Geological and climatic changes in quaternary shaped the evolutionary history of Calibrachoa heterophylla, an endemic South-Atlantic species of petunia

Abstract

Background: The glacial and interglacial cycles that characterized the Quaternary greatly affected the distribution and genetic diversity of plants. In the Neotropics, few phylogeographic studies have focused on coastal species outside of the Atlantic Rainforest. Climatic and sea level changes during the Quaternary played an important role in the evolutionary history of many organisms found in coastal regions. To contribute to a better understanding of plant evolution in this environment in Southern South America, we focused on Calibrachoa heterophylla (Solanaceae), an endemic and vulnerable wild petunia species from the South Atlantic Coastal Plain (SACP).

Results: We assessed DNA sequences from two cpDNA intergenic spacers and analyzed them using a phylogeographic approach. The present phylogeographic study reveals the influence of complex geologic and climatic events on patterns of genetic diversification. The results indicate that C. heterophylla originated inland and subsequently colonized the SACP; the data show that the inland haplogroup is more ancient than the coastal one and that the inland was not affected by sea level changes in the Quaternary. The major diversification of C. heterophylla that occurred after 0.4 Myr was linked to sea level oscillations in the Quaternary, and any diversification that occurred before this time was obscured by marine transgressions that occurred before the coastal sand barrier's formation. Results of the Bayesian skyline plot showed a recent population expansion detected in C. heterophylla seems to be related to an increase in temperature and humidity that occurred at the beginning of the Holocene.

Conclusions: The geographic clades have been formed when the coastal plain was deeply dissected by paleochannels and these correlate very well with the distributional limits of the clades. The four major sea transgressions formed a series of four sand barriers parallel to the coast that progressively increased the availability of coastal areas after the regressions and that may have promoted the geographic structuring of genetic diversity observed today. The recent population expansion for the entire species may be linked with the event of marine regression after the most recent sea transgression at ~5 kya.

Figure 1

South Atlantic coastal plain map. Southern Brazil and Uruguay physiographic map modified from Weschenfelder et al.[40], indicating South Atlantic Coastal Plain location and Barrier–Lagoon Systems I to IV positions according Tomazelli & Villwock [21].

Figure 2

Haplotypes network. Evolutionary relationships among haplotypes of Calibrachoa heterophylla cpDNA using Median-joining network approach. Colors identified the haplogroups. Circle sizes are proportional to haplotype frequency and crossed lines are substitutions inferred in the branches.

Figure 3

Collection site location. a) Map showing the sampling sites. The colors of the populations are related to the haplogroups identified by the network and Bayesian chronogram. Dotted lines represent paleochannels [40,51]. b)Calibrachoa heterophylla flower.

Figure 4

Bayesian phylogenetic tree. Bayesian chronogram, with clade posterior probability (>0.5) shown externally to the branches, and point estimates and confidence intervals for the ages (in million of years) are presented next to selected branches.

Figure 5

Bayesian skyline plot. Bayesian Skyline Plot for Calibrachoa heterophylla cpDNA showing the effective fluctuation in population size over time, the thick solid line represents the median estimates and the shaded area the 95% confidence interval. The dashed line indicates the Pleistocene-Holocene transition.

Figure 6

Sea level changes before and during South Atlantic coastal plain formation. Approximate paleogeographic reconstruction of sea level, based on reports in the literature and plotted on current data of altitude and bathymetry. The white circles identify the position of the current Calibrachoa heterophylla populations studied in this work. a) Maximum transgressive event which led to the formation of Barrier–Lagoon System I, Middle Pleistocene, 0.4 Myr ago, 21 m above current sea level [45]. b) The Pleistocene-Holocene transition, 11.7 Kyr ago, 70 m below current sea level [51]. The Patos and Mirim Lagoons are not shown because there are no accurate data about their conformation in this period.