Demographic stability and high historical connectivity explain the diversity of a savanna tree species in the Quaternary

Abstract

Background and aims: Cyclic glaciations were frequent throughout the Quaternary and this affected species distribution and population differentiation worldwide. The present study reconstructed the demographic history and dispersal routes of Eugenia dysenterica lineages and investigated the effects of Quaternary climate change on its spatial pattern of genetic diversity.

Methods: A total of 333 individuals were sampled from 23 populations and analysed by sequencing four regions of the chloroplast DNA and the internal transcribed spacer of the nuclear DNA. The analyses were performed using a multi-model inference approach based on ecological niche modelling and statistical phylogeography.

Key results: Coalescent simulation showed that population stability through time is the most likely scenario. The palaeodistribution dynamics predicted by the ecological niche models revealed that the species was potentially distributed across a large area, extending over Central-Western Brazil through the last glaciation. The lineages of E. dysenterica dispersed from Central Brazil towards populations at the northern, western and south-eastern regions. A historical refugium through time may have favoured lineage dispersal and the maintenance of genetic diversity.

Conclusions: The results suggest that the central region of the Cerrado biome is probably the centre of distribution of E. dysenterica and that the spatial pattern of its genetic diversity may be the outcome of population stability throughout the Quaternary. The lower genetic diversity in populations in the south-eastern Cerrado biome is probably due to local climatic instability during the Quaternary.

Keywords: Cerrado; coalescent simulation; ecological niche modelling; genetic diversity; palaeodistribution; phylogeography.

Fig. 1.

Geographical distribution of haplotypes and Bayesian clustering for cpDNA (A) and ITS (B), based on 23 populations of Eugenia dysenterica sampled in the Cerrado biome. Different colours were assigned for each haplotype according to the figure legend and the pie charts represent the haplotype frequency in each sampled population. For Bayesian clustering, each colour represents an inferred cluster (seven clusters for cpDNA and 11 for ITS) grouped by Cerrado geographical regions. For details on population codes and localities see Table S1.

Fig. 2.

Schematic representation the demographic history scenarios simulated for the 23 populations of Eugenia dysenterica sampled in the Cerrado biome, and their geographical representation as predicted by ecological niche models (ENMs). Circles represent hypothetical demes and indicate population stability or shrinkage through time. LGM, Last Glacial Maximum; Pres, present-day; N₀, effective population size at time t₀ (present); N₁, effective population size at time t₁₄₀₀ (1400 generations ago); N_t, logarithmic function for effective population size variation in coalescent simulation. The migration rate was 0·01 per generation.

Fig. 3.

Phylogenetic relationships among haplotypes using median-joining network of 23 populations of Eugenia dysenterica sampled in the Cerrado biome. Circumference size is proportional to haplotype frequency. The number of mutations is shown along lines in the network; ‘mv’ is the median vector. Different colours were assigned for each population according to the figure legend, grouped by Cerrado geographical region.

Fig. 4.

Relationships and time to most recent common ancestor (TMRCA) of haplotypes of 23 populations of Eugenia dysenterica lineages with cpDNA and ITS data combined. The blue bar corresponds to the 95 % highest posterior probability of the TMRCA; numbers below the branches are node supports (showing only nodes with posterior probability ≥ 0·9); numbers above the branches are the node dating (TMRCA). The time scale is in millions of years (Ma) before present. The colours represent Cerrado geographical regions.

Fig. 5.

Spatio-temporal dynamics of lineage diffusion among the 23 populations of Eugenia dysenteria sampled in the Cerrado biome, for 410, 380, 300, 250, 200, 130 and 70 ka. Arrows between locations represent branches in the tree along which the relevant location transition occurs. The map was adapted from the .kml file provided by SPREAD software generated using Google Earth (http://earth.google.com). For details on population codes and localities see Table S1.

Fig. 6.

Potential distribution of Eugenia dysenterica in the Neotropics, based on the consensus of the 13 ecological niche models and four atmosphere-ocean global circulation models used for modelling the palaeodistribution during the (A) LGM (21 ka), (B) mid-Holocene (6 ka) and (C) present-day. The historical refugium (D) shows areas climatically suitable throughout the period investigated.