Altitudinal gradients, biogeographic history and microhabitat adaptation affect fine-scale spatial genetic structure in African and Neotropical populations of an ancient tropical tree species

Abstract

The analysis of fine-scale spatial genetic structure (FSGS) within populations can provide insights into eco-evolutionary processes. Restricted dispersal and locally occurring genetic drift are the primary causes for FSGS at equilibrium, as described in the isolation by distance (IBD) model. Beyond IBD expectations, spatial, environmental or historical factors can affect FSGS. We examined FSGS in seven African and Neotropical populations of the late-successional rain forest tree Symphonia globulifera L. f. (Clusiaceae) to discriminate the influence of drift-dispersal vs. landscape/ecological features and historical processes on FSGS. We used spatial principal component analysis and Bayesian clustering to assess spatial genetic heterogeneity at SSRs and examined its association with plastid DNA and habitat features. African populations (from Cameroon and São Tomé) displayed a stronger FSGS than Neotropical populations at both marker types (mean Sp = 0.025 vs. Sp = 0.008 at SSRs) and had a stronger spatial genetic heterogeneity. All three African populations occurred in pronounced altitudinal gradients, possibly restricting animal-mediated seed dispersal. Cyto-nuclear disequilibria in Cameroonian populations also suggested a legacy of biogeographic history to explain these genetic patterns. Conversely, Neotropical populations exhibited a weaker FSGS, which may reflect more efficient wide-ranging seed dispersal by Neotropical bats and other dispersers. The population from French Guiana displayed an association of plastid haplotypes with two morphotypes characterized by differential habitat preferences. Our results highlight the importance of the microenvironment for eco-evolutionary processes within persistent tropical tree populations.

Fig 1. Location of Symphonia globulifera populations examined in this paper and kinship-distance relationships within populations.

The mean jackknife estimate of the kinship coefficient F_ij (± standard error) is plotted per distance class, as well as the permutation-based 95% CI for absence of FSGS (dashed grey lines).

Fig 2. Fine-scale spatial genetic structure in Neotropical populations of Symphonia globulifera.

Each individual is plotted on the map as a disc representing the colour of its specific plastid DNA haplotype (“H”) or as a pie chart indicating the ancestry proportions, Q, in different genetic clusters (“GP”), as defined in the STRUCTURE analysis for the number of clusters K best describing the data. Individual STRUCTURE barplots below each population map illustrate the distribution of ancestry proportion for each of the K gene pools.

Fig 3. Fine-scale spatial genetic structure in African populations of Symphonia globulifera.

Each individual is plotted on the map as a disc representing the colour of its specific plastid DNA haplotype (“H”) or as a pie chart indicating the ancestry proportions, Q, in different genetic clusters (“GP”), as defined in the STRUCTURE analysis for the number of clusters K best describing the data. Individual STRUCTURE barplots below each population map illustrate the distribution of ancestry proportion for each of the K gene pools.