Phylogeography of African Locust Bean (Parkia biglobosa) Reveals Genetic Divergence and Spatially Structured Populations in West and Central Africa

Abstract

The evolutionary history of African savannah tree species is crucial for the management of their genetic resources. In this study, we investigated the phylogeography of Parkia biglobosa and its modeled distribution under past and present climate conditions. This tree species is very valued and widespread in West Africa, providing edible and medicinal products. A large sample of 1610 individuals from 84 populations, distributed across 12 countries in Western and Central Africa, were genotyped using 8 nuclear microsatellites. Individual-based assignments clearly distinguished 3 genetic clusters, extreme West Africa (EWA), center of West Africa (CWA), and Central Africa (CA). Overall, estimates of genetic diversity were moderate to high, with lower values for populations in EWA (allelic richness after rarefaction [AR] = 6.4, expected heterozygosity [HE] = 0.78, and observed heterozygosity [HO] = 0.7) and CA (AR = 5.9, HE = 0.67, and HO = 0.61) compared with populations in CWA (AR = 7.3, HE = 0.79, and HO = 0.75). The overall population differentiation was found to be moderate (FST = 0.09). A highly significant isolation by distance pattern was detected, with a marked phylogeographic signature suggesting possible effects of past climate and geographic barriers to migration. Modeling the potential distribution of the species showed a contraction during the last glaciations followed by expansion events. The exploratory approximate Bayesian computation conducted suggests a best-supported scenario in which the cluster CWA traced back to the ancestral populations and a first split between EWA and CWA took place about 160000 years before present (BP), then a second split divided CA and CWA, about 100000 years BP. However, our genetic data do not enable us to conclusively distinguish among a few alternative possible scenarios.

Figure 1.

The 4 scenarios compared in approximate Bayesian computation. EWA, Extreme West Africa group; CWA, Central West Africa group; CA, Central Africa group; t_# = divergence time-scaled by generation time; N_# = effective population size; ra = admixture rate. Scenario 1: the 3 clusters (EWA, CWA, CA) split at the same time from the ancestral population (see additional explanations in Supplementary Material 2—ABC); scenario 2: cluster EWA diverged earlier from CWA than CA; scenario 3: CA diverged earlier from CWA than EWA; scenario 4: EWA and CA split from the ancestral population and CWA resulted from their admixture. Posterior probabilities of each scenario are presented in Supplementary Material 2—ABC, Table S4, scenarios from 1 to 4).

Figure 2.

IDW interpolation of allelic richness (A_R) calculated for 84 Parkia biglobosa populations using 8 SSRs loci and restricted to the modeled distribution area of the species. The color gradient indicates the level of allelic richness across the species’ range. Red lines represent genetic boundaries detected by BARRIER. See online version for full colors.

Figure 3.

Spatial distribution of genetic clusters. Colors of the pie charts refer to the 6 clusters identified by STRUCTURE (EWA, CWA 1, CWA 2, CWA 3, CWA 4, CA) and the proportion of the pie charts sectors to the relative number of individuals assigned. The histograms of individual assignments to genetics clusters are given for K = 3 and K = 6 clusters. See online version for full colors.

Figure 4.

PCoA showing the patterns of genetic structure of Parkia biglobosa grouping into 3 clusters corresponding to 3 geographic regions (EWA, CWA, CA). CWA is subdivided into 4 subclusters (CWA 1, CWA 2, CWA 3, and CWA 4). See online version for full colors.

Figure 5.

Relationship between pairwise F_ST and geographic distances among 84 populations of Parkia biglobosa. The symbols show population pairs from the 3 main genetic clusters.

Figure 6.

Predicted change of suitable habitat for Parkia biglobosa comparing projected LGM and contemporary climate conditions. Blue areas represent continued suitable habitat from LGM until present (original suitable habitat); light green indicates areas that were probably not suitable at the LGM, but are suitable at present (recent suitable habitat); and red areas represent potential suitable habitat during LGM but no longer at present (lost suitable habitat). See online version for full colors.