Demographical history and palaeodistribution modelling show range shift towards Amazon Basin for a Neotropical tree species in the LGM

Abstract

Background: We studied the phylogeography and demographical history of Tabebuia serratifolia (Bignoniaceae) to understand the disjunct geographical distribution of South American seasonally dry tropical forests (SDTFs). We specifically tested if the multiple and isolated patches of SDTFs are current climatic relicts of a widespread and continuously distributed dry forest during the last glacial maximum (LGM), the so called South American dry forest refugia hypothesis, using ecological niche modelling (ENM) and statistical phylogeography. We sampled 235 individuals of T. serratifolia in 17 populations in Brazil and analysed the polymorphisms at three intergenic chloroplast regions and ITS nuclear ribosomal DNA.

Results: Coalescent analyses showed a demographical expansion at the last c. 130 ka (thousand years before present). Simulations and ENM also showed that the current spatial pattern of genetic diversity is most likely due to a scenario of range expansion and range shift towards the Amazon Basin during the colder and arid climatic conditions associated with the LGM, matching the expected for the South American dry forest refugia hypothesis, although contrasting to the Pleistocene Arc hypothesis. Populations in more stable areas or with higher suitability through time showed higher genetic diversity. Postglacial range shift towards the Southeast and Atlantic coast may have led to spatial genome assortment due to leading edge colonization as the species tracks suitable environments, leading to lower genetic diversity in populations at higher distance from the distribution centroid at 21 ka.

Conclusion: Haplotype sharing or common ancestry among populations from Caatinga in Northeast Brazil, Atlantic Forest in Southeast and Cerrado biome and ENM evince the past connection among these biomes.

Keywords: Bignoniaceae; Dry forest refugia; Ecological niche modelling; Phylogeography; Pleistocene arc hypothesis; Quaternary climatic changes.

Fig. 1

Geographical distribution of haplotypes of Tabebuia serratifolia and Bayesian clustering for (a) ITS and (b) cpDNA, based on the sequencing of 257 individuals from 17 populations. Different colours were assigned for each haplotype according to the figure legend. The circle size represents the sample size in each population and the circle sections represent the haplotype frequency in each sampled population. For details on population codes and localities see Additional file 2: Table S1. For BAPS clustering, each colour represents an inferred cluster (5 clusters for ITS and 3 for cpDNA)

Fig. 2

Demographical and evolutionary history of Tabebuia serratifolia lineages, based on concatenated sequences of cpDNA and ITS nrDNA. a Extended Bayesian Skyline Plot showing effective population size increase at c. 150 ka. b Coalescent tree showing that most lineage divergences occurred after the Lower Pleistocene. Tip section colour corresponds to population, following the figure legend. The section size corresponds to the number of haplotypes in each population in each clade. Grey bar corresponds to 95 % credibility interval of the mean time to the moat common ancestor; numbers above the branches are the support to the node (posterior probability); numbers below the branches are the node dating (time to the moat common ancestor). Time scale is in millions of years (Ma) before present

Fig. 3

Maps of consensus of the 60 models expressing the ensemble potential distribution for Tabebuia serratifolia, based on ecological niche modelling. Potential distribution across the Neotropics during the (a) LGM (21 ka), (b) mid-Holocene (6 ka), (c) present-day (d) historical refugium through time (from the LGM to present-day)

Fig. 4

Spatial distribution of genetic diversity for ITS nuclear ribosomal DNA for Tabebuia serratifolia, in relation to the potential palaeodistribution at 21 ka. a Distribution of the haplotype diversity (h). b Distribution of the mutation parameter theta (θ). Circumference sizes are proportional to the value of genetic parameter, following the figure legends. The maps represent the consensus of the 60 models expressing the ensemble potential distribution for Tabebuia serratifolia, based on ecological niche modelling

Fig. 5

The demographical history scenarios simulated for Tabebuia serratifolia and their geographical representation. Circles represent the demes. The size and location of circle during the LGM indicate demographical population expansion or shrink, and geographical range shift at that time. LIG: last interglacial; LGM: last glacial maximum; Pres: present-day; N0: effective population size at time t0 (present); N1: effective population size at time t1400 (1,400 generations ago). The demographical scenarios correspond to: PLAH, Pleistocene Arc hypothesis; PPPH, the ‘Amazon SDF’ hypothesis; Both (PLAH + PPPH), i.e., an expansion throughout the Central and Southwest Brazil and also westward towards the Amazon Basin; Retraction, a retraction in geographical range in Central Brazil