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Conservation Genetics

, Volume 20, Issue 6, pp 1355–1367 | Cite as

Stepping stones or stone dead? Fecundity, pollen dispersal and mating patterns of roadside Qualea grandiflora Mart. trees

  • Carolina M. Potascheff
  • Sylvie Oddou-Muratorio
  • Etienne K. Klein
  • Antonio Figueira
  • Eduardo A. Bressan
  • Paulo E.  Oliveira
  • Tonya A. Lander
  • Alexandre M. SebbennEmail author
Research Article
  • 163 Downloads

Abstract

Forest fragmentation may affect mating and pollen dispersal patterns through conversion of continuous forests into small, spatially isolated remnant patches and individual trees in an anthropogenic landscape. We investigated reproductive investment and success, pollen dispersal, mating system, and genetic diversity and spatial structure of Qualea grandiflora trees in two environmental contexts: a continuous natural Cerrado area and isolated individuals on roadsides. Roadside trees produced more flowers and more fruit than Cerrado trees. Pollen dispersal kernels were fat-tailed in both contexts, indicating long-distance dispersal, but in Cerrado the mean pollen dispersal distance (524.7 m) and the effective number of pollen donors per mother-tree (Nep = 12.7) were higher than for roadside trees (60.9 m, Nep = 4.6). The levels and structure of genetic diversity, outcrossing rates (\(t_{m}\) > 0.98), and mating among relatives (\(t_{m} - t_{s}\) < 0.1) were similar in both environmental contexts. Allelic richness and number of private alleles were similar between the two environments. The fixation index was significantly lower in adults (minimum of 0.08) than in offspring (minimum of 0.23) in both contexts, suggesting selection against inbred individuals between offspring and adult stage. Our results indicate that the spatial isolation of roadside trees, by increasing the number of flowers produced, decreased pollinator movements, thereby reducing effective pollen flow and the number of pollen donors. All these results suggest that roadside trees can be used for harvesting seeds for recovery plans, and that these trees are a biological legacy, and reservoir of Q. grandiflora genetic diversity, from the original Cerrado forest.

Keywords

Brazilian Cerrado Forest fragmentation Microsatellite markers Tropical trees 

Notes

Acknowledgements

This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Process number 2014/17472-5) and CMP, AMS, PEO, and AF are recipients of Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) fellowships. We are grateful to Centrovias Sistemas Rodoviários S/A for field support, to Alexandre M. da Silva for the map design. We thank Anne Roig (URFM, INRA) for the assistance in completing the genotyping. SOM and EK were granted by the FCT-ANR EXPANDTREE project (FCT-ANR-13-ISV7-0003-01). TL was funded by the Leverhulme Trust.

Supplementary material

10592_2019_1217_MOESM1_ESM.doc (507 kb)
Supplementary material 1 (DOC 507 kb)

References

  1. Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188PubMedGoogle Scholar
  2. Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728CrossRefGoogle Scholar
  3. Amorim FW, Wyatt GE, Sazima M (2014) Low abundance of long-tongued pollinators leads to pollen limitation in four specialized hawkmoth-pollinated plants in the Atlantic Rain forest, Brazil. Naturwissenschaften 101:893–905PubMedCrossRefGoogle Scholar
  4. Antiqueira LMOR, Kageyama PY (2015) Reproductive system and pollen flow in progenies of Qualea grandiflora Mart., a typical species of the Brazilian Cerrado. Rev Arv 39:337–344CrossRefGoogle Scholar
  5. Antiqueira LMOR, Bajay MM, Monteiro M, Souza RGVC, Moreno MA, Kageyama PY (2012) Development of microsatellite markers for Qualea grandiflora (Vochysiaceae), a typical species of the Brazilian Cerrado. Am J Bot 99:e97–e98CrossRefGoogle Scholar
  6. Breed MF, Gardner MG, Ottewell KM, Navarro CM, Lowe AJ (2012) Shifts in reproductive assurance strategies and inbreeding costs associated with habitat fragmentation in Central American mahogany. Ecol Lett 15:444–452PubMedPubMedCentralCrossRefGoogle Scholar
  7. Breed MF, Ottewell KM, Gardner MG, Marklund MHK, Dormontt EE, Lowe AJ (2015) Mating patterns and pollinator mobility are critical traits in forest fragmentation genetics. Heredity 115:108–114PubMedCrossRefGoogle Scholar
  8. Costa RC, Santos FAM (2011) Padrões espaciais de Qualea grandiflora Mart. em fragmentos de cerrado no estado de São Paulo. Acta Bot Bras 25:215–222CrossRefGoogle Scholar
  9. Cuénin N, Flores O, Rivière E, Lebreton G, Reynaud B, Martos F (2019) Great genetic diversity but high selfing rates and short-distance gene flow characterize populations of a tree (Foetidia; Lecythidaceae) in the fragmented tropical dry forest of the Mascarene Islands. J Hered 110:287–299PubMedCrossRefGoogle Scholar
  10. Davies SJ, Cavers S, Finegan B, White A, Breed MF, Lowe AJ (2015) Pollen flow in fragmented landscapes maintains genetic diversity following stand-replacing disturbance in a neotropical pioneer tree, Vochysia ferruginea Mart. Heredity 115:125–129PubMedCrossRefGoogle Scholar
  11. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  12. Françoso RD, Brandão R, Nogueira CC, Salmona YB, Machado RB, Colli GR (2015) Habitat loss and the effectiveness of protected areas in the Cerrado biodiversity hotspot. Braz J Nat Conserv 13:35–40CrossRefGoogle Scholar
  13. Freitas SR, Sousa COM, Boscolo D, Metzger JP (2013) How are native vegetation and reserves affected by different road types? Oecolog Aust 17:447–458CrossRefGoogle Scholar
  14. Garcia C, Jordano P, Godoy JA (2007) Contemporary pollen and seed dispersal in a Prunus mahaleb population: patterns in distance and direction. Mol Ecol 16:1947–1955PubMedCrossRefGoogle Scholar
  15. Giustina LD, Baldoni AB, Tonini H, Azevedo VCR, Neves LG, Tardin FD, Sebbenn AM (2018) Hierarchical outcrossing among and within fruits in Bertholletia excelsa Bonpl. (Lecythidaceae) open-pollinated seeds. Genet Mol Res 17:16039872CrossRefGoogle Scholar
  16. Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486CrossRefGoogle Scholar
  17. Hadley AS, Betts MG (2012) The effects of landscape fragmentation on pollination dynamics: absence of evidence not evidence of absence. Biol Rev 87:526–544PubMedCrossRefGoogle Scholar
  18. Hardy O, Vekemans X (2002) SPAGeDI: a versatile computer program to analyze spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  19. Henriques RPB, Hay JD (2002) Patterns and dynamics of plant populations. In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 140–158CrossRefGoogle Scholar
  20. Herrerıas-Diego Y, Quesada M, Stonera KE, Lobo JA, Hernandez-Floresa Y, Montoya GS (2008) Effect of forest fragmentation on fruit and seed predation of the tropical dry forest tree Ceiba aesculifolia. Biol Conserv 141:241–248CrossRefGoogle Scholar
  21. Ismail CA, Ghazoul J, Ravikanth G, Kushalappa CG, Shaanker RU, Kettle CJ (2017) Evaluating realized seed dispersal across fragmented tropical landscapes: a two-fold approach using parentage analysis and the neighbourhood model. New Phytol 214:1307–1316PubMedCrossRefGoogle Scholar
  22. Kamm U, Rotach P, Gugerli F, Siroky M, Edwards P, Holderegger R (2009) Frequent long-distance gene flow in a rare temperate forest tree (Sorbus domestica) at the landscape scale. Heredity 103:476–482PubMedCrossRefGoogle Scholar
  23. Lander TA, Boshier DH, 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. Biol Conserv 143:2583–2590CrossRefGoogle Scholar
  24. Lander T, Bebber DP, Choy CTL, Harris SA, Boshier DH (2011) The circe principle explains how resource-rich land can waylay pollinators in fragmented landscapes. Curr Biol 21:1302–1307PubMedCrossRefGoogle Scholar
  25. Lander T, Klein EK, Stoeckel S, Mariette S, Musch B, Oddou-Muratorio S (2013) Interpreting realized pollen flow in terms of pollinator travel paths and land-use resistance in heterogeneous landscapes. Landsc Ecol 28:1769–1783CrossRefGoogle Scholar
  26. Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425CrossRefGoogle Scholar
  27. Lorenzi H (2000) Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. São Paulo, 4th edn. Instituto Plantarum, Nova OdessaGoogle Scholar
  28. Lowe AJ, Cavers S, Boshier D, Breed MF, Hollingsworth PM (2015) The resilience of forest fragmentation genetics-no longer a paradox-we were just looking in the wrong place. Heredity 115:97–99PubMedPubMedCentralCrossRefGoogle Scholar
  29. Manning AD, Fischer J, Lindenmayer DB (2006) Scattered trees are keystone structures—implications for conservation. Biol Conserv 132:311–321CrossRefGoogle Scholar
  30. Manoel RO, Freitas MLM, Furlani E, Alves PF, Moraes MLT, Sebbenn AM (2015) Individual, fruit, and annual variation in correlated mating in a Genipa americana population. Silvae Genet 64:108–116CrossRefGoogle Scholar
  31. Marshall TC, Slate J, Kruuk LE, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655PubMedCrossRefGoogle Scholar
  32. Martin FW (1959) Staining and observing pollen tubes in the style by means of fluorescence. Stain Technol 34:125–128PubMedCrossRefGoogle Scholar
  33. Moraes MA, Kubota TYK, Rossini BC, Marino CL, Freitas MLM, Moraes MLT, Silva AM, Cambuim J, Sebbenn AM (2018) Long-distance pollen and seed dispersal and inbreeding depression in Hymenaea stigonocarpa (Fabaceae: Caesalpinioideae) in the Brazilian savannah. Ecol Evol 8:7800–7816PubMedPubMedCentralCrossRefGoogle Scholar
  34. Oddou-Muratorio S, Klein EK, Demesure-Musch B, Austerlitz F (2006) Real-time patterns of pollen flow in the wild-service tree, Sorbus torminalis (Rosaceae). III. Mating patterns and ecological maternal neighborhood. Am J Bot 93:1650–1659PubMedCrossRefGoogle Scholar
  35. Oddou-Muratorio S, Vendramin GG, Buiteveld J, Fady B (2008) Population estimators or progeny tests: what is the best method to assess null allele frequencies at SSR loci? Conserv Genet 10:1343–1347CrossRefGoogle Scholar
  36. Oliveira PEAM (1998) Reproductive biology, evolution and taxonomy of the Vochysiaceae in Central Brazil. In: Owens S, Rudall P (eds) Reproductive biology: in systematics, conservation and economic botany. R Bot Gard, Kew, pp 381–393Google Scholar
  37. Oliveira PEAM, Gibbs PE, Barbosa AA (2004) Moth pollination of woody species in the Cerrados of Central Brazil: a case of so much owed to so few? Plant Syst Evol 245:41–54CrossRefGoogle Scholar
  38. Oliveira-Filho AT, Ratter JA (2002) Vegetation physiognomies and woody flora of the Cerrado biome. In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 91–120CrossRefGoogle Scholar
  39. Potascheff CM, Brito VLG, Galetto L, Sebbenn AM, Oliveira PEAM (2019) Nectar features and mixed pollination system in Qualea grandiflora (Vochysiaceae). SubmittedGoogle Scholar
  40. R Development Core Team (2012) R: A language and environment for statistical computing, reference index version 2.12.1. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
  41. Ritland K (1989) Correlated matings in the partial selfer Mimulus guttatus. Evolution 43:848–859PubMedCrossRefGoogle Scholar
  42. Ritland K (2002) Extensions of models for the estimation of mating systems using n independent loci. Heredity 88:221–228PubMedCrossRefGoogle Scholar
  43. Robledo-Arnuncio JJ, Austerlitz F, Smouse PE (2006) A new method of estimating the pollen dispersal curve independently of effective density. Genetics 173:1033–1045PubMedPubMedCentralCrossRefGoogle Scholar
  44. Robledo-Arnuncio JJ, Austerlitz F, Smouse PE (2007) POLDISP: a software package for indirect estimation of contemporary pollen dispersal. Mol Ecol Notes 7:763–766CrossRefGoogle Scholar
  45. Rymer PD, Sandiford M, Harris SA, Billingham MR, Boshier DH (2015) Remnant Pachira quinata pasture trees have greater opportunities to self and suffer reduced reproductive success due to inbreeding depression. Heredity 115:115–124PubMedCrossRefGoogle Scholar
  46. Sebbenn AM (2006) Sistema de Reprodução em Espécies Tropicais e suas Implicações para a seleção de Árvores Matrizes para Reflorestamentos Ambientais. In: Silva LD, Higa AR (eds) Pomar de espécies florestais nativas. Curitiba, FUPEF, pp 93–138Google Scholar
  47. Sebbenn AM, Carvalho ACM, Freitas MLM, Moraes SMB, Gaino APSC, Silva JM, Jolivet C, Moraes MLT (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 106:134–145PubMedCrossRefGoogle Scholar
  48. Silva CRS, Albuquerque PSB, Ervedosa FR, Figueira A, 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 106:973–985PubMedCrossRefGoogle Scholar
  49. Silvestre EA, Schwarcz K, Grando D, Campos JB, Sujii PS, Tambarussi EV, Macrini CMT, Pinheiro JB, Brancalion PHS, Zucchi MI (2018) Mating system and effective population size of the overexploited Neotropical tree (Myroxylon peruiferum L.f.) and their impact on seedling production. J Hered 109:264–271PubMedCrossRefGoogle Scholar
  50. Smouse PE, Sork VL (2004) Measuring pollen flow in forest trees: an exposition of alternative approaches. For Ecol Manag 197:21–38CrossRefGoogle Scholar
  51. Spoladore J, Mansano VF, Lemes MR, Freitas LCD, Sebbenn AM (2017) Genetic conservation of small populations of the endemic tree Swartzia glazioviana (Taub.) Glaz. (Leguminosae) in the Atlantic Forest. Conserv Genet 18:1105–1117CrossRefGoogle Scholar
  52. Strassburg BBN, Brooks T, Feltran-Barbieri R, Iribarrem A, Crouzeilles R, Loyola R, Latawiec AE, Oliveira Filho FJB, Scaramuzza CAM, Scarano FR, Soares-Filho B, Balmford A (2017) Moment of truth for the Cerrado hotspot. Nat Ecol Evol 1(4):1–4.  https://doi.org/10.1038/s41559-017-0099 CrossRefGoogle Scholar
  53. Tambarussi EV, Boshier D, Vencovsky R, Freitas MLM, Sebbenn AM (2015) Paternity analysis reveals significant isolation and near neighbor pollen dispersal in small Cariniana legalis Mart. Kuntze populations in the Brazilian Atlantic Forest. Ecol Evol 5:5588–5600PubMedPubMedCentralCrossRefGoogle Scholar
  54. Tambarussi EV, Boshier DH, Vencovsky R, Freitas MLM, Di-Dio OJ, Sebbenn AM (2016) Several Small: how inbreeding affects conservation of Cariniana legalis Mart. Kuntze (Lecythidaceae) the Brazilian Atlantic Forests largest tree. Int For Rev 18:502–510Google Scholar
  55. Tarazi R, Sebbenn AM, Kageyama PY, Vencovsky R (2013) Edge effects enhance selfing and seed harvesting efforts in the insect-pollinated Neotropical tree Copaifera langsdorffii (Fabaceae). Heredity 110:578–585PubMedPubMedCentralCrossRefGoogle Scholar
  56. Vasconcelos PB, Araújo GM, Bruna EM (2014) The role of roadsides in conserving Cerrado plant diversity. Biodivers Conserv 23:3035–3050CrossRefGoogle Scholar
  57. Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935PubMedCrossRefGoogle Scholar
  58. Wadt LHO, Baldoni AB, Silva VS, Campos T, Martins K, Azevedo VCR, Mata LR, Botin AA, Hoogerheide ESS, Tonini H, Sebbenn AM (2015) Mating system variation among populations, individuals and within and among fruits in Bertholletia excelsa. Silvae Genet 64:248–259CrossRefGoogle Scholar
  59. Young A, Boyles T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 5347:413–418CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Carolina M. Potascheff
    • 1
  • Sylvie Oddou-Muratorio
    • 2
  • Etienne K. Klein
    • 3
  • Antonio Figueira
    • 4
  • Eduardo A. Bressan
    • 4
  • Paulo E.  Oliveira
    • 5
  • Tonya A. Lander
    • 6
  • Alexandre M. Sebbenn
    • 7
    Email author
  1. 1.Instituto de BiologiaUniversidade de CampinasCampinasBrazil
  2. 2.Unité de Recherches Forestières MéditerranéennesInstitut National de la Recherche Agronomique, Domaine Saint PaulAvignonFrance
  3. 3.BioSP, Biostatistique et Processus Spatiaux, INRA, Domaine Saint PaulAvignonFrance
  4. 4.Centro de Energia Nuclear na AgriculturaUniversidade de São PauloPiracicabaBrazil
  5. 5.Departamento de BiociênciasUniversidade Federal de UberlândiaUberlândiaBrazil
  6. 6.Department of Plant SciencesUniversity of OxfordOxfordUK
  7. 7.Instituto Florestal de São Paulo, Seção de Melhoramento e Conservação Genética FlorestalPiracicabaBrazil

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