Insights into the historical assembly of global dryland floras: the diversification of Zygophyllaceae

Background Drylands cover nearly 41% of Earth’s land surface and face a high risk of degradation worldwide. However, the actual timeframe during which dryland floras rose on a global scale remains unknown. Zygophyllaceae, an important characteristic component of dryland floras worldwide, offers an ideal model group to investigate the diversification of dryland floras. Here, we used an integration of the phylogenetic, molecular dating, biogeographic, and diversification methods to investigate the timing and patterns of lineage accumulation for Zygophyllaceae overall and regionally. We then incorporated the data from other dominant components of dryland floras in different continents to investigate the historical construction of dryland floras on a global scale. Results We provide the most comprehensive phylogenetic tree for Zygophyllaceae so far based on four plastid and nuclear markers. Detailed analyses indicate that Zygophyllaceae colonized Africa, Asia, Australia, and the New World at different periods, sometimes multiple times, but Zygophyllaceae lineages in the four regions all experienced a rapid accumulation beginning at the mid-late Miocene (~ 15–10 Ma). Other eleven essential elements of dryland floras become differentiated at the same time. Conclusions Our results suggest that the rise of global dryland floras is near-synchronous and began at the mid-late Miocene, possibly resulting from the mid-Miocene global cooling and regional orogenetic and climate changes. The mid-late Miocene is an essential period for the assembly and evolution of global dryland floras. Electronic supplementary material The online version of this article (10.1186/s12862-018-1277-z) contains supplementary material, which is available to authorized users.


Additional file 1
Table S1 Species, voucher information and GenBank accession numbers for the datasets of four markers.

Table S2
The parameters of the best-fit model for each DNA region.

Table S3
The crown group ages and ancestral habitat types of eleven representative plant groups in dryland floras across different continents.  The best-fit model was determined by the Akaike information criterion (AIC) in jModelTest. "-" indicates inapplicable.

Ancestral habitat Comment
Africa Vachellia (Fabaceae) 16.6 (13.5-23.4) dryland African species of Vachellia is mainly distributed in dry woodlands except that three species inhabit in mesic forests [1]. Our inference of habitat evolution indicates that the most recent common ancestor (MRCA) of African Vachellia occurred in dryland habitat (Additional file 2: Figure S4a). Sect. Euphorbia (Euphorbiaceae) 14 (10.5-17.8) dryland Most of Sect. Euphorbia species are dominants of dryland floras throughout Africa (including Madagascar) except that a few of species inhabit in humid montane regions [2,3]. Our inference of habitat evolution indicates that the MRCA of Sect. Euphorbia lived in dryland habitat (Additional file 2: Figure S4b).

Asia
Caragana (Fabaceae) 18.37 (12.11-25.87) dryland (steppe) Species of Caragana are primarily restricted to dryland floras, with a few outliers extending to non-dryland floras. Zhang et al. inferred evolution of habitats in the genus and found that its MRCA inhabited in Junggar steppe of Northwest dryland region of China [4]. Consolida (Ranunculaceae) 16.9 (13.4-20.9) dryland Species of Consolida are mainly distributed in central Asian and Irano-Turanian dryland regions, with a few extending to the Mediterranean basin [5]. Our inference of habitat evolution indicates that the MRCA of Consolida occurred in dryland habitat (Additional file 2: Figure S4c).

Australia
Austrostipa (Poaceae) 14.55 (6.48-24.21) dryland Genus Austrostipa is a major component of dryland grasslands in Australia, with a few outliers extending to other habitats [6]. Our inference of habitat evolution indicates that the MRCA of Consolida occurred in dryland habitat (Additional file 2: Figure S4d).  [3]. Our inference of habitat evolution indicates that the MRCA of the subsection occurred in dryland habitat (Additional file 2: Figure S4e). HPD = highest posterior density. a,b Taxa are from tropical America and western North America, respectively.