.L., Nason, J.D., Gene flow in forest trees (2000) Forest Conservation Genetics: Principles and Practice, pp. 81-90. , CSIRO Publishing, Collingwood, A. Young, D. Boshier, T. Boyle (Eds.)Hedrick, P.W., (2011) Genetics of Populations, , Jones and Bartlett Publishers, SudburyHoldridge, L.R., (1967) Life Zone Ecology, , Tropical Scientific Center, San JoseHoll, K.D., Loik, M.E., Lin, E.H.V., Samuels, I.A., Tropical montane forest restoration in Costa Rica: overcoming barriers to dispersal and establishment (2000) Restor. Ecol., 8, pp. 339-349Jakobsson, M., Rosenberg, N.A., CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure (2007) Bioinformatics, 23, pp. 1801-1806Jones, F.A., Hubbell, S.P., Demographic spatial genetic structure of the Neotropical tree, Jacaranda copaia (2006) Mol. Ecol., 15, pp. 3205-3217Kalinowski, S.T., Counting alleles with rarefaction: private alleles and hierarchical sampling designs (2004) Conserv. Genet., 5, pp. 539-543Lemes, M.R., Gribel, R., Proctor, J., Grattapaglia, D., Population genetic structure of mahogany (Swietenia macrophylla King, Meliaceae) across the Brazilian Amazon, based on variation at microsatellite loci: implications for conservation (2003) Mol. Ecol., 12, pp. 2875-2883Lima, R.A.F., Martini, A.M.Z., Gandolfi, S., Rodrigues, R.R., Repeated disturbances and canopy disturbance regime in a tropical semi-deciduous forest (2008) J. Trop. Ecol., 24, pp. 85-93Litrico, I., Ronfort, J., Verlaque, R., Thompson, J.D., Spatial structure of genetic variation and primary succession in the pioneer tree species Antirhea borbonica on La Reunion (2005) Mol. Ecol., 14, pp. 1575-1584Lorenzi, H., (1992) Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil, , Plantarum, São PauloLoveless, M.D., Hamrick, J.L., Ecological determinants of genetic structure in plant populations (1984) Annu. Rev. Ecol. Syst., 15, pp. 65-95Marinoni, L., Miranda, G.F.G., Thompson, F.C., Abundância e riqueza de espécies de Syrphidae (Diptera) em áreas de borda e interior de floresta no Parque Estadual de Vila Velha, Ponta Grossa, Paraná, Brasil (2004) Revista Brasileira de Entomologia, 48, pp. 553-559Martini, A.M.Z., Lima, R.A.F., Franco, G.A.D.C., Rodrigues, R.R., The need for full inventories of tree modes of disturbance to improve forest dynamics comprehension: an example from a semideciduous forest in Brazil (2008) For. Ecol. Manage., 255, pp. 1479-1488McCauley, D.E., Ellis, J.R., Recombination and linkage disequilibrium among mitochondrial genes in structured populations of the gynodioecious plant Silene vulgaris (2008) Evolution, 62, pp. 823-832McCauley, D.E., Raveill, J., Antonovics, J., Local founding events as determinants of genetic structure in a plant metapopulation (1995) Heredity, 75, pp. 630-636Narbona, E., Arista, M., Ortiz, P.L., Explosive seed dispersal in two perennial mediterranean Euphorbia species (Euphorbiaceae) (2005) Am. J. Bot., 92, pp. 510-516Ndiade-Bourobou, D., Hardy, O.J., Favreau, B., Moussavou, H., Nzengue, E., Mignot, A., Bouvet, J.-M., Long-distance seed and pollen dispersal inferred from spatial genetic structure in the very low-density rainforest tree, Baillonella toxisperma Pierre, in Central Africa (2010) Mol. Ecol., 19, pp. 4949-4962Nei, M., (1987) Molecular Evolutionary Genetics, , Columbia University Press, New YorkPassos, L.C., Fenologia, polinização e reprodução de duas espécies de Croton (Euphorbiaceae) em Mata Semidecídua (1995), MSc Thesis, University of Campinas, BrazilPassos, L., Ferreira, S.O., Ant dispersal of Croton priscus (Euphorbiaceae) seeds in a tropical semideciduous forest in southeastern Brazil (1996) Biotropica, 28 (4 b), pp. 697-700Petit, R., El Mousadik, A., Pons, O., Identifying populations for conservation on the basis of genetic markers (1998) Conserv. Biol., 12, pp. 844-855Pritchard, J.K., Stephens, M., Donnelly, P., Inference of population structure using multilocus genotype data (2000) Genetics, 155, pp. 945-959Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J., Hirota, M.M., The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation (2009) Biol. Conserv., 142, pp. 1141-1153Rodrigues, R.R., (2005), http://www.lerf.esalq.usp.br/old/parrel2005.php, 4° Relatório temático do Projeto Parcelas Permanentes (04.09.14)Rosenberg, N.A., DISTRUCT: a program for the graphical display of population structure (2004) Mol. Ecol. Notes, 4, pp. 137-138Silvestrini, M., Ecology and evolution of Croton floribundus Spreng.: how are the genetic diversity and structure of a pioneer tree species affected by natural and human disturbances? (2014), PhD Thesis, University of Campinas, BrazilSilvestrini, M., Santos, F.A.M., Variation in the population structure between a natural and a human modified forest for a pioneer tropical tree species not restricted to large gaps (2015) Ecol. Evol., , (submitted for publication)Silvestrini, M., Pinto-Maglio, C.A.F., Zucchi, M.I., Santos, F.A.M., Cytogenetics and characterization of microsatellite loci for a South American pioneer tree species, Croton floribundus (2013) Genome, 56, pp. 743-751Slatkin, M., Gene flow and genetic drift in a species subject to frequent local extinctions (1977) Theor. Popul. Biol., 12, pp. 253-262Slatkin, M., Gene flow in natural populations (1985) Annu. Rev. Ecol. Syst., 16, pp. 393-430Slatkin, M., Gene flow and the geographic structure of natural populations (1987) Science, 236, pp. 787-792Sokal, R.R., Rohlf, F.J., (2012) Biometry: The Principles and Practice of Statistics in Biological Research, , W.H. Freeman and Company, New YorkStamp, N.E., Lucas, J.R., Ecological correlates of explosive seed dispersal (1983) Oecologia, 59, pp. 272-278Swaine, M.D., Whitmore, T.C., On the definition of ecological species groups in tropical rain forests (1988) Vegetatio, 75, pp. 81-86Swanson, M.E., Franklin, J.F., Beschta, R.L., Crisafulli, C.M., DellaSala, D.A., Hutto, R.L., Lindenmayer, D.B., Swanson, F.J., The forgotten stage of forest succession: early-successional ecosystems on forest sites (2011) Front. Ecol. Environ., 9, pp. 117-125Tabanez, M.F., Durigan, G., Keuroghlian, A., Barbosa, A.F., Freitas, C.A., Silva, C.E.F., Silva, D.A., Contieri, W.A., Plano de Manejo da Estação Ecológica dos Caetetus (2005) Instituto Florestal Série Registros, 29, pp. 1-104Tabarelli, M., Peres, C.A., Melo, F.P.L., The 'few winners and many losers' paradigm revisited: emerging prospects for tropical forest biodiversity (2012) Biol. Conserv., 155, pp. 136-140Uhl, C., Nepstad, D., Silva, J.M.C., Vieira, I., Restauração da floresta em pastagens degradadas (1991) Ciência Hoje, 13, pp. 23-31Uriarte, M., Clark, J.S., Zimmerman, J.K., Comita, L.S., Forero-Montaña, J., Thompson, J., Multidimensional trade-offs in species responses to disturbance: implications for diversity in a subtropical forest (2012) Ecology, 93, pp. 191-205Válio, I.F.M., Scarpa, F.M., Germination of seeds of tropical pioneer species under controlled and natural conditions (2001) Revista Brasileira de Botânica, 24, pp. 79-84Wade, M.J., McCauley, D.E., Extinction and recolonization: their effects on the genetic differentiation of local populations (1988) Evolution, 42, pp. 995-1005Wang, R., Compton, S.G., Chen, X., Fragmentation can increase spatial genetic structure without decreasing pollen-mediated gene flow in a wind-pollinated tree (2011) Mol. Ecol., 20, pp. 4421-4432Weising, K., Gardner, R.C., A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms (1999) Genome, 42, pp. 9-19Whitlock, M.C., McCauley, D.E., Some population genetic consequences of colony formation and extinction: genetic correlations within founding groups (1990) Evolution, 44, pp. 1717-1724Wright, S., Breeding structure of populations in relation to speciation (1940) Am. Nat., 74, pp. 232-24