[en] How the Central African rain forests have been affected by climatic fluctuations of the Quaternary remains debated. Phylogeographical studies have shown that tree species from western Central Africa often display spatially congruent genetic discontinuities, supporting the hypothesis that the forest was previously fragmented. Extensive seed dispersal is expected to accelerate the admixture between gene pools but most of the species studied so far have presumably limited seed dispersal abilities. Here, we genotyped 15 nuclear and three plastid microsatellite markers in a low-density Central African tree species with long-distance seed dispersal: Baillonella toxisperma (Sapotaceae). While plastid markers revealed a weak structure in Cameroon, nuclear markers highlighted three genetic clusters: two distributed in Cameroon and separating Atlantic coastal forests from the inland forests, and one cluster occurring in Gabon. Substantial genetic differentiation with a phylogeographical signal was detected only between Cameroonian and Gabonese populations, suggesting two major genetic clusters located approximately North and South of the equatorial climatic hinge. Genetic differentiation was very low between the clusters within Cameroon. This pattern could be partially explained by the climate niche distribution modelling applied on the Last Glacial Maximum (LGM) which predicts a unique remnant population per country. The deep North-South differentiation in a species with long-distance seed dispersal supports the hypothesis that Central African rain forests have been fragmented at the height of the equator during a substantial part of the Quaternary.
Allal F, Sanou H, Millet L, Vaillant A, Camus-Kulandaivelu L, Logossa ZA, Lefèvre F, Bouvet JM (2011) Past climate changes explain the phylogeography of Vitellaria paradoxa over Africa. Heredity 107:174–186
Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J Appl Ecol 43:1223–1232
Anhuf D, Ledru MP, Behling H, Da Cruz FW, Cordeiro RC, Van der Hammen T, Karmann I, Marengo JA, De Oliveira PE, Pessenda L, Siffedine A (2006) Paleo-environmental change in Amazonian and African rainforest during the LGM. Palaeogeogr Palaeocl 239:510–527
Araújo MB, New M (2007) Ensemble forecasting of species distributions. Trends Ecol Evol 22:42–47
Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Blatrix R, Peccoud J, Born C, Piatscheck F, Benoit L, Sauve M, Djiéto-Lordon C, Atteke C, Wieringa JJ, Harris DJ, McKey D (2017) Comparative analysis of spatial genetic structure in an ant–plant symbiosis reveals a tension zone and highlights speciation processes in tropical Africa. J Biogeogr 44:1856–1868
Born C, Alvarez N, McKey D, Ossari S, Wickings EJ, Hossaert-McKey M, Chevallier M-H (2011) Insights into the biogeographical history of the Lower Guinea Forest domain: evidence for the role of refugia in the intraspecific differentiation of Aucoumea klaineana. Mol Ecol 20:131–142
Bousquet J, Simon L, Lalonde M (1990) DNA amplification from vegetative and sexual tissues of trees using polymerase chain reaction. Can J For Res 20:254–257
Campagne P, Smouse PE, Varouchas G, Silvain JF, Leru B (2012) Comparing the van Oosterhout and Chybicki-Burczyk methods of estimating null allele frequencies for inbred populations. Mol Ecol Resour 12:975–982
Castellanos-Morales G, Gutiérrez-Guerrero YT, Gámez N, Eguiarte LE (2016) Use of molecular and environmental analyses for integrated in situ and ex situ conservation: the case of the Mexican prairie dog. Biol Conserv 204:284–295
Chen C, Durand E, Forbes F, François O (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol Ecol Notes 7:747–756
Chybicki IJ, Burczyk J (2009) Simultaneous estimation of null alleles and inbreeding coefficients. J Heredity 100:106–113
Daïnou K, Bizoux JP, Doucet J-L, Mahy G, Hardy OJ, Heuertz M (2010) Forest refugia revisited: nSSRs and cpDNA sequences support historical isolation in a wide-spread African tree with high colonization capacity, Milicia excelsa (Moraceae). Mol Ecol 19:4462–4477
Daïnou K, Mahy G, Duminil J, Dick C, Doucet J-L, Donkpégan ASL, Pluijgers M, Sinsin B, Lejeune P, Hardy OJ (2014) Speciation slowing down in widespread and long-living tree taxa: insights from the tropical timber tree genus Milicia (Moraceae). Heredity 113:74–85
Daïnou K, Blanc-Jolivet C, Degen B, Kimani P, Ndiade-Bourobou D, Donkpegan ASL, Tosso F, Kaymak E, Bourland N, Doucet J-L, Hardy OJ (2016) Revealing hidden species diversity in closely related species using nuclear SNPs, SSRs and DNA sequences–a case study in the tree genus Milicia. BMC Evol Biol 16:259
Dauby G, Duminil J, Heuertz M, Hardy OJ (2010) Chloroplast DNA polymorphism and phylogeography of a Central African tree species widespread in mature rainforests: Greenwayodendron suaveolens (Annonaceae). Trop Plant Biol 3:4–13
Dauby G, Duminil J, Heuertz M, Koffi G, Stevart T, Hardy OJ (2014) Congruent phylogeographical patterns of eight tree species in Atlantic Central Africa provide insights into the past dynamics of forest cover. Mol Ecol 23:2299–2312
Dauby G, Zaiss R, Blach-Overgaard A, Catarino L, Damen T, Deblauwe V, Dessein S, Dransfield J, Droissart V, Duarte MC, Engledow H (2016) RAINBIO: a mega-database of tropical African vascular plants distributions. PhytoKeys 74:1–18
Debout GD, Doucet JL, Hardy OJ (2011) Population history and gene dispersal inferred from spatial genetic structure of a Central African timber tree, Distemonanthus benthamianus (Caesalpinioideae). Heredity 106:88–99
Debroux L (1998) 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. Thèse de doctorat. Faculté universitaire des sciences agronomiques de Gembloux
Debroux L, Delvingt W, Mbolo M, Amougou A (1998) Régénération du moabi et du mukulungu au Cameroun: perspectives pour l’aménagement. Bois For Trop 255:5–17
Demenou B, Piñeiro R, Hardy OJ (2016) Origin and history of the Dahomey gap separating West and Central African rain forests: insights from the phylogeography of the legume tree Distemonanthus benthamianus. J Biogeogr 43:1020–1031
Demesure B, Sodzi N, Petit R (1995) A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 4:129–134
Dolezel J, Binarova P, Lucretti S (1989) Flow cytometry was used to analyse the DNA content of nuclei isolated from plant tissues and from callus and cell suspension cultures in vitro. Biol Plantarum 62:113–120
Duminil J, Caron H, Scotti I, Cazal SO, Petit RJ (2006) Blind population genetics survey of tropical rainforest trees. Mol Ecol 15:3505–3513
Duminil J, Heuertz M, Doucet JL, Bourland N, Cruaud C, Gavory F, Doumenge C, Navascués M, Hardy OJ (2010) CpDNA-based species identification and phylogeography: application to African tropical tree species. Mol Ecol 19:5469–5483
Dupont LM, Jahns S, Marret F, Ning S (2000) Vegetation change in equatorial West Africa: time-slices for the last 150 ka. Palaeogeogr Palaeocl 155:95–122
Estoup A, Angers B (1998) Microsatellites and minisatellites for molecular ecology: theoretical and empirical considerations. In: Carvalho GR (ed) Advances in molecular ecology. IOS Press, Amsterdam
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Faye A, Deblauwe V, Mariac C, Richard D, Sonké B, Vigouroux Y, Couvreur TLP (2016) Phylogeography of the genus Podococcus (Palmae/Arecaceae) in Central African rain forests: climate stability predicts unique genetic diversity. Mol Phylogenet Evol 105:126–138
Fielding AH, Bell JF (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24:38–49
Fourcade Y, Engler JO, Rödder D, Secondi J (2014) Mapping species distributions with MAXENT using a geographically biased sample of presence data: a performance assessment of methods for correcting sampling bias. PLoS One 9:e97122
François O, Durand E (2010) Spatially explicit Bayesian clustering models in population genetics. Mol Ecol Resour 10:773–784
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 (1985) Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65:324–337
Guillot G, Estoup A, Mortier F, Cosson JF (2005) A Spatial Statistical Model for Landscape Genetics. Genetics 170 (3):1261–1280
Gonmadje CF, Doumenge C, Sunderland TCH, Balinga MPB, Sonké B (2012) Analyse phytogéographiques des forêts d'Afrique Centrale: le cas du massif de Ngovayang (Cameroun). Plant Ecol Evol 145:152–164
Grivet D, Heinze B, Vendramin G, Petit R (2001) Genome walking with consensus primers: application to the large single copy region of chloroplast DNA. Mol Ecol Notes 1:345–349
Gutiérrez-Tapia P, Palma RE (2016) Integrating phylogeography and species distribution models:cryptic distributional responses to past climate change in an endemic rodent from the Central Chile hotspot. Divers Distrib 22:638–650
Hardy OJ, Vekemans X (2002) Spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Hardy OJ, Charbonnel N, Fréville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482
Hardy OJ, Born C, Budde K, Daïnou K, Dauby G, Duminil J, Ewédjé EEB, Gomez C, Heuertz M, Koffi GK, Lowe AJ, Micheneau C, Ndiade-Bourobou D, Piñeiro R, Poncet V (2013) Comparative phylogeography of African rain forest trees: a review of genetic signatures of vegetation history in the Guineo-Congolian region. Compt Rendus Geosci 345:284–296
Heikkinen RK, Luoto M (2006) Methods and uncertainties in bioclimatic envelope modelling under climate change. Prog Phys Geogr 6:751–777
Heuertz M, Duminil J, Dauby G, Savolainen V, Hardy OJ (2014) Comparative phylogeography in rainforest trees from Lower Guinea, Africa. PLoS One 9:e84307
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978
Ikeda DH, Max TL, Allan GJ, Lau MK, Shuster SM, Whitham TG (2017) Genetically informed ecological niche models improve climate change predictions. Glob Chang Biol 23:164–176
Iturbide M, Bedia J, Herrera S, del Hierro PO, Gutiérrez JM (2015) A framework for species distribution modelling with improved pseudo-absence generation. Ecol Model 312:166–174
Jakobsson M, Rosenberg NA (2007) Clumpp: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806
Janes JK, Miller JM, Dupuis JR, Malenfant RM, Gorrell JC, Cullingham CI, Andrew RL (2017) The K = 2 conundrum. Mol Ecol 26:3594–3602
Knowles L, Alvarado-Serrano DF (2010) Exploring the population genetic consequences of the colonization process with spatio-temporally explicit models: insights from coupled ecological, demographic and genetic models in montane grasshoppers. Mol Ecol 19:3727–3745
Lam NSN (1983) Spatial interpolation methods: a review. Am Cartographer 10:129–150
Letouzey R (1985) Notice de la carte phytogeographique du Cameroun au 1:500,000. Institut de la carte internationale de la végétation. Toulouse, France
Levinsky I, Araújo MB, Nogués-Bravo D, Haywood AM, Valdes PJ, Rahbek C (2013) Climate envelope models suggest spatio-temporal co-occurrence of refugia of African birds and mammals. Glob Ecol Biogeogr 22:351–363
Lowe A, Gillies A, Wilson J, Dawson I (2000) Conservation genetics of bush mango from Central/West Africa: implications from random amplified polymorphic DNA analysis. Mol Ecol 9:831–841
Maley J (1996) The African rain forest - main characteristics of changes in vegetation and climate from the Upper Cretaceous to the Quaternary. In: Alexander IJ, Swaine MD, Watling R (eds) Essays on the ecology of the Guinea-Congo rain forest. The Royal Society of Edinburgh, Edinburgh, pp 31–73
Maley J (1997) Middle to Late Holocene changes in tropical Africa and other continents: paleomonsoon and sea surface temperature variations. In: Dalfes HN, Kukla G, Weiss H (eds) Third millennium BC climate change and Old World collapse. Springer, Berlin, pp 611–640
Migliore J, Kaymak E, Mariac C, Couvreur TL, Lissambou BJ, Piñeiro R, Hardy OJ (2018) Pre-Pleistocene origin of phylogeographical breaks in African rain forest trees: new insights from Greenwayodendron (Annonaceae) phylogenomics. J Biogeogr. 10.1111/jbi.13476
Naimi B, Araújo MB (2016) Sdm: a reproducible and extensible R platform for species distribution modelling. Ecography 39:368–375
Ndiade-Bourobou D, Vaillant A, Favreau B, Gayrin E, Bouvet J-M (2009) Isolation and characterization of 15 nuclear microsatellite markers for Baillonella toxisperma Pierre (Sapotaceae), a low-density tree species of Central Africa. Mol Ecol Resour 9:1135–1138
Ndiade-Bourobou D, Hardy OJ, Favreau B, Moussavou H, Nzengue E, Mignot A, Bouvet J-M (2010) 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 19:4949–4962
Piñeiro R, Dauby G, Kaymak E, Hardy OJ (2017) Pleistocene population expansions of shade-tolerant trees indicate fragmentation of the African rainforest during the Ice Ages. Proc R Soc B 284
Plenderleith K, Brown N (2000) Baillonella toxisperma: a state of knowledge study. Oxford Forestry Institute (Oxford University), Oxford
Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Puechmaille SJ (2016) The program does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Molecular Ecology Resources 16 (3):608–627
QGIS Development Team (2018) QGIS geographic information system. Open Source Geospatial Foundation Project. http://qgis.osgeo.org
Riul P, Targino CH, Júnior LAC, Creed JC, Horta PA, Costa GC (2013) Invasive potential of the coral Tubastraea coccinea in the Southwest Atlantic. Mar Ecol Prog Ser 480:73–81
Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94:275–288
Singer A, Schückel U, Beck M, Bleich O, Brumsack HJ, Freund H, Geimecke C, Lettmann KA, Millat G, Staneva J, Vanselow A (2016) Small-scale benthos distribution modelling in a North Sea tidal basin in response to climatic and environmental changes (1970s-2009). Mar Ecol Prog Ser 551:13–30
Thuiller W, Lafourcade B, Engler R, Araújo MB (2009) BIOMOD - a platform for ensemble forecasting of species distributions. Ecography 32:369–373
Thuiller W, Georges D, Engler R (2014) Biomod2: ensemble platform for species distribution modeling. http://CRAN.Rproject.org/package=biomod2
Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935
Verity R, Nichols RA (2016) Estimating the number of subpopulations (K) in structured populations. Genetics 203:1827–1839
Vinceti B, Loo J, Gaisberger H, van Zonneveld MJ, Schueler S, Konrad H, Kadu CA, Geburek T (2013) Conservation priorities for Prunus africana defined with the aid of spatial analysis of genetic data and climatic variables. PLoS One 8:e59987
Wakasugi T, Sugita M, Tsudzuki T, Sugiura M (1998) Updated gene map of tobacco chloroplast DNA. Plant Mol Biol Rep 16:231–241
Weising K, Gardner RC (1999) A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42:9–19
White F (1986) La Vegetation de L’Afrique (the vegetation of Africa), Vol 20. IRD Editions (France)
