High selfing rate, limited pollen dispersal and inbreeding depression in the emblematic African rain forest tree Baillonella toxisperma - Management implications
Duminil, Jérôme; Mendene Abessolo, D. T.; Ndiade Bourobou, D.et al.
2016 • In Forest Ecology and Management, 379, p. 20-29
Inbreeding; Gene flow; Logging; Selfing; Spatial genetic structure; Timber species
Abstract :
[en] Mating system and gene flow are major influencing factors of species population dynamics and evolution. These factors are often not characterized in tropical tree species, yet they constitute basic information that must be considered to implement sustainable management practices. In particular, as logging implies a reduction of the density of congeneric mates, the connectivity through pollination between individuals has to be well characterized (selfing versus outcrossing rates, distances between mates). We conducted a genetic-based analysis (using 10 nuclear microsatellites) to determine the mating system and gene flow characteristics of an emblematic timber tree species from lowland rain forests of the Congo Basin, Baillonella toxisperma (Sapotaceae). The species, which is frequently exploited for its wood and for a number of non-timber forest products, naturally occurs at low densities (ca. 0.01–0.1 individuals/ha). It is supposedly an entomophilous species whose seeds are probably dispersed by mammals. We have shown that the species presents a mixed-mating system (about 20–40% of selfing depending on analysis method). However, the comparison of inbreeding parameters among cohorts suggests that inbred individuals die between seedling and mature tree stages. The mean pollen dispersal distance was relatively low for such a low-density population species (estimated to be 690 or 777 m depending on analysis method) and, together with a low mean number of pollen donors (NEP = 2.76), it suggests a pattern of nearest-neighbour mating where allo-pollen could be a limiting factor. However, B. toxisperma presents a relatively weak genetic structure (Sp statistic = 0.0095) indicative of long gene dispersal distance (rg = 3–5 km according to the assumed effective population density). Overall, this would indicate that gene flow occurs mainly by extensive seed dispersal in this species. These results suggest that mammals and local populations involved in the dispersal of the species play a key role by lowering biparental inbreeding effects. Sustainable population management might require assisted regeneration using unrelated planting material.
Doucet, Jean-Louis ; Université de Liège > Ingénierie des biosystèmes (Biose) > Laboratoire de Foresterie des régions trop. et subtropicales
Loo, J.
Hardy, Olivier J.
Language :
English
Title :
High selfing rate, limited pollen dispersal and inbreeding depression in the emblematic African rain forest tree Baillonella toxisperma - Management implications
Aguilar, R., Quesada, M., Ashworth, L., Herrerias-Diego, Y., Lobo, J., Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol. Ecol. 17 (2008), 5177–5188.
Ashley, M.V., Plant parentage, pollination, and dispersal: how DNA microsatellites have altered the landscape. CRC Crit. Rev. Plant Sci. 29 (2010), 148–161.
Ashman, T.-L., Knight, T.M., Steets, J.A., Amarasekare, P., Burd, M., Campbell, D.R., Dudash, M.R., Johnston, M.O., Mazer, S.J., Mitchell, R.J., Morgan, M.T., Wilson, W.G., Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85 (2004), 2408–2421.
Austerlitz, F., Dick, C.W., Dutech, C., Klein, E.K., Oddou-Muratorio, S., Smouse, P.E., Sork, V.L., Using genetic markers to estimate the pollen dispersal curve. Mol. Ecol. 13 (2004), 937–954.
Barrett, S.C.H., Eckert, C.G., Current issues in plant reproductive biology. Isr. J. Bot. 39 (2013), 5–12.
Barrett, S.C.H., Harder, L.D., Worley, A.C., The comparative biology of pollination and mating in flowering plants. Philos. Trans. R. Soc. London Ser. B-Biol. Sci. 351 (1996), 1271–1280.
Bawa, K., Ashton, P., Nor, S., 1990. Reproductive ecology of tropical forest plants: management issues. In: Bawa, K., Hadley, M. (Eds.), Reproductive Ecology of Tropical Forest Plants.
Beaune, D., Fruth, B., Bollache, L., Hohmann, G., Bretagnolle, F., Doom of the elephant-dependent trees in a Congo tropical forest. For. Ecol. Manage. 295 (2013), 109–117.
Bittencourt, J.V.M., Sebbenn, A.M., Patterns of pollen and seed dispersal in a small, fragmented population of the wind-pollinated tree Araucaria angustifolia in southern Brazil. Heredity (Edinb) 99 (2007), 580–591.
Bizoux, J.-P., Daïnou, K., Bourland, N., Hardy, O.J., Heuertz, M., Mahy, G., Doucet, J.-L., Spatial genetic structure in Milicia excelsa (Moraceae) indicates extensive gene dispersal in a low density wind pollinated tropical tree. Mol. Ecol. 18 (2009), 4398–4408.
Born, 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. Proc. R. Soc. B-Biol. Sci. 275 (2008), 2171–2179.
Charlesworth, D., Charlesworth, B., Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18 (1987), 237–268.
Chybicki, I.J., Note on the applicability of the F-model in analysis of pollen pool heterogeneity. J. Hered. 104 (2013), 578–585.
Chybicki, I.J., Burczyk, J., Seeing the forest through the trees: comprehensive inference on individual mating patterns in a mixed stand of Quercus robur and Q. petraea. Ann. Bot. 112 (2013), 561–574.
Chybicki, I.J., Burczyk, J., NM+: software implementing parentage-based models for estimating gene dispersal and mating patterns in plants. Mol. Ecol. Resour. 10 (2010), 1071–1075.
Chybicki, I.J., Burczyk, J., Simultaneous estimation of null alleles and inbreeding coefficients. J. Hered. 100 (2009), 106–113.
Connell, J.H., On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. den Boer, P.J., Gradwell, G.R., (eds.) Dynamics of Populations, 1971, Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands, 298–312.
Côrtes, M.C., Uriarte, M., Lemes, M.R., Gribel, R., Kress, W.J., Smouse, P.E., Bruna, E.M., Low plant density enhances gene dispersal in the Amazonian understory herb Heliconia acuminata. Mol. Ecol. 22 (2013), 5716–5729.
Debout, G.D.G., Doucet, J.L., Hardy, O.J., Population history and gene dispersal inferred from spatial genetic structure of a Central African timber tree, Distemonanthus benthamianus (Caesalpinioideae). Heredity (Edinb) 106 (2010), 88–99.
Debroux, L., L'aménagement des forêts tropicales fondé sur la gestion des populations d'arbres: l'exemple du moabi (Baillonella toxisperma Pierre) dans la forêt du Dja, Cameroun. PhD Thesis, 1998, Fac. Univ. Sci. Agron., Gembloux, Belgium.
Dick, C.W., Hardy, O.J., Jones, F.A., Petit, R.J., Spatial scales of pollen and seed-mediated gene flow in tropical rain forest trees. Trop. Plant Biol. 1 (2008), 20–33.
Doucet, J.-L., Daïnou, K., Ligot, G., Ouédraogo, D.-Y., Bourland, N., Ward, S.E., Tekam, P., Lagoute, P., Fayolle, A., Enrichment of Central African logged forests with high-value tree species: testing a new approach to regenerating degraded forests. Int. J. Biodivers. Sci. Ecosyst. Serv. Manage., 2016, 1–13.
Doucet, J.-L., Kouadio, L., Le moabi, une espèce “phare” de l'exploitation forestière en Afrique centrale. Parcs et Réserves 62 (2007), 25–31.
Doucet, J.-L., Kouadio, Y.L., Monticelli, D., Lejeune, P., Enrichment of logging gaps with moabi (Baillonella toxisperma Pierre) in a Central African rain forest. For. Ecol. Manage. 258 (2009), 2407–2415.
Duminil, J., Daïnou, K., Kombi Kaviriri, D., Gillet, P., Loo, J., Doucet, J.-L., Hardy, O.H., Relationships between population density, fine-scale genetic structure, mating system and pollen dispersal in a timber tree from African rainforests. Heredity (Edinb) 116 (2016), 295–303.
Duminil, J., Hardy, O.J., Petit, R.J., Plant traits correlated with generation time directly affect inbreeding depression and mating system and indirectly genetic structure. BMC Evol. Biol., 9, 2009, 177.
Eckert, C.G., Kalisz, S., Geber, M.A., Sargent, R., Elle, E., Cheptou, P.-O., Goodwillie, C., Johnston, M.O., Kelly, J.K., Moeller, D.A., Porcher, E., Ree, R.H., Vallejo-Marín, M., Winn, A.A., Plant mating systems in a changing world. Trends Ecol. Evol. 25 (2010), 35–43.
Forget, P.M., Dennis, A.J., Mazer, S.J., Jansen, P.A., Kitamura, S., Lambert, J.E., Westcott, D.A., Seed allometry and disperser assemblages in tropical rainforests: a comparison of four floras on different continents. Dennis, A.E.W.S., Green, R., Westcott, D.A., (eds.) Seed Dispersal: Theory and Its Application in a Changing World, 2007, CAB International Publishing, Wallingford, UK, 5–36.
Gaino, A.P.S.C., Silva, A.M., Moraes, M.A., Alves, P.F., Moraes, M.L.T., Freitas, M.L.M., Sebbenn, A.M., Understanding the effects of isolation on seed and pollen flow, spatial genetic structure and effective population size of the dioecious tropical tree species Myracrodruon urundeuva. Conserv. Genet. 11 (2010), 1631–1643.
Gautier-Hion, A., Duplantier, J.-M., Quris, R., Feer, F., Sourd, C., Decoux, J.-P., Dubost, G., Emmons, L., Erard, C., Hecketsweiler, P., Moungazi, A., Roussilhon, C., Thiollay, J.-M., Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65 (1985), 324–337.
Goodwillie, C., Kalisz, S., Eckert, C.G., The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu. Rev. Ecol. Evol. Syst. 36 (2005), 47–79.
Hall, J.S., Seed and seedling survival of African mahogany (Entandrophragma spp.) in the Central African Republic: implications for forest management. For. Ecol. Manage. 255 (2008), 292–299.
Hardy, 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., Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Mol. Ecol. 15 (2006), 559–571.
Hardy, O.J., Vekemans, X., SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol. Ecol. Notes 2 (2002), 618–620.
Heuertz, M., Vekemans, X., Hausman, J.F., Palada, M., Hardy, O.J., Estimating seed vs. pollen dispersal from spatial genetic structure in the common ash. Mol. Ecol. 12 (2003), 2483–2495.
Janzen, D.H., Herbivores and the number of tree species in tropical forests. Am. Nat. 104 (1970), 501–528.
Klekowski, E., Genetic load and its causes in long-lived plants. Trees 2 (1988), 195–203.
Letouzey, R., 1968. Etude phytogéographique du Cameroun. In: Paul Lechevalier (Ed.), Encycl. Biol., vol. LXIX, Paris, 513 p.
Loiselle, B.A., Sork, V.L., Nason, J., Graham, C., Spatial genetic-structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am. J. Bot. 82 (1995), 1420–1425.
Lourmas, M., Kjellberg, F., Dessard, H., Joly, H.I., Chevallier, M.-H., Reduced density due to logging and its consequences on mating system and pollen flow in the African mahogany Entandrophragma cylindricum. Heredity (Edinb) 99 (2007), 151–160.
Meunier, Q., Moumbogou, C., Doucet, J.-L., Les Arbres Utiles Du Gabon. 2015, Les Presses agronomiques de Gembloux, Gembloux, Belgium.
Micheneau, C., Dauby, G., Bourland, N., Doucet, J.-L., Hardy, O.J., Development and characterization of microsatellite loci in Pericopsis elata (Fabaceae) using a cost-efficient approach. Am. J. Bot. 98 (2011), e268–270.
Murawski, D.A., Hamrick, J.L., The effect of the density of flowering individuals on the mating systems of nine tropical tree species. Heredity (Edinb) 67 (1991), 167–174.
Ndiade Bourobou, D., Dynamique spatiale et temporelle de la diversité génétique d'une espèce rare en Afrique Centrale : Baillonella toxisperma Pierre (le Moabi). Ph.D., 2011, Montpellier Univ. Fr.
Ndiade Bourobou, D., Vaillant, A., Favreau, B., Gayrin, E., Bouvet, J.M., Isolation and characterization of 15 nuclear microsatellite markers for Baillonella toxisperma Pierre (Sapotaceae), a low-density tree species of Central Africa. Mol. Ecol. Resour. 9 (2009), 1135–1138.
Ndiade-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. Mol. Ecol. 19 (2010), 4949–4962.
Nei, M., Estimation of average heterozygosity and genetic distance for small number of individuals. Genetics 89 (1978), 583–590.
Nielsen, R., Tarpy, D.R., Kern Reeve, H., Estimating effective paternity number in social insects and the effective number of alleles in a population. Mol. Ecol. 12 (2003), 3157–3164.
Ouborg, N.J., Piquot, Y., Van Groenendael, J.M., Population genetics, molecular markers and the study of dispersal in plants. J. Ecol. 87 (1999), 551–568.
Ouédraogo, D.-Y., Beina, D., Picard, N., Mortier, F., Baya, F., Gourlet-Fleury, S., Thinning after selective logging facilitates floristic composition recovery in a tropical rain forest of Central Africa. For. Ecol. Manage. 262 (2011), 2176–2186.
Petit, R.J., Duminil, J., Fineschi, S., Hampe, A., Salvini, D., Vendramin, G.G., Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol. Ecol. 14 (2005), 689–701.
Plenderleith, K., Brown, N., Moabi (Baillonella toxisperma). Clark, L.E., Sunderland, T., (eds.) The Key Non-Timber Forest Products of Central Africa - State of the Knowledge, 2004, USAID, 186.
Ratnam, W., Rajora, O.P., Finkeldey, R., Aravanopoulos, F., Bouvet, J.-M., Vaillancourt, R.E., Kanashiro, M., Fady, B., Tomita, M., Vinson, C., Genetic effects of forest management practices: global synthesis and perspectives. For. Ecol. Manage. 333 (2014), 52–65.
Ritland, K., Extensions of models for the estimation of mating systems using n independent loci. Heredity (Edinb) 88 (2002), 221–228.
Robledo-Arnuncio, J.J., Austerlitz, F., Smouse, P.E., POLDISP: a software package for indirect estimation of contemporary pollen dispersal. Mol. Ecol. Notes 7 (2007), 763–766.
Van de Peer, Y., ZT: a software tool for simple and partial Mantel tests. J. Stat. Softw. 7 (2002), 1–12.
Vekemans, X., Hardy, O.J., New insights from fine-scale spatial genetic structure analyses in plant populations. Mol. Ecol. 13 (2004), 921–935.
Ward, M., Dick, C.W., Gribel, R., Lowe, A.J., To self, or not to self.. A review of outcrossing and pollen-mediated gene flow in neotropical trees. Heredity (Edinb) 95 (2005), 246–254.