Unravelling the genetic differentiation among varieties of the Neotropical savanna tree Hancornia speciosa Gomes

Abstract

Background and aims: Spatial distribution of species genetic diversity is often driven by geographical distance (isolation by distance) or environmental conditions (isolation by environment), especially under climate change scenarios such as Quaternary glaciations. Here, we used coalescent analyses coupled with ecological niche modelling (ENM), spatially explicit quantile regression analyses and the multiple matrix regression with randomization (MMRR) approach to unravel the patterns of genetic differentiation in the widely distributed Neotropical savanna tree, Hancornia speciosa (Apocynaceae). Due to its high morphological differentiation, the species was originally classified into six botanical varieties by Monachino, and has recently been recognized as only two varieties by Flora do Brasil 2020. Thus, H. speciosa is a good biological model for learning about evolution of phenotypic plasticity under genetic and ecological effects, and predicting their responses to changing environmental conditions.

Methods: We sampled 28 populations (777 individuals) of Monachino's four varieties of H. speciosa and used seven microsatellite loci to genotype them.

Key results: Bayesian clustering showed five distinct genetic groups (K = 5) with high admixture among Monachino's varieties, mainly among populations in the central area of the species geographical range. Genetic differentiation among Monachino's varieties was lower than the genetic differentiation among populations within varieties, with higher within-population inbreeding. A high historical connectivity among populations of the central Cerrado shown by coalescent analyses may explain the high admixture among varieties. In addition, areas of higher climatic suitability also presented higher genetic diversity in such a way that the wide historical refugium across central Brazil might have promoted the long-term connectivity among populations. Yet, FST was significantly related to geographic distances, but not to environmental distances, and coalescent analyses and ENM predicted a demographical scenario of quasi-stability through time.

Conclusions: Our findings show that demographical history and isolation by distance, but not isolation by environment, drove genetic differentiation of populations. Finally, the genetic clusters do not support the two recently recognized botanical varieties of H. speciosa, but partially support Monachino's classification at least for the four sampled varieties, similar to morphological variation.

Fig. 1.

Populations sampled (28) and Bayesian cluster of individuals (777) of Hancornia speciosa based on seven nuclear microsatellite loci. Different colours were assigned to different clusters according to the key. For population codes, see Supplementary DataTable S1.

Fig. 2.

Environmental suitability for Hancornia speciosa in the Neotropics expressed by the ensemble of 50 ENMs for the LGM (21 ka), mid-Holocene (6 ka), the present and the historical refugium through time (suitability >0.5).

Fig. 3.

Spatial distribution of genetic diversity of Hancornia speciosa in relation to the historical refugium, i.e. areas climatically suitable throughout the time (in green). (A) Allelic richness (A_r). (B) Genetic diversity (H_e). (C) θ. (D) Effective population size (N_e). Circumference sizes are proportional to the value of genetic parameter, according to the keys.