Pollen and seed dispersal are key processes affecting the demographic and evolutionary dynamics of plant species and are also important considerations for the sustainable management of timber trees. Through direct and indirect genetic analyses, we studied the mating system and the extent of pollen and seed dispersal in an economically important timber species, Entandrophragma cylindricum (Meliaceae). We genotyped adult trees, seeds and saplings from a 400-ha study plot in a natural forest from East Cameroon using eight nuclear microsatellite markers. The species is mainly outcrossed (t = 0.92), but seeds from the same fruit are often pollinated by the same father (correlated paternity, r = 0.77). An average of 4.76 effective pollen donors (N ) per seed tree contributes to the pollination. Seed dispersal was as extensive as pollen dispersal, with a mean dispersal distance in the study plot approaching 600 m, and immigration rates from outside the plot to the central part of the plot reaching 40% for both pollen and seeds. Extensive pollen- and seed-mediated gene flow is further supported by the weak, fine-scale spatial genetic structure (Sp statistic = 0.0058), corresponding to historical gene dispersal distances (σ ) reaching approximately 1,500 m. Using an original approach, we showed that the relatedness between mating individuals (F = 0.06) was higher than expected by chance, given the extent of pollen dispersal distances (expected F = 0.02 according to simulations). This remarkable pattern of assortative mating could be a phenomenon of potentially consequential evolutionary and management significance that deserves to be studied in other plant populations.
Taxonomic classification based on morphology alone can prove difficult. This is the case of the polymorphic forest tree species Santiria trimera in Africa, whose classification has remained controversial for over a century. Studies combining chloroplast and nuclear DNA sequences show the existence of several phylogenetic clades in this taxon, with some occurring in sympatry in western Central Africa suggesting the existence of at least two species. By combining genetic and morphological markers, we aim to assess the species delimitation in the Santiria species complex. Morphological trait (trunk, leaflet, flower and fruit characteristics) analysis using 223 standing individuals and 103 herbarium samples were combined with genetic analyses using 479 individuals genotyped at eight microsatellite markers. Genetic clusters were identified using Bayesian assignment in order to delimit species following the Biological Species Concept and to identify distinctive characters from morphometric analyses in retrospect. Three genetic clusters were identified and found to occur in sympatry. The type of inflorescence and the colour of unripe fruit were the most discriminant morphological traits among those genetic clusters, while many quantitative traits showed overlapping distributions between genetic clusters and explain the difficulty encountered by previous botanists to resolve the taxonomy of Santiria. The combination of genetic and morphological data suggests the presence of three species within the taxon Santiria trimera from western Central Africa. This work should guide a taxonomic revision within the genus Santiria in Africa.
Combining genetic and morphological markers is a powerful approach for species delimitation, much needed in tropical species complexes. Greenwayodendron (Annonaceae) is a widespread genus of trees distributed from West to East African rainforests. Two species and four infra‐specific taxa are currently recognized. However, preliminary genetic studies and morphological observations suggested the occurrence of additional species, undescribed to date. We tested species delimitation within Greenwayodendron by combining morphological and population genetics data. First, a visual inspection of about a thousand specimens suggested the existence of seven morphogroups: four of them occur in Central Africa and overlap in Gabon while three others are allopatric, occurring respectively in West Africa, East Africa, and the islands of São Tomé and Príncipe. Their morphological differentiation was confirmed by analysis of 27 morphological characters coded from 233 herbarium specimens. Second, after genotyping 800 samples at eight nuclear microsatellites, Bayesian clustering analyses (STRUCTURE) identified four genetic clusters corresponding to the well‐sampled morphogroups but failed to separate the three remaining morphogroups represented by few samples. However, we show that this is an inherent limit of the STRUCTURE algorithm, whereas factorial correspondence analysis (FCA) and pairwise FST and RST measures confirmed the genetic differentiation of all morphogroups. We considered that a clear genetic differentiation occurring between sympatric populations advocates for recognizing distinct species following the biological species concept. Our analyses highlight that the current taxonomic treatment of Greenwayodendron underestimates the total number of species. We identified two new species and support separation at the rank of species of two varieties (G. suaveolens subsp. suaveolens var. gabonica, G. suaveolens subsp. suaveolens var. suaveolens) and one subspecies (G. suaveolens subsp. usambaricum). The taxonomic status of specimens collected in São Tomé and Príncipe remains inconclusive, partly due to the limited fertile material available. Our study highlights the strength of combining morphological and population genetics data for discovering new taxa. Guidelines for using genetic clustering approaches in species delimitation are provided.
Resolving phylogenetic relationships allows the investigation of how species diversity has evolved in various ecosystems. The genera Entandrophragma and Khaya consist of tree species distributed in different African biomes (lowland rain forest, dry forest and savanna, montane forest), and are suitable to examine how (single or multiple events) and when the processes of diversification led to biome transitions. Based on the sequencing of plastome (pDNA: c. 160,000 bp), ribosomal DNA (rDNA: c. 5,300 bp), and habitat characteristic data for each species, we have: (i) reconstructed phylogenetic relationships between species and estimated the divergence period between the main lineages, and (ii) reconstructed ancestral states regarding biome preferences. The phylogenetic trees obtained with both markers support monophyly of the five sections of Entandrophragma previously defined based on fruit and floral characters. Nevertheless, the position of some species from the pDNA and rDNA tree topologies varied within sections. In Khaya, pDNA and rDNA show very divergent topologies, possibly due to a more recent diversification involving incomplete lineage sorting and/or recurrent hybridization events. Khaya diversified during the Pliocene and Pleistocene according to both markers; whereas, according to rDNA data, the Entandrophragma sections diverged during the early Miocene and species within sections diverged from the late Miocene to the Pleistocene. Divergence date estimates tended to be more recent using pDNA data. Biome transitions could not be reconstructed in Khaya as the species tree remains unresolved. Contrarily, three independent biome transitions were inferred in Entandrophragma. The first transition from rain to dry forests occurred during the Miocene and two other transitions were inferred during the Pleistocene, one from rain forest to dry forest and another from rain forest to mountain forest. Overall, we demonstrate that multiple biome transitions occurred, starting from a rain forest biome, possibly reflecting the global trend of aridification of Africa throughout the Cenozoic.
Paleo-environmental data show that the distribution of African rain forests was affected by Quaternary climate changes. In particular, the Dahomey Gap (DG)a 200 km wide savanna corridor currently separating the West African and Central African rain forest blocks and containing relict rain forest fragmentswas forested during the mid-Holocene and possibly during previous interglacial periods, whereas it was dominated by open vegetation (savanna) during glacial periods. Genetic signatures of past population fragmentation and demographic changes have been found in some African forest plant species using nuclear markers, but such events appear not to have been synchronous or shared across species. To better understand the colonization history of the DG by rain forest trees through seed dispersal, the plastid genomes of two widespread African forest legume trees, Anthonotha macrophylla and Distemonanthus benthamianus, were sequenced in 47 individuals for each species, providing unprecedented phylogenetic resolution of their maternal lineages (857 and 115 SNPs, respectively). Both species exhibit distinct lineages separating three regions: 1. Upper Guinea (UG, i.e. the West African forest block), 2. the area ranging from the DG to the Cameroon volcanic line (CVL), and 3. Lower Guinea (LG, the western part of the Central African forest block) where three lineages co-occur. In both species, the DG populations (including southern Nigeria west of Cross River) exhibit much lower genetic diversity than UG and LG populations, and their plastid lineages originate from the CVL, confirming the role of the CVL as an ancient forest refuge. Despite the similar phylogeographic structures displayed by A. macrophylla and D. benthamianus, molecular dating indicates very contrasting ages of lineage divergence (UG diverged from LG since c. 7 Ma and 0.7 Ma, respectively) and DG colonization (probably following the Mid Pleistocene Transition and the Last Glacial Maximum, respectively). The stability of forest refuge areas and repeated similar forest shrinking/expanding events during successive glacial periods might explain why similar phylogeographic patterns can be generated over contrasting timescales. Piñeiro et al., 2017). Environmental barriers (e.g. dry corridors separating wet ecosystems) can impede the homogenization of species pools while favoring genetic divergence between conspecific populations, as recently shown for the Dahomey Gap (Demenou et al., 2017; Demenou et al., 2016; Iloh et al., 2017). The Dahomey Gap (hereafter DG) is a c. 200 km wide corridor (Demenou, 2018) dominated by open vegetation in eastern Ghana, Togo, Benin, and western Nigeria, which separates two major Guineo-Congolian forest blocks: Upper Guinea (hereafter UG), which extends from Sierra Leone to Ghana, and Lower Guinea
Seed and pollen dispersal are important for defining sustainable forest management practices. By reducing population density, selective logging could affect not only the seed production of timber species but also the selfing rate and the patterns of seed and pollen rains. To assess these risks, we characterized seed and pollen dispersal patterns and the fine-scale spatial genetic structure (FSGS) of Pericopsis elata, a gregarious, wind-dispersed legume tree which is highly logged in Central Africa and threatened by overexploitation. Eleven microsatellite markers were used to genotype 189 adults and 664 seedlings in a 4 km 2 plot in the Democratic Republic of Congo (DRC). According to the neighbourhood model, seed dispersal was extremely leptokurtic, with 80% of seeds dispersal distances <75 m, 15% >500 m. Pollen dispersal was locally more extensive (median distance 260 m), but pollen immigration was not detected, and the selfing rate (54%) appeared particularly high compared to other tropical tree species. Limited gene dispersal resulted in remarkably high FSGS (S p = 0.072). A decay of inbreeding with age also suggests that the species is prone to inbreeding depression. The reproductive success of trees was positively related to their diameter at breast height (dbh), with half of the progeny mothered by trees with dbh > 97 cm and fathered by trees with dbh > 119 cm. Our study highlights that (1) seed sources must be diversified for plantation or population reinforcement to limit consanguinity, and (2) the legal minimum cutting diameter in DRC (60 cm) should be increased to maintain enough post-logging reproductive potential.
Par la qualité de leur bois et leurs nombreux usages traditionnels, les espèces du genre Entandrophragma font l’objet d’une intense exploitation, susceptible de compromettre leur pérennité en l’absence de gestion durable. La présente étude dresse un état de la situation de cinq espèces commerciales principales de ce genre : Entandrophragma angolense, E. congoense (souvent assimilée par erreur à E. angolense), E. candollei, E. cylindricum et E. utile. Elle propose des pistes de recherche pour améliorer les stratégies de gestion durable au sein de ce genre. L’étude est principalement basée sur les données scientifiques (publications), économiques (statistiques de production et d’exportation) et juridiques (lois et réglementations), mais aussi sur les plans d’aménagement et les rapports d’inventaire. Les connaissances sur leur gestion sont encore fragmentaires alors qu’elles sont considérées comme vulnérables dans la liste rouge de l’UICN. La forte exploitation industrielle ou artisanale de ces espèces ne s’effectue pas toujours dans le respect d’un plan d’aménagement validé, ni de la durée minimum des rotations qui permettraient l’un et l’autre un taux de reconstitution pérennisant cette ressource. Leur gestion durable exige notamment le développement et le respect de mesures d’aménagement pour rendre leur exploitation renouvelable à long terme. Cette exploitation doit s’appuyer sur une gestion adéquate des peuplements naturels et sur le reboisement ainsi que sur des mesures de conservation. Les recherches à développer doivent intéresser leur vitesse de croissance face aux évolutions climatiques, l’évaluation de leurs stocks (production, biomasse, carbone), l’actualisation de leur distribution spatiale, l’amélioration de leur régénération naturelle, les processus de leur reproduction, leurs propriétés anatomiques et technologiques, autant de pistes pertinentes pour garantir la pérennité des espèces exploitables du genre Entandrophragma.
Interpreting morphological variability in terms of species delimitation can be challenging. However, correcting species delineation can have strong implications for the sustainable management of exploited species. Up to now, species delimitation between two putative timber species from African forests, Entandrophragma congoense and E. angolense, remained unclear. To investigate their differences, we applied an integrated approach which combines morphological traits and genetic markers. We characterized 13 morphological characters from 81 herbarium specimens and developed 15 new polymorphic microsatellite markers to genotype 305 samples (herbarium samples and specimens collected in the field across the species distribution ranges). Principal Component Analysis (PCA) of morphological data and Bayesian clustering analyses of genetic data were used to assess differentiation between putative species. These analyses support two well-differentiated groups (FST = 0.30) occurring locally in sympatry. Moreover, these two groups present distinct morphological characters at the level of the trunk, leaflets and seeds. Our genetic markers identified few individuals (4%) that seem to be hybrids, though there is no evidence of genetic introgression from geographic patterns of genetic variation. Hence, our results provide clear support to recognize E. congoense as a species distinct from E. angolense, with a much lower genetic diversity than the latter, and that should be managed accordingly. This work highlights the power of microsatellite markers in resolving species boundaries.
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