The Neotropical tree Ilex paraguariensis A. St. Hil. (Aquifoliaceae): pollen and seed dispersal in a fragmented landscape

Authors

  • Carlos Seoane
  • Vinicius Diaz
  • Paulo Kageyama
  • Maria Moreno
  • Evandro Tambarussi
  • Ananda Aguiar
  • Alexandre Sebbenn

DOI:

https://doi.org/10.15287/afr.2019.1427

Keywords:

conservation genetics, gene ow, mixed ombrophilous forest, microsatellite markers, population genetics

Abstract

Ilex paraguariensis is a dioecious, Neotropical tree endemic to South America with wide cultural, economic and ecological signi cance. However, due to extensive fragmentation and deforestation throughout its natural area of occurrence, studies on gene ow and genetic diversity are needed to drive genetic conservation and improvement strategies. Based on the sampling of all adult and juvenile trees in two I. paraguariensis populations, we investigate the reali ed pollen and seed ow and dispersal distance, spatial genetic structure (SGS) and genetic diversity using microsatellite markers. We found limited genetic di erentiation between populations (G’ st = 0.033), but signi cant di erences in terms of genetic diversity (R: 4.7 vs 3.9, H 0 : 0.495 vs 0.371, H e : 0.445 vs 0.375), pollen (10 vs. 23.3%) and seed immigration (0 vs. 3.3%), mating among relatives (t r : 16 vs 30%) and biparental inbreeding (F r : 0.253 vs. 0.345). Within populations, the genetic diversity was similar between adults and juveniles, but adults presented signi cantly lower xation index than juveniles, suggesting selection against inbred individuals between juvenile and adult life stages. We also found similar mean pollen (255 vs. 293 m) and seed (385 vs. 323 m) dispersal distances within populations. Our results show that the studied populations are not genetically isolated and some mating occurs among related trees due to SGS; however, the frequency of biparental inbred individuals decrease over the life course due to inbreeding depression. These results contribute directly to species management and seed collection and inform in situ and ex situ conservation programs.

References

Ackerman M. S, Johri P., Spitze K., Xu S., Doak T. G., Young K., Lynch M., 2017. Estimating seven coefficients of pairwise relatedness using population-genomic data. Genetics 206(1):105–118. DOI: 10.1534/genetics.116.190660Almeida A. N., Bittencourt A. M., Santos A. J., Eisfeld C. L., Souza V. S., 2009. Production and price evolution of the main extractive non timber forest products in Brazil. Cerne 15(3):282–287.Ashley M.V., 2010. Plant parentage, pollination, and dispersal: How DNA microsatellite have altered the landscape. Critical Reviews in Plant Sciences 29(3):48–161. DOI: 10.1080/07352689.2010.481167Baldauf C., Ciampi-Guillardi M., Aguirra T. J., Correa C.E., Santos F. A. M., Souza A. P., Sebbenn A.M., 2014. Genetic diversity, spatial genetic structure and realized seed and pollen dispersal of Himatanthus drasticus (Apocynaceae) in the Brazilian savanna. Conservation Genetics 15(5):1073–1083. DOI: 10.1007/s10592-014-0600-5Bezemer N., Krauss S. L., Phillips R. D., Roberts D. G., Hopper S. D., 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(6):460–471. DOI: 10.1038/hdy.2016.61Carpanezzi A.A., 1995. Cultura da erva-mate no Brasil: conflitos e lacunas. In: Winge H, Ferreira A. G., Mariath J. E. A., Tarasconi L. C. (Eds.). Erva-mate: biologia e cultura no Cone Sul. Porto Alegre: Ed. da UFRGS, p. 43–46.Carvalho P. E. R., 1994 Espécies florestais brasileiras: Recomendações silviculturais, potencialidades e uso de madeira. Brasília: EMBRAPA-CNPF.Chaves C. L., Sebbenn A. M., Baranoski A., Goez B. D., Gaino A. P. S. C., Ruas C. F., Ruas E., Ruas P.E., 2017. Gene dispersal via seeds and pollen and their effects on genetic structure in the facultative-apomictic Neotropical tree Aspidosperma polyneuron. Silvae Genetica 65(2):2–12. DOI: 10.1515/sg-2016-0016Collevatti R. G., Estolano R., Garcia S. F., Hay J.D., 2010. Short-distance pollen dispersal and high self-pollination in a bat-pollinated neotropical tree. Tree Genet Genome 6(4):555–564. DOI: 10.1007/s11295-010-0271-4Debat H. J., Grabiele M., Aguilera P. M., Bubillo R. E., Otegui M. B., Ducasse D. A., Zapata P. D., Marti, D.A., 2014. Exploring the genes of yerba mate (Ilex paraguariensis A. St.-Hil.) by NGS and de novo transcriptome assembly. PlosOne 9:e109835. DOI: 10.1371/journal.pone.0109835Degen B., Sebbenn A. M., 2014. Genetic and tropical forest. In: Pancel L, Kölh M (eds). Tropical Forestry Handbook, 2nd ed. Berlin Heidelberg: Springer Verlag, Germany.Diaz V.S., Seoane C. E. S., Kageyama P. Y., Sebbenn A. M., 2013. Diversidade genética, estrutura genética espacial e fluxo gênico da erva-mate (Ilex paraguariensis A. St. Hil.) em dois fragmentos florestais na área de entorno do Parque Nacional do Iguaçu - PR. Documentos 247:1–46.Dow B. D., Ashley M. V., 1996. Microsatellite analysis of seed dispersal and parentage of sampling in bur oak, Quercus macrocarpa. Molecular Ecology 5(5):615–627. DOI: 10.1111/j.1365-294X.1996.tb00357.xDoyle J. J., Doyle J. L., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytoch Bull 19:11–15.Duminil J., Dainou K., Kaviriri D. K., Gillet P., Loo J., Doucet J. L., Hardy O.J., 2016. Relationships between population density, fine-scale genetic structure, mating system and pollen dispersal in a timber tree from African rainforests. Heredity 116(3):295–303. DOI: 10.1038/hdy.2015.101Ellstrand N.C., 2014. Is gene flow the most important evolutionary force in plants? American Journal of Botany 101(5):737–753. DOI: 10.3732/ajb.1400024Ferreira A. G., Kaspary R., Ferreira H. B., Rosa L. M. 1983.Proporção de sexo e polinização em Ilex paraguariensis St. Hil. Brasil Flor 53:29–33.Gaino A. P. S. C., Silva A. M., Moraes M. A., Alves P. F., Moraes M. L. T. M., Freitas M. L. M., Sebbenn A. M., 2010. Understanding the effects of isolation on seed and pollen flow, spatial genetic structure and effective population size of the dioecious tropical tree Myracrodruon urundeuva. Conservation Genetics 11(5):1631–1643. DOI: 10.1007/s10592-010-0046-3Garcia A. S., Bressan E. A., Bellester V. R., Figueira A., Sebbenn A. M., 2019. High rates of pollen and seed flow in Hymenaea stigonocarpa on a highly fragmented savanna landscape in Brazil. New For 50(6):991–1006. DOI: 10.1007/s11056-019-09710-3Goudet J., 1995. FSTAT (Version 1.2): A computer program to calculate F-statistics. Journal of Heredity 86(6):485–486. DOI: 10.1093/oxfordjournals.jhered.a111627Goverde M., Schweizer K., Baur B., Erhardt A., 2002. Small-scale habitat fragmentation effects on pollinator behavior: experimental evidence from the bumblebee Bombus veteranus on calcareous grasslands. Biological Conservation 104(3):293–299. DOI: 10.1016/S0006-3207(01)00194-XHamrick J.L., Trapnell D.W., 2011. Using population genetic analyses to understand seed dispersal patterns. Acta Oecologica 37(6):641–649. DOI: 10.1016/j.actao.2011.05.008Hardy O., Vekemans X., 2002. SPAGeDI: a versatile computer program to analyze spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2:618–620. DOI: 10.1046/j.1471-8278.2002.00305.xHardy O. J., Maggia L., Bandou E., Breyne P., Caron H., Chevallier M. H., Doligez A., Dutech C., Kremer A., Latouche-Halle C., Troispoux V., Veron V., Degen B., 2006. Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Molecular Ecology 15(2):559–571. DOI: 10.1111/j.1365-294X.2005.02785.xHardy O. J., Delaide B., Hainaut H., Gillet J. F., Gillet P., Kaymak E., Vankerckhove N., Dumminil J., Doucet J.L., 2019. Seed and pollen dispersal distances in two African legume timber trees and their reproductive potential under selective logging. Molecular Ecology 28:3119–3134. DOI: 10.1111/mec.15138Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59(8):1633–1638. ICMBIO. Parque Nacional do Iguaçu. <http://www4.icmbio.gov.br/parna_iguacu//>.Ismail C. A., Ghazoul J., Ravikanth G., Kushalappa C. G., Shaanker R. U., Kettle C. J., 2017. Evaluating realized seed dispersal across fragmented tropical landscapes: a two-fold approach using parentage analysis and the neighbourhood model. New Phytologist 214:1307–1316. DOI: 10.1111/nph.14427Leonarduzzi C., Leonardi S., Menozzi P., Piotti A., 2012. Towards an optimal sampling effort for paternity analysis in forest trees: what do the raw numbers tell us? iForest 5:18–25. DOI: 10.3832/ifor0606-009Loiselle 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(11):1420–1425.Lower 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. DOI: doi.org/10.1038/hdy.2015.40Manoel RO, Freitas MLM, Furlani Junior E, Alves PF, Moraes MLT, Sebbenn AM (2017) Low levels of pollen and seed flow in a riparian forest fragment of the dioecious tropical tree Genipa americana L. For Res Eng: Int Journal 1(1):00003. DOI: 10.15406/freij.2017.01.00003Marshall T. C., Slate J., Kruuk L. E. B, Pemberton J.M., 1998. Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology 7(5):639–655.Martins K., Raposo A., Klimas C. A., Veasey E. A., Kainer K., Wadt L. H.O., 2012. Pollen and seed flow patterns of Carapa guianensis Aublet. (Meliaceae) in two types of Amazonian forest. Genetics and Molecular Biology 35(4):818–826. DOI: 10.1590/S1415-47572012005000068Monthe F. K., Hardy O. J., Doucet J. L., Loo J., Duminil J., 2017. Extensive seed and pollen dispersal and assortative mating in the rain forest tree Entandrophragma cylindricum (Meliaceae) inferred from indirect and direct analyses. Molecular Ecology 26(19):5279–5291. DOI: 10.1111/mec.14241Moraes M. A. M., Gaino A. P. S., Moraes M. L. T., Freitas M. L. M., Sebbenn A. M., 2012. Estimating coancestry within open-pollinated progenies of a dioecious species: the case study of Myracrodruon urundeuva. Silvae Genetica 61(6):256–264. DOI: 10.1515/sg-2012-0032Moraes M. A, Kubota T. Y. K., Rossini B. C., Marino C. L., Freitas M. L. M., Moraes M.L.T., Silva A. M., Cambuim J., Sebbenn A. M., 2018. Long-distance pollen and seed dispersal and inbreeding depression in Hymenaea stigonocarpa (Fabaceae: Caesalpinioideae) in the Brazilian savannah. Ecology Evolution 8:7800–7816. DOI: 10.1002/ece3.4253Oliveira M. C. S., Regitano L. C., Roese A. D., Ahthonisen D. G., Parma M. M., Scagliusi S. M. M., Timoteo W. H. B., Jardim S. N., 2007. Fundamentos teóricos-práticos e protocolos de extração e de amplificação de DNA por meio da técnica de reação em cadeia de polimerase. São Carlos: Embrapa Pecuária Sudeste.Pereira M. F., Ciampi A. Y., Inglis P. W., Souza V. A., Azevedo, V. C., 2013. Shotgun sequencing for microsatellite identification in Ilex paraguariensis (Aquifoliaceae). Applications in Plant Sciences1(3):1200245. DOI: 10.3732/apps.1200245Potascheff C. M., Oddue-Muratorio S., Klein E. K., Figueira A., Bressan E. A., Oliveira P. E., Lander T., Sebbenn A. M., 2019. Stepping stones or stone dead? Fecundity, pollen dispersal and mating patterns of roadside Qualea grandiflora Mart. Trees. Conservation Genetics 20(6):1355-1367. DOI: 10.1007/s10592-019-01217-wRibeiro M. C., Metzger J. P., Martensen A. C., Ponzoni F. J., Hirato M. M., 2009. The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142(6):1141–1153. DOI: 10.1016/j.biocon.2009.02.021Sant’Anna C. S., Sebbenn A. M., Klabunde G. H. F., Bittencourt R., Nodari R. O., Mantovani A., Reis M. S., 2013. Realized pollen and seed dispersal within a continuous population of the dioecious coniferous Brazilian pine [Araucaria angustifolia (Bertol.) Kuntze]. Conservation Genetics 14(3):601–613. DOI: 10.1007/s10592-013-0451-5Sebbenn A.M., 2006. Sistema de reprodução em espécies arbóreas tropicais e suas implicações para a seleção de árvores matrizes para reflorestamentos ambientais. In: Higa A. R., Silva L. D. (Eds). Pomares de sementes de espécies florestais nativas (pp. 93–138). FUPEF, Curitiba.Sebbenn A. M., Carvalho A. C. M, Freitas M. L. M, Moraes S. M. B, Gaino A. P. S. C, Silva J. M., Jolivet C., Moraes M. L. T., 2011. Low level 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(1):134–145. DOI: 10.1038/hdy.2010.33Silva C. R. S., Albuquerque P. S. B., Ervedosa F. R., Figueira A., Sebbenn A.M., 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 106:973–985. DOI: 10.1038/hdy.2010.145Spoladore J., Mansano V.F., Lemes M. R., Freitas L. C.D., Sebbenn A.M., 2017. Genetic conservation of small populations of the endemic tree Swartzia glazioviana (Taub.) Glaz. (Leguminosae) in the Atlantic Forest. Conservation Genetics 18(5):1105–1117. 10.1007/s10592-017-0962-6Sturion J. A., Stuepp C. A., Wendling I., 2017. Genetic parameters estimates and visual selection for leaves production in Ilex paraguariensis. Bragantia 76(4):492–500. DOI: 10.1590/1678-4499.2016.419 Tambarussi E. V.,Sebbenn A. M., Alves-Pereira A., Vencovsky R., Cambuim J., da Silva A., Moraes, M., Moraes, M. L.T., 2017. Dipteryx alata Vogel (Fabaceae) a neotropical tree with high level of selfing: implication for conservation and breeding programs. Annals of Forest Research, 60(2): 243–261. DOI: 10.15287/afr.2017.842Tarazi R., Sebbenn A.M., Kageyama P.Y., Vencovsky R., 2013. Long-distance dispersal in a fire-and livestock-protected savanna. Ecolology Evolution 3(4):1003–1015. DOI: 10.1002/ece3.515Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analysis in plant populations. Molecular Ecology 13(4):921–935. DOI: 10.1046/j.1365-294x.2004.02076.xWendt S. N., Sousa V. A., Quoirion M., Mazza M. C., Sturion J. A., Sebbenn A. M., 2009. Baixa taxa de contaminação de pólen, desvios de cruzamentos aleatórios e endogamia em um pomar de sementes de Ilex paraguariensis. Scientia Forestalis 37(82):185–196.

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2019-12-31

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Research article