ABSTRACT
The genetic diversity of African forest resources is poorly documented while it can be the basis for adapting these resources to climatic variations. This study aimed to characterize the genetic diversity of the Acacia senegal (L.) Willd in its natural range in Niger. 252 individuals from 10 populations of the species, across three gum basins were analyzed with 9 nuclear microsatellite markers. Genetic diversity indexes are high in all the populations studied: number of allele (Na) varies from 4.00 to 5.44; allele richness (R) varies from 3.42 to 4.49; observed heterozygosity (Ho) and expected heterozygosity (He) range from 0.44 to 0.56 and from 0.46 to 0.63, respectively. The values of differentiation index (Fst) per pair of population range from 0.0057 to 0.110 and 20% of these values are not significant indicating a low differentiation between populations. In addition, Molecular Variance Analysis shows that 93% of total variation is within populations. Through Bayesian model, a structure of population into three groups is observed. These results could form the basis for building sustainable management and conservation strategies of genetic resources of A. senegal in Niger.
Key words: Genetic diversity, microsatellites, Acacia senegal, climate change, Niger.
The major challenge of biological conservation is the preservation of genetic diversity in the maintenance of the evolutionary process of species (Assogbadjo et al., 2006). Using genetic data to determine evolutionary relationships between species and populations signifi-cantly contributes to their conservation (Chiveu et al., 2008). Genetic variation in several trees species on earth is a trans-generational resource of great social, economic and environmental importance. Commonly referred to as "forest genetic resources", these variations are expressed by differences between species, populations, and individuals or chromosomes and have an actual or potential value (Young et al., 2001).
The management of forest genetic resources has caused serious national and international concern over the past few years due to overexploitation and unfavorable climatic conditions which have led to severe degradation of ecosystems. This phenomenon affects particularly the Sahelian region including Niger.
Among African forest species, Acacia senegal (L.) Willd. has a wide distribution in the arid and semi-arid regions of Africa, from South Africa northwards to Sudan (Maydell, 1983), because it tolerates aridity and eroded soils (Raddad et al., 2005; Chiveu et al., 2008). A. senegal (L.) Willd is a leguminous multipurpose species belonging to the subgenus Aculeiferum (Arce and Blanks, 2001). The international botanical community accepts the retypifying Acacia with a new type which would place most species ascribed to the present subgenus Aculeiferum into the genus Senegalia (Boatwright et al., 2014; Kyalangalilwa et al., 2013; Haddad, 2011).
In Niger, A. senegal is distributed along a climatic gradient between the isohyets 620 and 250 mm (Elhadji et al., 2012, 2016), forming a band from west to east and of which three gum basins are distinct (western basin, central basin and eastern basin) (FAO, 2003). However, since the droughts of 1974 and 1982, natural stands of A. senegal are constantly degrading under combined effects of anthropogenic actions and climatic variability (Amani, 2010). The deforestation of the natural stand of the gum groves for installation of crop fields, the exploitation of wood for domestic energy and mutilation of trees to feed animals constitute some factors of deterioration (Ichaou, 2008). In addition to the aforementioned factors, aging of trees, their high mortality and low capacity of regeneration are added (Maisharou and Nourou, 2004). Indeed, the natural stand regeneration, which is mainly done by seeds coming from the trees in situ, would depend on the maintenance of genetic diversity of the populations. The genetic diversity would also help to cope with unpredictable climatic changes or to establish breeding programs (Blanc et al., 1999). It is important to know the structure of genetic diversity which constitutes the partition of variation between different populations and which could be their capacity to adapt to environmental changes.
While the importance of A. senegal in rural economy (Guinko et al., 1996) and soil stabilization and fertility (Abdou et al., 2013; Wickens et al., 1995) is undeniable, the importance of genetic diversity of natural populations in Niger is still very poorly studied. The knowledge of the partitioning of genetic variation within species is a prerequisite for defining strategies for conservation, management and sustainable use of the species' resources. The main objective of the study is to analyze the genetic diversity and structure of the natural stands of A. senegal in Niger through (i) the quantification of genetic diversity within each population, (ii) the determination of genetic structure of populations and (iii) the estimation of gene flow between these populations.
Presentation of study sites
The study is conducted in the three basins of gum arabic production in Niger, namely western basin, central basin and eastern basin (Figure 1). The sites of western basin (Kiki, Kokoyé, Tempena and Bégorou) are characterized by a Sahelian climate with two seasons (a rainy season from June to October and a dry season from November to May) with rainfall varying between 620 and 400 mm. For the sites of the central basin (Aseye, Dakoro and Bader), the annual rainfall varies between 400 and 350 mm and the climate is Sahelo-Saharan with a long dry season (9 months) and a short rainy season. In the sites of the eastern basin (Malam Mainari, Gouré and Nguel kolo), annual rainfall varies between 300 and 250 mm and this site is characterized by a dry climate (a long dry season and rainy season hardly reaching 3 months in the year). In all the sites, the vegetation consists of woody species: Acacia tortilis, Acacia seyal, Acacia laeta, Acacia dudgeoni, Balanites aegyptiaca, Boscia senegalensis, Combretun glutinosum, Combretum micratum, Calotropis procera, Leptadenia pyrotechnica, Maerua crassifolia, Ziziphus mauritiana, Tamarandis indica and Herbaceous: Alysicarpus avalifolius, Cyperus indica, Eragrostris tremula, Acanthospermum hispidum, Cenchrus biflorus. But A. senegal is dominant. The highest average daily temperature (38.50°C) is observed to the east and north center of Niger, corresponding to the sites of the eastern and central basins in April and May of the year. While in the west, it varies between 35 and 36.50°C (western basin).
Sampling
Ten natural A. senegal populations scattered in the three gum basins were sampled (Figure 1 and Table 1). The number of sample per population and basin is consigned in Table 1. A total of 252 trees (young and adult) distant at least 50 m fresh leaves were collected to avoid sampling related to trees. Such a sampling plan makes it possible to capture the maximum of variability within a population. Leaf samples were dried using silica gel before shipment to the genetics laboratory of the IRD (Niamey) representation in Niger.
DNA extraction and SSR marker analysis
DNA was extracted from 0.5 g of dried leaves using the protocol described by Ky et al. (2000). The quality of DNA was assessed by electrophoresis on a 1% agarose gel and quantified using a nano-drop spectrophotometer (ND1000, Thermo Scientific, USA) at Center for Medical Research and Sanitary (CERMES) in Niamey, Niger. Nine nuclear SSR markers (mAsCIRB10, mAsCIRC07, mAsCIRE06, mAsCIRE07, mAsCIRE10, mAsCIRF02, mAsCIRF03, mAsCIRH01 and mAsCIRH09) developed in A. senegal var. senegal by Assoumane et al. (2009) were used for diversity analysis. The 252 samples were genotyped at the ICRISAT Plant Genetics Laboratory in India.
Data analysis and statistical test
Genetic diversity
The following five parameters were used to quantify genetic diversity in the studied populations: Number of alleles per locus (Na), Allelic richness (R); this parameter determines the mean number of alleles taking into account sample size, which conditions the number of alleles observed in the population, observed heterozygosity (Ho), expected heterozygosity (He), and Wright (1965) fixation index (Fis). Fstat software 2.9.3 (Goudet, 2001) was used to calculate these diversity parameters.
Population’s genetic structure
Four methods of analysis were used: (1) Fst calculation using Fstat 2.9.3 software (Goudet, 2001); (2) genetic distance tree using Darwin 5.0.85 software (Perrier and Jacquemond-Collet, 2006); (3) Bayesian model using STRUCTURE 2.3.1 software (Pritchard et al., 2000) and (4) Analysis of Molecular Variance Analysis) (AMOVA) using the GenAlEx 6.5 program (Peakall and Smouse, 2012).
Fst calculation: The significance of Fst values were tested at the 5% threshold after 1000 permutations of alleles within populations.
Gene flow between populations was estimated by the indirect method based on the assumption of mutation-drift equilibrium. The number of migrants per generation (Nm) is calculated from the average of Shannon diversity index. The calculation was done with the GenAlEx version 6.5 software (Peakall and Smouse, 2012) according to the following classical formula:
Fst: index of population differentiation.
Genetic distance tree: Jaccard’s distance was used to calculate the matrix of genetic distances because some individuals had more than two alleles for a locus. Jaccard's distance makes it possible to obtain an unbiased estimate of the genetic distance between individuals, as it does not consider the absence of the allele (0) as a similarity. It is calculated by the following formula:
where dij = dissimilarity between two units i and j; a = number of variables for which xi = presence and xj = presence; b = number of variables for which xi = presence and xj = absence; c = number of variables for which xi = absence and xj = presence; xi and xj being the values of the variables for units i and j.
A Neighbour-Joining genetic distance tree (Saitou and Nei, 1987) was constructed from the genetic distance matrix for all samples.
Bayesian model: The genetic structure was also described by a Bayesian model using the software STRUCTURE 2.3.1 (Pritchard et al., 2000). In the STRUCTURE program, the admixture correlated allele model was used. This model assumes that all individuals share common ancestors and that alleles are correlated within populations. Thirteen “runs” were made to test independent K-values using 400,000 MCMC (Markov Chain Monte Carlo) and
40,000 burn-in periods.
Analysis of Molecular Variance (AMOVA): The distribution of genetic variation was evaluated specifying that the population groups constituting the three basins. AMOVA applied formula is:
where AR = Estimated variance among basins; AP = Estimated variance among populations; AI = Estimated variance among individuals; and WI = Estimated variance within individuals.
Genetic diversity
The diversity parameters data are shown in Table 2. The number of alleles per locus (Na) varies from 4 (Gouré) to 5.44 (Aseye). The allelic richness (R) varies from 3.42 (Gouré) to 4.49 (Tempena). The heterozygosis is also higher in Tempena (He = 0.63, Ho = 0.56) and lower in Goure (He = 0.46; Ho = 0.46). These parameters (Na, R, Ho and He) reveal a fairly high genetic diversity in the natural populations studied. The fixation index (Fis) is different from zero and positive in all populations except in Bégorou, N'guelKolo, Dakoro and Gouré populations, where Fis is not significantly different from zero. The overall value of Fis is 0.104 and is significantly different from zero.
Genetic structure
Differentiation detected by Fst
Table 3 presents the matrix of differentiation index (Fst) calculated by population pair. The populations of same gum basin have low Fst values that are not often significant at the 5% threshold. The overall Fst is 0.059; this reflects moderate differentiation according to Wright's ranking. In addition, overall average number of migrants (Nm) per generation is 3.288. It is high between populations in same basin and moderately low between populations of different basins (Table 4).
Structure detected by genetic distance tree
The individual genetic distance tree of the Neighbour-Joining type (Saitou and Nei, 1987) presents a low individualization of branches. However, almost 3 distinct groups can be observed corresponding to 3 gum basins and two pools gathering individuals from all the basins (Figure 2).
Structure detected by Bayesian model
For K = 3, the model highlights three groups corresponding exactly to 3 gum basins (Figure 3). Nevertheless, in each group, individuals with a genetic proportion coming from the neighbouring groups were observed.
When using a K = 2 value to evaluate population structure, populations of western basin and central basin formed a single group and eastern basin populations form a second group (Figure 4).
Genetic variability partitioning by AMOVA
The AMOVA showed that 83% of variation is within individuals, 10% between individuals, 2% between populations and 5% between basins (Table 5).
The distribution of forest tree species has a major impact on the extent of their genetic variability and structure. A. senegal is widely distributed in Niger, from west to east forming a broad band in which three large gum basins were singled. In this study, the populations of these gum basins have a fairly high mean genetic diversity (Ho = 0.48, He = 0.54) compared to values found for other forest species analyzed with the same types of markers (Table 6). Genetic diversity in A. senegal species is higher than average genetic diversity of tropical trees (He = 0.211) and conifers (He = 0.207) (Borgel et al., 2003). However, the genetic diversity observed in A. senegal is lower than that found in Acacia mangium (He = 0.70) by Butcher et al. (2000) or in A. senegal var. kerensi (He =0.63-0.70) by Omondi et al. (2009).
The fixation index (Fis) indicated a deficiency in hetero-zygosity from expected results under the assumptions of Hardy Weinberg. A positive value of Fis indicates a heterozygosity deficiency relative to the panmictic balance. A deficiency in heterozygosity can be explained mainly by 3 factors (Assoumane, 2011; Mohamed et al., 2010; Jordana, 2003): breeding regime that does not favor cross-breeding, existence of null alleles and effect of Wahlund. Indeed, for crossbreeding between relatives, it is well known that inbreeding (mating between an individual and his ascendants, his collaterals and/or his descendants) modifies the genotypic frequencies resulting in loss of genetic variability over generations. The second factor may be inherent to the existence of null alleles for some loci. Null alleles are alleles which do not amplify during polymerase chain reaction (PCR) due to mutation in the binding of the primer region. Then, individuals are considered homozygous for these loci, while they are heterozygous and this phenomenon would reduce the number of heterozygous. The last factor refers to the presence of subpopulations within populations considered (substructure) can induce Wahlund effect. The presence of null alleles was not tested in our data. Nevertheless, a Wahlund effect can be assumed because at Aseye population where two groups distant about 10 km were sampled, a Fis value (Fis = 0.131) was found which is significant at the 1% threshold. Then the two groups can be considered as different populations. The Fis (0.104) is comparable to that Fis (0.08) measured by Assoumane et al. (2012) and significantly different from zero in a population of A. dudgeoni (Dogona) in the western areas of Niger.
The Fst calculated among all populations (Fst = 0.059) indicates moderate differentiation among populations. In addition, Fst observed in the study is comparable to those found in Table 6 in forest species with same markers. The genetic differentiation level is due to the existence of gene flow among populations.
The importance of gene flow between populations could be explained by the mode of seed dispersal and the presence of pollinators. Seed dispersal of A. senegal can be ensured by wind (anemophilic mode) after dehiscence of the pods. The socio-economic role of A. senegal in rural households (gum arabic) could also contribute to the exchange of plant from region to another and village to another (Ichaou, 2008). In addition to human action (anthropozoic mode), animals through grazing also contribute significantly to gene flows among A. senegal populations. Indeed, most of the studied populations constitute grazing areas for transhumant herders moving from one point to another and facilitating seed dissemination.
According to Kremer et al. (2012) and Buckley et al. (2010), improved forest species adaptation to changes in environmental conditions is better when there is more gene flow between populations up. For Slatkin (1987), a low gene flow (Nm<1) results from local differentiation that leads to genetic drift and a higher gene flow (Nm>1) makes population adjustment for survival. Values of 1 to 10 migrants per generation are essential for restoration and resistance to genetic drift and prevention of natural selection (Blanquart and Gandon, 2011; Lopez et al., 2009). In ours study, the average number of migrants per generation (Nm) is 3.288 and high Nm are observed between populations in the same gum basin. Low Nm is recorded between the most geographically distant populations: Kokoyé-Malan Mainari with Nm = 0.993 and Tempena-N'guelkolo with Nm = 0.857. Indeed, populations of low Nm are spaced further by 1500 km, which would probably reduce gene flow between them.
The total variability is explained by intra-population variation (93%) and 2 and 5% of variability are attributed, respectively to variations among populations and among gum basins. This result, which confirms that of Fst, is in agreement with Chavallier and Borgel (unpublished results), who observed that most genetic variability in higher plants and particularly in woody plants is within Populations (Fst = 8.45%). However, Rathore et al. (2016) observed in 11 populations of Gymnema sylvestre contrary results. These authors found a strong genetic differentiation of populations of the species (Fst = 70%) and low gene flow (Nm = 0.21) through SSR markers. Their results are explained by the great geo-graphical distance between populations studied, which created a geographic isolation limiting the possibilities of gene flow among populations.
With STRUCTURE program, individuals group by basin mainly due to small difference between populations that constitute the gum basin.
Geographical proximity promotes gene flow between populations of the same basin. This is confirmed for k = 2, where we got the grouping of populations of western basin and those of central basin in the same group. The assignment of populations of two gum basins in a group is probably due to gene flow favored by low geographical distance between them.
Implications for sustainable management and conservation of the species
The assessment of genetic variability among and within forest tree populations is a prerequisite for any restoration or renewal of these species (William and Hamrick, 1996). From results of this study, we can say that conservation of the species in Niger could be done easily through the method of in situ conservation. However, the species is threatened by human actions related to abuse of natural resources and degradation of its habitat. Effective and rigorous measures are needed to reverse current trends, because if nothing is done, it will inevitably lead to the disappearance of several populations of the species and these resources. The organization of genetic variability in the species revealed in this study is an important parameter to include in any future sustainable management strategy. Two aspects are of primary importance for the implementation of in situ conservation programs: local pedoclimatic conditions of origin and genetic diversity within the species. Indeed, the inclusion of these aspects would avoid the lack of seed germination, seedling mortality and/or long term loss. The effective management of genetic resources requires the identification of priority areas where conservation efforts can be better focused. Structuring by gum basin identified in our study helps to retain basin scale as an in situ conservation unit. Any time, if needed, seeds from western basin can be used to repopulate populations of central basin and vice versa, because there is a similarity (low differentiation) between the two gum basins.
Knowledge of genetic diversity and its partitioning within the species is essential to build any strategy for management and sustainable conservation of natural resources. In this study, a relatively high genetic diversity was found in natural populations of A. senegal. The bulk of genetic variability in the species is within populations. The populations belonging to the same gum basin are similar, resulting from gene flows between them. The interpretation of individual’s differentiation within populations assumed a Whalund effect. Further studies need to be conducted to confirm this factor or to explore other factors explaining the deficit in heterozygote’s observed in more than half of the studied populations.
These results could be used as part of the restoration of degraded lands and rangelands through the plantation of A. senegal performed annually by the environmental services, development programs and projects and national, international non-governmental organizations (NGOs). It is recommended to use the seeds from the populations of the catchment area of the intervention zone to set up the nurseries.
The authors have not declared any conflict of interests.
REFERENCES
|
Abdou MA, Zoubeirou AM, Kadri A, Ambouta JMK, Dan Lamso N (2013). Effet de l'arbre Acacia senegal sur la fertilité des sols de gommeraies au Niger. Int. J. Biol. Chem. Sci. 7(6):2328-2337.
Crossref
|
|
|
|
Aldrich PR, Hamrick JL, Chavarriaga P, Kochert G (1998). Microsatellite analysis of demographic genetic structure in fragmented populations of the tropical tree Symphonia globulifera. Mol. Ecol. 7:933-944.
Crossref
|
|
|
|
Amani I (2010). Caractérisation des peuplements de principales essences productrices de gomme dans différentes conditions stationnelles de la commune de Torodi/Niger. Thèse de Doctorat. Spécialité: Ecologie et Environnement. USTHB/Algérie. 127 p.
|
|
|
|
Arce LR, Banks H (2001). A preliminary survey of pollen and other morphological characters in neotropical Acacia subgenus Aculeiferum (Leguminosae: Mimosoideae). Bot. J. Linn. Soc.135:263-270.
Crossref
|
|
|
|
Assogbadjo AE, Kyndt T, Sinsin B, Gheysen G, Van damme P (2006).Patterns of genetic and morphometric diversity in Baobab (Adansonia digitata) populations across different climatic zones of Benin (West Africa). Ann. Bot. 97:819-830.
Crossref
|
|
|
|
Assoumane A (2011). Déterminants de la variation génotypique et phénotypique de Acacia senegal (L.) Willd. dans son aire de distribution en Afrique soudano-sahélienne. Thèse de doctorat, Université Abdou Moumouni de Niamey – Niger. 118 p.
|
|
|
|
Assoumane A, Vaillant A, Zoubeirou AM, Verhaegen D (2009). Isolation characterization of microsatellite markers for Acacia senegal (L.) willd., a multipurpose arid and semi-arid tree. Mol. Ecol. Resour. 9:1380-1383.
Crossref
|
|
|
|
Assoumane A, Zoubeirou AM, Benedicte F, Gilles B, Saadou M, Verhaegen D (2012). Differentiation between two sub-species of Acacia senegal complex: Acacia senegal (L.) Willd. and Acacia dudgeoni Craib ex Holland using morphological traits and molecular markers. Genet. Resour. Crop Evol. 48:59-39.
Crossref
|
|
|
|
Blanc M, Boshier H, Powell (1999). Genetic variation within a fragmented population of Swietenia humilis Zucc. Mol. Ecol. 8(11):1899-1909.
Crossref
|
|
|
|
Blanquart F, Gandon S (2011). Evolution of migration in a periodically changing environment. Am. Nat. 177(2):188-201.
Crossref
|
|
|
|
Boatwright JS, Van der Bank M, Maurin O (2014). Name changes in African Acacia species. Veld and Flora 100:33.
|
|
|
|
Borgel A, Cardoso C, Sané D, Chevallier M (2003). La génétique d'Acacia raddiana. In: Grouzis M, Le Floc'h É (Eds.). Un arbre au désert: Acacia raddiana. IRD Éditions. Tiré de
View
|
|
|
|
Buckley J, Bridle JR, Pomiankowski A (2010). Novel variation associated with species range expansion. BMC Evol. Biol.10(382):1471-2148.
Crossref
|
|
|
|
Butcher PA, Decroocq, Gray Y, Moran GF (2000). Development, inheritance and cross-species amplification of microsatellites markers from Acacia mangium. Théor. Appl. Genet.101:1282-1290.
Crossref
|
|
|
|
Chiveu CJ, Dangasuk OG, Omunyin ME, Wachira FN (2008). Genetic diversity in Kenyan populations of Acacia senegal (L.) willd revealed by combined RAPD and ISSR markers. Afr. J. Biotechnol. 7(14):2333-2340.
|
|
|
|
Collevatti RG, Grattapaglia D, Hay JD (2001). Population genetic structure of the endangered tropical tree species Caryocar brasiliense, based on variability at microsatellite loci. Mol. Ecol. 10:349-356.
Crossref
|
|
|
|
Dutech C, Joly HI, Jarne P (2004). Gene flow, historical population dynamics and genetic diversity within French Guiana populations of a rainforest tree species, Vouacapoua americana. Heredity 92:69-77.
Crossref
|
|
|
|
Elhadji SD, Alzouma MZ, Adamou MM, Abdou MM, Assoumane A (2012). Réponse au déficit hydrique de quatre provenances de Acacia senegal vivant dans les conditions contrastées au Niger. Annales de l'Université Abdou Moumouni de Niamey.Tome XIII-A: 63-71.
|
|
|
|
Elhadji SD, Lawali S, Assoumane A, Issoufou HB, Maisharou A, Alzouma MZ (2016). Local perceptions of climate change and adaptation strategies in the management of Acacia senegal parks in Niger. J. Biodivers. Environ. Sci. 9(1):319-328.
|
|
|
|
England PR, Usher AV, Whelan RJ, Ayre DJ (2002). Microsatellite diversity and genetic structure of fragmented populations of the rare, ï¬re-dependent shrub Grevillea macleayana. Mol. Ecol. 11:967-977.
Crossref
|
|
|
|
Goudet J (2001). FSTAT, a program to estimate and test gene diversities and fixation indices. Version 2.9.3. Department of Ecology & Evolution, Biology Building, UNIL, CH-1015 Lausanne, Switzerland,
View
|
|
|
|
Guinko S, Ibrahim N, Wickens GE, Seil El Din AG (1996). Rôle des acacias dans l'économie rurale des régions sèches d'Afrique et du Proche-Orient. Cahier FAO Conservation 27:140.
|
|
|
|
Haddad WA (2011). Classification and nomenclature of the genus Acacia (Leguminosae), with emphasis on Africa. Dendron 43:34-43.
|
|
|
|
Ichaou A (2008). Identification et caractérisation des formations gommières à l'échelle de la commune de Torodi. 52.
|
|
|
|
Jordana J (2003). Genetic structure of eighteen local South European beef cattle breeds by comparative F-statistics analysis. J. Anim. Breed. Genet. 120:73-87.
Crossref
|
|
|
|
Kremer A, Ronce O, Robledo-Arnuncio JJ, Guillaume F, Bohrer G, Nathan R, Bridle JR, Gomulkiewicz R, Klein EK, Ritland K, Kuparinen A, Gerber S, Schueler S (2012). Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecol. Lett. 15(4):378-392.
Crossref
|
|
|
|
Ky CL, Barre P, Lorieux M, Trouslot P, Akaffou S, Louarn J, Charrier A, Hamon S, Noirot M (2000). Interspecific genetic linkage map, segregation distortion and genetic conversion in coffee (Coffea sp.). Theor. Appl. Genet. 101(4):669-676.
Crossref
|
|
|
|
Kyalangalilwa B, Boatwright JS, Daru BH, Maurin O, Van der Bank M (2013). Phylogenetic position and revised classification of Acacia s.l. (Fabaceae; Mimosoideae) in Africa, including new combinations in Vachellia and Senegalia. Bot. J. Linn. Soc. 172:500-523.
Crossref
|
|
|
|
Lemes MR, Gribel R, Proctor J, Grattapaglia D (2003). Population genetic structure of mahogany (Swietenia macrophylla King, Meliaceae) across the Brazilian Amazon based on variation at microsatellite loci: implications for conservation. Mol. Ecol. 12:2845-2883.
Crossref
|
|
|
|
Lhuillier E, Butaud JF, Bouvet JM (2006). Extensive clonality and strong differentiation in the insular Paciï¬c tree Santalum insulaire: implications for its conservation. Ann. Bot. 98:1061-1072.
Crossref
|
|
|
|
Lopez S, Rousset F, Shaw FH, Shaw RG, Ronce O (2009). Joint effects of inbreeding and local adaptation on the evolution of genetic load after fragmentation. Conserv. Biol. 23(6):1618-1627.
Crossref
|
|
|
|
Maisharou A, Nourou H (2004). Rapport des études filières gomme arabique au Niger. Ministère de l'Environnement et de la Lutte Contre la Désertification, Niamey-Niger. 41 p.
|
|
|
|
Maydell Von HJ (1983). Arbres et arbuste du sahel, leurs caractéristiques et leur utilisation. G.T.Z. Eschborn, 529.
|
|
|
|
Mohamed OA, Salem FB, Sonia B, Djemali MN (2010). Analyse moléculaire de la diversité génétique des dromadaires (Camelus dromedarius) en Tunisie. Biotechnol. Agron. Soc. Environ. 14(3):399-408.
|
|
|
|
Muller F, Voccia M, Ba A, Bouvet JM (2009). Genetic diversity and gene flow in a Caribbean tree Pterocarpus ofï¬cinalis Jacq.: a study based on chloroplast and nuclear microsatellites. Genetica. 135:185-198.
Crossref
|
|
|
|
Novick RR, Dick CD, Lemes MR, Navarro C, Caccon A, Bermingham E (2003). Genetic structure of Mesoamerican population of big-leaf mahogany (Swietenia macrophylla) inferred from microsatellite analysis. Mol. Ecol. 12:2885–2893.
Crossref
|
|
|
|
Omondi SF, Cavers S, Khasa DP (2009). Genetic diversity and population structure of Acacia senegal (L.) willd. In kenya. Tropical Plant Biology 3: 59-70.
Crossref
|
|
|
|
Peakall R, Smouse PE (2012). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537-2539.
Crossref
|
|
|
|
Perrier X, Jacquemond-Collet J (2006). Darwin software. http://darwin.cirad.fr/darwin.
|
|
|
|
Pritchard JK, Stephens M, Donnelly P (2000). Inference of population structure using multilocus genotype data. Genetics 155:945-959.
|
|
|
|
Raddad EY, Salih AA, Elfadl MA, Kaarakka V, Luukkanen O (2005). Symbiotic nitrogen fixation in eight Acacia senegal provenances in dry land clays. Plant Soil 27(5):261-269.
Crossref
|
|
|
|
Rathore PK, Madihalli S, Hegde S, Hegde HV, Bhagwat RM, Gupta VS, Kholkute SD, Baran Jha T, Roy S (2016). Assessment of Genetic diversity of Gymnema sylvestre (Retz.) R.Br. from Western Ghats and Eastern India, India. J. Biodivers. Environ. Sci. 9(1):82-92.
|
|
|
|
Rossetto M, Slade RW, Baverstock PR, Henry RJ, Lee LS (1999). Microsatellite variation and assessment of genetic structure in tea tree (Melaleuca alternifolia – Myrtaceae). Mol. Ecol 8:633-643.
Crossref
|
|
|
|
Saitou N, Nei M (1987).The neighbor joining method: a new method for reconstructing phylogenetic trees. Mol. Ecol. Evol. 4(4):406-425.
|
|
|
|
Slatkin M (1987). Gene flow and the geographic structure of natural populations. Science 236(4803):787-792.
Crossref
|
|
|
|
Sanou H, Lovett N, Bouvet JM (2005). Comparison of quantitative and molecular variation in agroforestry populations of the shea tree (Vitellaria paradoxa C.F. Gaertn) in Mali. Mol. Ecol 14:2601-2610.
Crossref
|
|
|
|
Todou G, Benoit L, Eeckenbrugge G, Joly HI, Onana JM, Akoa A (2013). Comparaison des diversités génétiques de Dacryodes edulis (G.Don) H.J. Lam et de Dacryodes buettneri (Engel.) H.J. Lam (Burséracées), deux espèces forestières utiles en Afrique centrale. Int. J. Biol. Chem. Sci. 7(3):1243-1254.
Crossref
|
|
|
|
Wickens GE, Seif El Din AG, Sita G, Nahal I (1995). Role of Acacia species in the rural economy of dry Africa and the Near East. FAO Conservation Guide 27:1-152.
|
|
|
|
William C, Hamrick J (1996). Elite populations for conifer breeding and gene conservation. J. Can. For. Res. 26(3):453-461.
Crossref
|
|
|
|
Wright S (1965).The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395-420.
Crossref
|
|
|
|
Young JM, Kuykendall LD, Martinez-Romero E, Kerr A, Sawada H (2001). A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations. Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicolaand R. vitis. Int. J. Syst. Bacteriol. 51:89-103.
Crossref
|
