Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-16T09:47:15.098Z Has data issue: false hasContentIssue false

Estimating genetic diversity, mating system and pollen dispersal to inform ex situ conservation of the tree Genipa americana L.

Published online by Cambridge University Press:  01 March 2021

Marília Freitas de Vasconcelos Melo
Affiliation:
Universidade Federal do Alagoas, Campus de Engenharias e Ciências Agrárias, CEP 57100-000, Rio Largo, AL, Brazil
Alexandre Magno Sebbenn
Affiliation:
Instituto Florestal de São Paulo, C.P. 1322, CEP 01059-970, São Paulo, SP, Brazil
Bruno Cesar Rossini*
Affiliation:
Universidade Estadual Paulista, Instituto de Biotecnologia, UNESP, CEP 18607-440, Botucatu, SP, Brazil
Ana Veruska Cruz da Silva Muniz
Affiliation:
Embrapa Tabuleiros Costeiros, CEP 49025-040, Aracaju, SE, Brazil
Carlos Jose Rodrigues
Affiliation:
Cia Energética de São Paulo, Usina Porto Primavera, CEP 19274-000, Primavera, SP, Brazil
Celso Luis Marino
Affiliation:
Universidade Estadual Paulista, Instituto de Biotecnologia, UNESP, CEP 18607-440, Botucatu, SP, Brazil
Mario Luiz Teixeira de Moraes
Affiliation:
Universidade Estadual Paulista, Faculdade de Engenharia, UNESP, CEP 15385-000, Ilha Solteira, SP, Brazil
*
*Corresponding author. E-mail: bruno.rossini@unesp.br

Abstract

Using microsatellite loci, we assessed the mating system and genetic diversity of the dioecious tropical tree Genipa americana in a natural population (NP) and a progeny test (PT). For NP, we also estimated the paternity correlation within and among fruits and mean pollen dispersal distance. As expected for dioecious species, all offspring originated from outcrossing (t = 1). Mating among relatives (1 − ts) and paternity correlation (rp) were variable among progenies (1 − ts = 0.03–0.19; rp = 0.04–0.40), but greater in NP than in PT. Fixation index (F) was generally significant and lower in adults than in offspring, indicating selection against inbred individuals. Paternity correlation was higher within (0.40) than among (0.26) fruits, indicating a lower effective number of pollen donors (Nep) within (2.5) than among (3.8) fruits. Due to the higher rp in NP, the effective size within progenies (Ne) was lower (2.69) than PT (3.27). The pollen dispersal pattern was strongly leptokurtic, suggesting long-distance pollen dispersal (mean of 179 m). The results show that both populations can be used for seed collection in environmental reforestation programmes; however, considering that PT is structured in maternal progenies, NP is more suitable for seed collection due to the lower probability of mating among related trees.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of NIAB

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

Abou-Shaara, HF (2014) The foraging behaviour of honey bees, Apis mellifera: a review. Veterinarini Medicina 59: 110.CrossRefGoogle Scholar
Baldauf, C, Ciampi-Guillardi, M, Aguirra, TJ, Corrêa, CE, Santos, FAM, Souza, AP and Sebbenn, AM (2014) Genetic diversity spatial genetic structure and realized seed and pollen dispersal of Himatanthus drasticus (Apocynaceae) in the Brazilian savanna. Conservation Genetics 15: 10731083.CrossRefGoogle Scholar
Baldoni, AB, Wadt, LHO, Campos, T, Silva, VS, Azevedo, VCR, Mata, LR, Botin, AA, Mendes, NO, Tardin, FD, Tonini, H, Hoogerheide, ESS and Sebbenn, AM (2017) Contemporary pollen and seed dispersal in natural populations of Bertholletia excelsa (Bonpl.). Genetics and Molecular Research 16: gmr16039756.CrossRefGoogle Scholar
Bakkali, AE, Haouane, H, Hadiddou, A, Oukabli, A, Santoni, S, Udupa, SM, Van Damme, P and Khadari, B (2013) Genetic diversity of on-farm selected olive trees in Moroccan traditional olive orchards. Plant Genetic Resources 11: 97105.CrossRefGoogle Scholar
Bezemer, N, Krauss, SL, Phillips, RD, Roberts, DG and Hopper, SD (2016) Paternity analysis reveals wide pollen dispersal and high multiple paternity in a small isolated population of the bird-pollinated Eucalyptus caesia (Myrtaceae). Heredity 117: 460470.CrossRefGoogle Scholar
Braga, AC and Collevatti, RG (2011) Temporal variation in pollen dispersal and breeding structure in a bee-pollinated Neotropical tree. Heredity 106: 911919.CrossRefGoogle Scholar
Breed, MF, Ottewell, KM, Gardner, MG, Marklund, MHK, Dormontt, EE and Lowe, AJ (2015) Mating patterns and pollinator mobility are critical traits in forest fragmentation genetics. Heredity 115: 108114.CrossRefGoogle ScholarPubMed
Caballero, A, Bravo, I and Wang, J (2016) Inbreeding load and purging: implications for the short-term survival and the conservation management of small populations. Heredity 118: 177185.CrossRefGoogle ScholarPubMed
Carvalho, PER (1994) Espécies florestais brasileiras: recomendações silviculturais, potencialidade e uso da madeira. Embrapa Florestas, Colombo.Google Scholar
Chybicki, IJ and Burczyk, J (2009) Simultaneous estimation of null alleles and inbreeding coefficients. Journal of Heredity 100: 106113.CrossRefGoogle ScholarPubMed
Colombo, AF and Joly, CA (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: 697708.CrossRefGoogle Scholar
Crestana, MSM, Toledo Filho, DV and Campos, JB (2004) Florestas: sistemas e recuperação com essências nativas, produção de mudas e legislação Campinas: Coordenadoria de Assistência Técnica Integral, pp. 216.Google Scholar
Degen, B and Sebbenn, AM (2014) Genetic and tropical forest. In: Pancel, L and Kölh, M (eds) Tropical Forestry Handbook. Berlin: Heidelberg: Springer-Verlag, pp. 130.Google Scholar
De Vere, N, Jones, LE, Gilmore, T, Moscrop, J, Lowe, A, Smith, D, Hegarty, MJ, Creer, S and Ford, CR (2017) Using DNA metabarcoding to investigate honey bee foraging reveals limited flower use despite high floral availability. Scientific Reports 7: 42838.CrossRefGoogle ScholarPubMed
Dinerstein, E, Olson, DM, Graham, DJ, Webster, AL, Primm, AS, Bookbinder, MP and Ledec, GA (1995) Conservation Assessment of the Terrestrial Ecoregions of Latin America and the Caribbean. Washington: World Bank, pp. 176.CrossRefGoogle Scholar
Doyle, JJ and Doyle, JL (1990) Isolation of plant DNA from fresh tissue. Focus 12: 1315.Google Scholar
Durigan, G and Nogueira, JCB (1990) Recomposição de matas ciliares. Série Registros: Instituto Florestal de São Paulo 4: 114.Google Scholar
Francisco, CF (1989) Análise ambiental e consequência do desmatamento no município de Presidente Prudente no período de 1914 à 1986. Rio Claro. Dissertação (Mestrado em Geografia) Instituto de Geociências e Ciências Exatas, Universade Estadual Paulista.Google Scholar
Francoso, RD, Haidar, RF and Machado, RB (2016) Tree species of South America central savanna: endemism, marginal areas and the relationship with other biomes. Acta Botanica Basilica 30: 7886.CrossRefGoogle Scholar
Feres, JM, Sebbenn, AM, Guidugli, MC, Mestriner, MA, Moraes, MLT and Alzate-Marin, AL (2012) Mating system parameters at hierarchical levels of fruits, individuals and populations in the Brazilian insect-pollinated tropical tree, Tabebuia roseo-alba (Bignoniaceae). Conservation Genetics 13: 393405.CrossRefGoogle Scholar
Fuchs, EJ and Hamrick, JL (2011) Mating system and pollen flow between remnant populations of the endangered tropical tree, Guaiacum sanctum (Zygophyllaceae). Conservation Genetics 12: 175185.CrossRefGoogle Scholar
Fuchs, EJ, Lobo, JA and Quesada, M (2003) Effects of forest fragmentation and flowering phenology on the reproductive success and mating patterns of the tropical dry forest tree Pachira quinata. Conservation Biology 17: 149157.CrossRefGoogle Scholar
Giustina, LD, Baldoni, AB, Tonini, H, Azevedo, VCR, Neves, LG, Tardin, FD and Sebbenn, AM (2018) Hierarchical outcrossing among and within fruits in Bertholletia excelsa Bonpl. (Lecythidaceae) open-pollinated seeds. Genetics and Molecular Research 17: gmr16039872.CrossRefGoogle Scholar
Goudet, J (1995) FSTAT (version 2.9.3.2.): a computer program to calculate F-statistics. Journal of Heredity 86: 485486.CrossRefGoogle Scholar
Hardy, OJ, Maggia, L, Bandou, E, Breyne, P, Henri Caron, H, Chevallier, M, Doliguez, A, Dutech, C, Kremer, A, Latouche-Halle, C, Troispoux, V, Veron, V and Degen, B (2006) Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Molecular Ecology 15: 559579.CrossRefGoogle ScholarPubMed
Hausman, CE, Bertke, MM, Jaeger, JF and Rocha, OJ (2014) Genetic structure of green ash (Fraxinus pennsylvanica): implications for the establishment of ex situ conservation protocols in light of the invasion of the emerald. Plant Genetic Resources: Characterization and Utilization 12: 286297.CrossRefGoogle Scholar
Hedrick, PW (2005) A standardized genetic differentiation measure. Evolution 59: 16331638.CrossRefGoogle ScholarPubMed
Hodgkin, T, Rao, VR, Cibrian-Jaramillo, A and Gaiji, S (2003) The use of ex situ conserved plant genetic resources. Plant Genetic Resources 1: 1929.CrossRefGoogle Scholar
Ismail, SA, Ghazoul, J, Ravikanth, G, Uma Shaanker, R, Kushalappa, CG and Kettle, CJ (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
Lande, R (1995) Mutation and conservation. Conservation Biology 9: 782791.CrossRefGoogle Scholar
Lander, TA, Boshier, DH and Harris, SA (2010) Fragmented but not isolated: contribution of single trees, small patches and long-distance pollen flow to genetic connectivity for Gomortega keule, an endangered Chilean tree. Biological Conservation 143: 25832590.CrossRefGoogle Scholar
Lander, TA, Harris, SA, Cremona, PJ and Boshier, DH (2019) Impact of habitat loss and fragmentation on reproduction, dispersal and species persistence for an endangered Chilean tree. Conservation Genetics 20: 973985.CrossRefGoogle Scholar
Manoel, RO, Alves, PF, Dourado, CL, Gaino, APSC, Freitas, MLM, Moraes, MLT and Sebbenn, AM (2012) Contemporary pollen flow, mating patterns and effective population size inferred from paternity analysis in a small fragmented population of the Neotropical tree Copaifera langsdorffii Desf. (Leguminosae-Caesalpinioideae). Conservation Genetics 13: 613623.CrossRefGoogle Scholar
Manoel, RO, Freitas, MLM, Barreto, MA, Moraes, MLT, Souza, AP and Sebbenn, AM (2014) Development and characterization of 32 microsatellite loci in Genipa americana (Rubiaceae). Applications in Plant Sciences 2: 1300084.CrossRefGoogle Scholar
Manoel, RO, Freitas, MLM, Furlani Junior, E, Alves, PF, Moraes, MLT and Sebbenn, AM (2015a) Individual, fruit, and annual variation in correlated mating in a Genipa americana population. Silvae Genetica 69: 108116.CrossRefGoogle Scholar
Manoel, RO, Freitas, MLM, Tambarussi, EV, Cambuim, J, Moraes, MLT and Sebbenn, AM (2015b) Study of Mendelian inheritance, genetic linkage and genotypic disequilibrium at six microsatellite loci of Genipa americana L. (Rubiaceae). Genetics and Molecular Research 14: 81618169.CrossRefGoogle Scholar
Manoel, RO, Freitas, MLM, Furlani Junior, E, Alves, PF, Moraes, MLT and Sebbenn, AM (2017) Low levels of pollen and seed flow in a riparian forest fragment of the dioecious tropical tree Genipa americana L. Forestry Research and Engineering: International Journal 1: 1827.Google Scholar
Moraes, MA, Kubota, TYK, Rossini, BC, Marino, CL, Freitas, MLM, Moraes, MLT, Silva, AM, Cambuim, J and Sebbenn, AM (2018) Long-distance pollen and seed dispersal and inbreeding depression in Hymenaea stigonocarpa (Fabaceae: Caesalpinioideae) in the Brazilian savannah. Ecology and Evolution 8: 78007816.CrossRefGoogle ScholarPubMed
Nunney, L and Campbell, KA (1993) Assessing minimum viable population size: demography meets population genetics. Tree 8: 234239.Google ScholarPubMed
Oliveira, JB. (1999) Mapa pedológico do Estado de São Paulo: legenda expandida. Instituto Agronômico, Campinas.Google Scholar
Potascheff, CM, Oddou-Muratorio, S, Klein, EK, Figueira, A, Bressan, EA, Oliveira, PE, Lander, TA and Sebbenn, AM (2019) Stepping stones or stone dead? Fecundity, pollen dispersal and mating patterns of roadside Qualea grandiflora Mart. trees. Conservation Genetics 20: 13551367.CrossRefGoogle Scholar
Rabbani, ARC, Silva-Mann, R and Ferreira, RA (2012) Variabilidade genética de Genipa americana L. pertencente ao baixo curso do rio São Francisco. Revista Arvore 36: 401409.CrossRefGoogle Scholar
Reim, S, Proft, A, Heinz, S and Lochschmidt, F (2015) Pollen movement in a Malus sylvestris population and conclusions for conservation measures. Plant Genetic Resources: Characterisation and Utilisation 15: 1220.CrossRefGoogle Scholar
Ritland, K (2002) Estimation of gene frequency and heterozygosity from pooled samples. Molecular Ecology Notes 78: 370372.CrossRefGoogle Scholar
Robledo-Arnuncio, JJ, Austerlitz, F and Smouse, PE (2007) POLDISP: a software package for indirect estimation of contemporary pollen dispersal. Molecular Ecology 7: 763766.CrossRefGoogle Scholar
Ruzza, DAC, Rossi, AAB, Bispo, RB, Tiago, AV, Cochev, JS, Rossi, FS and Fernandes, JM (2018) The genetic diversity and population structure of Genipa americana (Rubiaceae) in Northern Mato Grosso, Brazil. Genetics and Molecular Research 17: gm18017.CrossRefGoogle Scholar
Schuelke, M (2000) An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18: 233234.CrossRefGoogle ScholarPubMed
Sebbenn, AM (2006) Sistema de reprodução em espécies arbóreas tropicais e suas implicações para a seleção de árvores matrizes para reflorestamentos ambientais. In: Higa, AR and Silva, LD (eds) Pomares de Sementes de Espécies Nativas.Curitiba: FUDEP, pp. 193198.Google Scholar
Sebbenn, AM, Kageyama, PY and Vencovsky, R (1998) Variabilidade genética, sistema reprodutivo e estrutura genética especial em Genipa americana L. através de marcadores isoenzimáticos. Scientia Forestalis 53: 1530.Google Scholar
Sebbenn, AM, Boshier, D, Freitas, MLM, Zanatto, ACS, Sato, AS, Ettori, LC and Moraes, E (2007) Results of an international provenance trial of Cordia alliodora in São Paulo, Brazil at five and 23 years of age. Silvae Genetica 56: 110117.CrossRefGoogle Scholar
Sergipe, (2000) Secretaria de Estado do Planejamento e da Ciência e Tecnologia. Santana do São Francisco. In: Perfis Municipais Aracaju, pp. 75.Google Scholar
Silva, CRS, Albuquerque, PSB, Ervedosa, FR, Mota, JWS, Figueira, A and Sebbenn, AM (2011) Understanding the genetic diversity, spatial genetic structure and mating system at the hierarchical levels of fruits and individuals of a continuous Theobroma cacao population from the Brazilian Amazon. Heredity 106: 973985.CrossRefGoogle ScholarPubMed
Silva, RFB, Millington, JDA, Moran, EF, Batistella, M and Liu, J (2020) Three decades of land-use and land cover changes in mountain regions of the Brazilian Atlantic Forest. Landscape and Urban Planning 204: 103948.CrossRefGoogle Scholar
Smouse, PE and Sork, VL (2004) Measuring pollen flow in forest trees: an exposition of alternative approaches. Forest Ecology and Management 197: 2138.CrossRefGoogle Scholar
Solís-Hernández, W and Fuchs, EJ (2019) Effective gene flow patterns across a fragmented landscape in southern Costa Rica for Symphonia globulifera (Clusiaceae): a species with mobile seed and pollen dispersers. Revista de Biología Tropical 67: 95111.CrossRefGoogle Scholar
Sousa, VA, Sebbenn, AM, Hattemer, H and Ziehe, M (2005) Correlated mating in populations of a dioecious Brazilian conifer, Araucaria angustifolia (Bert.) O. Ktze. Forest Genetics 12: 107119.Google Scholar
Souza, FB, Kubota, TYK, Tambarussi, EV, Freitas, MLM, Moraes, MLT, Silva, AM, Cambuim, J and Sebbenn, AM (2018) Historic pollen and seed dispersal in fragmented populations of the two largest trees of the Atlantic Forest. Forestry Research and Engineering: International Journal 2: 100109.Google Scholar
Spoladore, J, Mansano, VF, Lemes, MR, Freitas, LCD and Sebbenn, AM (2017) Genetic conservation of small populations of the endemic tree Swartzia glazioviana (Taub.) Glaz. (Leguminosae) in the Atlantic Forest. Conservation Genetics 18: 11051117.CrossRefGoogle Scholar
Steffan-Dewenter, I and Kuhn, A (2003) Honeybee foraging in differentially structured landscapes. Proceedings: Biological Sciences 270: 569575.Google ScholarPubMed
Tamaki, I, Setsuko, S and Tomaru, N (2009) Estimation of outcrossing rates at hierarchical levels of fruits, individuals, populations and species in Magnolia stellata. Heredity 102: 381388.CrossRefGoogle ScholarPubMed
Tambarussi, EV, Boshier, D, Vencovsky, R, Freitas, MLM and Sebbenn, AM (2015) Paternity analysis reveals significant isolation and near neighbour pollen dispersal in small Cariniana legalis Mart. Kuntze populations in the Brazilian Atlantic Forest. Ecology and Evolution 5: 55885600.CrossRefGoogle Scholar
Tarazi, R, Sebbenn, AM, Kageyama, PY and Vencovsky, R (2013) Edge effects enhance selfing and seed harvesting efforts in the insect-pollinated Neotropical tree Copaifera langsdorffii (Fabaceae). Heredity 110: 578585.CrossRefGoogle Scholar
Wadt, LHO, Baldoni, AB, Silva, VS, Campos, T, Martins, K, Azevedo, VCR, Mata, LR, Botin, AA, Hoogerheide, ESS, Tonini, H and Sebbenn, AM (2015) Mating system variation among populations, individuals and within and among fruits in Bertholletia excelsa. Silvae Genetica 64: 248259.CrossRefGoogle Scholar
Supplementary material: File

Melo et al. supplementary material

Melo et al. supplementary material 1

Download Melo et al. supplementary material(File)
File 308.7 KB
Supplementary material: File

Melo et al. supplementary material

Melo et al. supplementary material 2
Download Melo et al. supplementary material(File)
File 78.4 KB