Radiating diversification and niche conservatism jointly shape the inverse latitudinal diversity gradient of Potentilla L. (Rosaceae)

Abstract

Background: The latitudinal diversity gradient (LDG), characterized by an increase in species richness from the poles to the equator, is one of the most pervasive biological patterns. However, inverse LDGs, in which species richness peaks in extratropical regions, are also found in some lineages and their causes remain unclear. Here, we test the roles of evolutionary time, diversification rates, and niche conservatism in explaining the inverse LDG of Potentilla (ca. 500 species). We compiled the global distributions of ~ 90% of Potentilla species, and reconstructed a robust phylogenetic framework based on whole-plastome sequences. Next, we analyzed the divergence time, ancestral area, diversification rate, and ancestral niche to investigate the macroevolutionary history of Potentilla.

Results: The genus originated in the Qinghai-Tibet Plateau during the late Eocene and gradually spread to other regions of the Northern Hemisphere posterior to the late Miocene. Rapid cooling after the late Pliocene promoted the radiating diversification of Potentilla. The polyploidization, as well as some cold-adaptive morphological innovations, enhanced the adaptation of Potentilla species to the cold environment. Ancestral niche reconstruction suggests that Potentilla likely originated in a relatively cool environment. The species richness peaks at approximately 45 °N, a region characterized by high diversification rates, and the environmental conditions are similar to the ancestral climate niche. Evolutionary time was not significantly correlated with species richness in the latitudinal gradient.

Conclusions: Our results suggest that the elevated diversification rates in middle latitude regions and the conservatism in thermal niches jointly determined the inverse LDG in Potentilla. This study highlights the importance of integrating evolutionary and ecological approaches to explain the diversity pattern of biological groups on a global scale.

Keywords: Potentilla; Diversification; Evolutionary time; Inverse latitudinal diversity gradient; Niche conservatism; Species richness.

Fig. 1

Historical biogeography of Potentilla. (a) Five biogeographic regions and potential dispersal routes of Potentilla. (b) Ancestral range estimation using BioGeoBEARS with the BAYAREALIKE + J model. Nodes 1–7 refer to the stem ages of the eight clades, nodes 8–15 refer to the crown ages of the eight clades, and nodes 16–17 refer to the dispersal events. (c) Temporal patterns in the net diversification rate of Potentilla across the globe and five biogeographic regions estimated by the empirical time-calibrated tree; red curve shows global temperature differences over the last 37.44 Ma as compared to current temperature and is modified from Westerhold et al. [88]. The map used in this study was downloaded from DIVA-GIS (http://www.diva-gis.org/Data). Qua. = Quaternary

Fig. 2

Diversification rate analyses of Potentilla. (a) Phylorate plot showing the speciation rates along each branch. Arrows, shifts in speciation rates. The four traits used for trait-dependent analyses (A–D) are plotted at right—A: ploidy; B: leaves hair; C: root; D: basal leaves. The colors of the circles in A–D correspond to the boxplots c–f. (b) Speciation, extinction, and net diversification rates over time according to BAMM analysis. (c–e) Binary trait-dependent diversification inferred by HiSSE analyses. (f) Multistate trait-dependent diversification estimated by MuSSE analysis. Asterisks in (c-e) indicate significant differences according to t tests. ****P < 0.0001; N.S., not significant

Fig. 3

Distribution of species richness (a, b), evolutionary time (c, d), mean diversification rates (e, f), and level of deviation from ancestral climate (g, h) of Potentilla calculated based on the 149-dataset and 451-dataset, respectively. The resolution of grid cells was 100 km × 100 km

Fig. 4

Latitudinal trends in species richness, evolutionary time, diversification rates, and level of deviation from ancestral niche calculated based on the 149-dataset (a), and the 451-dataset (b)