Reconciling fossils with phylogenies reveals the origin and macroevolutionary processes explaining the global cycad biodiversity

Abstract

The determinants of biodiversity patterns can be understood using macroevolutionary analyses. The integration of fossils into phylogenies offers a deeper understanding of processes underlying biodiversity patterns in deep time. Cycadales are considered a relict of a once more diverse and globally distributed group but are restricted to low latitudes today. We still know little about their origin and geographic range evolution. Combining molecular data for extant species and leaf morphological data for extant and fossil species, we study the origin of cycad global biodiversity patterns through Bayesian total-evidence dating analyses. We assess the ancestral geographic origin and trace the historical biogeography of cycads with a time-stratified process-based model. Cycads originated in the Carboniferous on the Laurasian landmass and expanded in Gondwana in the Jurassic. Through now-vanished continental connections, Antarctica and Greenland were crucial biogeographic crossroads for cycad biogeography. Vicariance is an essential speciation mode in the deep and recent past. Their latitudinal span increased in the Jurassic and restrained toward subtropical latitudes in the Neogene in line with biogeographic inferences of high-latitude extirpations. We show the benefits of integrating fossils into phylogenies to estimate ancestral areas of origin and to study evolutionary processes explaining the global distribution of present-day relict groups.

Keywords: Antarctica; Cycadales; Greenland; fossil leaves; historical biogeography; total-evidence analysis.

Fig. 1

Global distribution of Cycadales. (a) Species richness of the 10 extant cycad genera across continents. (b) IUCN threat categories for 337 extant cycad species (redrawn from IUCN, 2022). (c) Map showing the extant distribution of cycad diversity (red areas) and sampled fossil localities (purple dots), indicating broader geographic distribution in the past.

Fig. 2

Bayesian total‐evidence dated phylogeny of Cycadales. This chronogram is the resulting consensus tree from the MrBayes analyses performed with the fossilized‐birth‐death model and an uncorrelated relaxed molecular clock. The tree includes 321 extant species and 60 extinct species with median divergence times along with 95% Highest Posterior Density (blue bars) for each node. C, Carboniferous; J, Jurassic; K, Cretaceous; N, Neogene; P, Permian; Pg, Paleogene; T, Triassic.

Fig. 3

Ages of extant genera and fossil placements. (a) Phylogenetic relationships for extant (genera are collapsed) and extinct cycads with support values (Posterior Probability indicated when > 0.3). Node support for extant genera is only indicated when < 1. (b) Posterior distributions for the crown ages of the extant genera. Eo, Eocene; M, Miocene; N, Neogene; O, Oligocene; Pg, Paleogene. Ma, million years ago.

Fig. 4

Historical biogeography of cycads. Estimates of ancestral areas were performed with a time‐stratified model in Dispersal–Extinction–Cladogenesis (DEC) with fossils included (a) and with fossils excluded (b). The extant genera have been collapsed to focus on deep‐time biogeography (for details within each genus, see Supporting Information Fig. S6 when fossils are included and Fig. S7 when fossils are excluded). The bottom‐right corner legend indicates colored areas used in this study corresponding to colored squares for each node, representing inferred ancestral area(s) with the DEC model, and colored circles for fossil species representing known distributions (except for extant genera with one or two species only). The red‐highlighted shades show the cycad expansion into Gondwana during the Jurassic and Cretaceous. The bottom‐left corner map represents the global paleogeography in the Jurassic (180 million years ago (Ma)). Paleomap used with permission © 2020 Colorado Plateau Geosystems Inc. Arrows indicate fossil species illustrated. Pictures from Mario Coiro. C, Carboniferous; N, Neogene; Perm, Permian; Pg, Paleogene.

Fig. 5

Biogeographic processes explaining the global distribution pattern of cycads. The number of dispersal events into a region and out of a region as well as the number of local extinctions (extirpations) are compared between analyses including fossils (a, b) and analyses excluding fossils (c, d). Area names: WP, West Palearctic; EP, East Palearctic; WN, West Nearctic; EN, East Nearctic; CA, Central America; WI, Caribbean Islands; SA, South America; AF, Africa; IN, India; WA, Southeast Asia; AU, Australasia; GR, Greenland; AN, Antarctica.

Fig. 6

Reconstruction of the latitudinal span of cycads during geological times. This estimate has been obtained using the method of Silvestro et al. (2018b) as implemented in Zhang et al. (2022). Gray polygon represents the reconstructed span, black dots represent the paleolatitude and age of fossil tips, while black triangles show the latitude of extant species. C, Carboniferous; J, Jurassic; K, Cretaceous; N, Neogene; P, Permian; Pg, Paleogene; Tr, Triassic.