Aridification as a driver of biodiversity: a case study for the cycad genus Dioon (Zamiaceae)

Abstract

Background and aims: Aridification is considered a selective pressure that might have influenced plant diversification. It is suggested that plants adapted to aridity diversified during the Miocene, an epoch of global aridification (≈15 million years ago). However, evidence supporting diversification being a direct response to aridity is scarce, and multidisciplinary evidence, besides just phylogenetic estimations, is necessary to support the idea that aridification has driven diversification. The cycad genus Dioon (Zamiaceae), a tropical group including species occurring from humid forests to arid zones, was investigated as a promising study system to understand the associations among habitat shifts, diversification times, the evolution of leaf epidermal adaptations, and aridification of Mexico.

Methods: A phylogenetic tree was constructed from seven chloroplast DNA sequences and the ITS2 spacer to reveal the relationships among 14 Dioon species from habitats ranging from humid forests to deserts. Divergence times were estimated and the habitat shifts throughout Dioon phylogeny were detected. The epidermal anatomy among Dioon species was compared and correlation tests were performed to associate the epidermal variations with habitat parameters.

Key results: Events of habitat shifts towards arid zones happened exclusively in one of the two main clades of Dioon. Such habitat shifts happened during the species diversification of Dioon, mainly during the Miocene. Comparative anatomy showed epidermal differences between species from arid and mesic habitats. The variation of epidermal structures was found to be correlated with habitat parameters. Also, most of the analysed epidermal traits showed significant phylogenetic signals.

Conclusions: The diversification of Dioon has been driven by the aridification of Mexico. The Miocene timing corresponds to the expansion of arid zones that embedded the ancestral Dioon populations. As response, species in arid zones evolved epidermal traits to counteract aridity stress. This case study provides a robust body of evidence supporting the idea that aridification is an important driver of biodiversity.

Keywords: Aridification; Dioon; Mexico; Zamiaceae; climate change; cycads; diversification; epidermal anatomy; habitat shift.

Fig. 1.

Definition of infrageneric clades and groups in Dioon. A Bayesian tree was constructed from seven cpDNA regions and one nrDNA sequence region of 35 accessions representing 14 species of the cycad genus Dioon. Accession labels correspond to those shown in Table 1. Posterior probability values are indicated above branches. Phylogenetic groups are annotated on the right and their geographical distributions are illustrated in the upper-left inset. Asterisks indicate accessions that were also analysed on epidermal anatomy.

Fig. 2.

The history of diversification of Dioon is associated with the aridification of Mexico. This ultrametric tree was constructed with BEAST (Drummond et al., 2012) using a birth–death model. Bold node labels (i, ix and xii) indicate calibration nodes. Left inset indicates the climate-based habitat categories, and the pie charts at nodes represent probabilities for the ancestral climate categories estimated with the maximum likelihood method in Mesquite (Maddison and Maddison, 2016). Ages of relevant nodes are annotated in Table 3. The distribution of groups is illustrated in the upper left inset (W, western; S, southern; E, eastern; Spi, Spinulosum clade). Accession labels correspond to those used in Table 1. Asterisks indicate accessions that were also analysed on epidermal anatomy.

Fig. 3.

Pearson product-moment correlation plots between trait measurements (vertical axes, in μm) and habitat variables (horizontal axes) in Dioon. Squared correlation coefficient (R²) values are indicated in each plot. Colour of plotted values corresponds to habitat categories as indicated in Fig. 1. Significant correlations (P < 0.05) are indicated with bold borders. Traits A–G correspond to those indicated in Table 2, and daggers (^†) indicate traits that show significant phylogenetic signal. Values are detailed in Table 4.

Fig. 4.

Phylogenetically independent contrast (PIC) correlation plots between trait measurements (vertical axes) and habitat variables (horizontal axes) in Dioon. Values of the squared PIC coefficient (PICC²) (Paradis et al., 2004) are indicated in each plot. Significant correlations (P < 0.05) are indicated by bold borders. Traits A–G correspond to those indicated in Table 2, and daggers (^†) indicate traits that show significant phylogenetic signal. Values are detailed in Table 4.

Fig. 5.

Categorical anatomical traits traced in the phylogeny of Dioon using the maximum likelihood method in Mesquite (Maddison and Maddison, 2016). (A) Ancestral reconstruction of absence/presence of papillae and its associated ring type, defined in the photographs at the right. Bars = 20 μm. (B) Ancestral reconstruction of furrows (photograph at the right; bar = 100 μm). Pie charts at nodes of trees represent the likelihood of the trait’s ancestral state.