Transcriptome sequencing data provide a solid base to understand the phylogenetic relationships, biogeography and reticulated evolution of the genus Zamia L. (Cycadales: Zamiaceae)

Abstract

Background and aims: Cycads are a key lineage to understand the early evolution of seed plants and their response to past environmental changes. However, tracing the evolutionary trajectory of cycad species is challenging when the robust relationships at inter- or infrageneric level are not well resolved.

Methods: Here, using 2901 single-copy nuclear genes, we explored the species relationships and gene flow within the second largest genus of cycads, i.e. Zamia, based on phylotranscriptomic analyses of 90 % extant Zamia species. Based on a well-resolved phylogenetic framework, we performed gene flow analyses, molecular dating and biogeographical reconstruction to examine the spatiotemporal evolution of Zamia. We also performed ancestral state reconstruction of a total of 62 traits of the genus to comprehensively investigate its morphological evolution.

Key results: Zamia comprises seven major clades corresponding to seven distinct distribution areas in the Americas, with at least three reticulation nodes revealed in this genus. Extant lineages of Zamia initially diversified around 18.4-32.6 (29.14) million years ago in Mega-Mexico, and then expanded eastward into the Caribbean and southward into Central and South America. Ancestral state reconstruction revealed homoplasy in most of the morphological characters.

Conclusions: This study revealed congruent phylogenetic relationships from comparative methods/datasets, with some conflicts being the result of incomplete lineage sorting and ancient/recent hybridization events. The strong association between the clades and the biogeographic areas suggested that ancient dispersal events shaped the modern distribution pattern, and regional climatic factors may have resulted in the following in situ diversification. Climate cooling starting during the mid-Miocene is associated with the global expansion of Zamia to tropical South America that has dramatically driven lineage diversification in the New World flora, as well as the extinction of cycad species in the nowadays cooler regions of both hemispheres, as indicated by the fossil records.

Keywords: Zamia; Cycadales; biogeography; character evolution; gymnosperms; transcriptomics.

Fig. 1.

Morphology and habitat variations in selected taxa of Zamia. (A) Zamia pseudoparasitica, epiphytic in habitat, Panama; (B) Z. dressleri, corrugated leaves in habitat, Panama; (C) Z. soconuscensis, in montane forest, Chiapas (Mexico); (D) Z. pyrophylla, emergent leaf, Colombia; (E) Z. restrepoi, raised leaf venation details, Colombia; (F) Z. splendens, decumbent female strobili, Mexico; (G) Z. oreillyi, emergent leaf, Honduras; (H) Z. sandovallii, decumbent leaf, Honduras; (I) Z. onan-reyesii, rainforest habitat, Honduras; (J) Z. chigua, linear parallel leaf details, Colombia. Photographs by A. Lindstrom.

Fig. 2.

Phylogenetic tree of Zamia using coalescent (left) and concatenated (right) analyses, based on nucleotide dataset of 2901 SCNGs using all codon positions (nt) and first and second codon positions only (nt12). Support values are not mentioned if branches are maximally supported in both datasets. Otherwise, * and − indicate maximum support and branch support <80 %, respectively. Dotted branches highlight incongruence among two analyses. Major phylogenetic clades in the genus are indicated with black vertical bars with species names.

Fig. 3.

Spatiotemporal evolution of Zamia. (A) Chronograms and ancestral area reconstruction of Zamia derived from the 50-gene ML tree with topologies constrained to the coalescent tree (nt12), using three secondary calibration points derived from Coiro et al. (2023). Numbers 1–15 represent major divergence events in Zamia. Nodes 1 and 2 are mentioned in the inset, and the grey-shaded area of the inset is enlarged to indicate the position of nodes 3–15. Blue bars represent the 95 % HPD. The mean divergence times and 95 % HPSs are provided for each node of interest in Table 3. The pie charts indicate the ancestral area of each node (>5 % only). (B) The map of the Americas in the inset is enlarged to show the geographical distribution of major clades among the seven distinct areas of the genus distribution in Mega-Mexico and adjacent regions.

Fig. 4.

Macroevolution of Zamia. (A) Median rates of speciation (pink), net diversification (blue) and extinction (green) estimated by BAMM, with colour density shading to denote confidence in evolutionary rates through time. The unit of speciation, extinction and diversification is speciation events per million years and the rates of niche traits are unitless. Global surface temperature changes are denoted by the red curve using the dataset of Zachos et al. (2008). (B) Phylogenetic distribution of net diversification rate shifts on the dated phylogeny from TreePL. The net diversification rates are displayed on branches with colours from low (blue) to high (red) values.

Fig. 5.

Ancestral state reconstruction of (A) stem habit and (B) eophyll in Mesquite under the Mk1 model, on the phylogenetic tree of Zamia derived from coalescent (nt12) analyses. The pie chart at each node represents the probability of each character state for that morphological character.

Fig. 6.

Ancestral state reconstruction of (A) pinna plication and (B) pinna venation in Mesquite under the Mk1 model, on the phylogenetic tree of Zamia derived from coalescent (nt12) analyses. The pie chart at each node represents the probability of each character state for that morphological character.