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

Abstract

Summary 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.

Embracing uncertainty: The way forward in plant fossil phylogenetics

“…This method works on dated phylogenies as well, but it can only illustrate the distribution of a single taxon per graph. RoguePlots are rather simple to use, being implemented in an R package (https://github.com/seraklop/RoguePlots/; for a short tutorial, see https://mariocoiro.blog/2020/12/02/how-to-represent-uncertainty-in-phylogenies-rogueplots-to-the-rescue/), and have been successfully applied to plant analyses (Coiro et al, 2020, 2023; López‐Martínez et al, 2023; Pessoa et al, 2023).…”

“…Although molecular phylogenetics remains the most widely used method of inferring the evolutionary history of living groups, the use of morphological data in phylogenetic inference has seen a renaissance in the last decade. This trend has been catalyzed by the development of techniques that allow the integration of fossils as tips in dated phylogenetic trees (Ronquist et al, 2012; Gavryushkina et al, 2014; Heath et al, 2014; Zhang et al, 2016), thus allowing the use of fossil information to better understand macroevolutionary processes and dynamics (Slater et al, 2012; Slater and Harmon, 2013) and biogeography (Zhang et al, 2022; Coiro et al, 2023). Some authors have even advanced the possibility that the inclusion of fossil taxa using morphology could lead to more accurate phylogenetic hypotheses (Koch and Parry, 2020; Mongiardino Koch et al, 2021).…”

“…Even within this renaissance, researchers interested in morphological phylogenetics applied to fossil plants have had to face more challenges than colleagues working on other fossil groups. Phylogenies including plant fossils, though able to retrieve robust relationships (Schoenenberger et al, 2020; Matsunaga et al, 2021; Tang et al, 2022; Coiro et al, 2023; López‐Martínez et al, 2023), sometimes retrieve uncertain relationships with low support or lack resolution compared to molecular phylogenies. This low support is partly due to the nature of the plant fossil record itself, composed of separate organs with differing levels of available characters for phylogenetic analyses (Bateman and Hilton, 2009).…”

Why plant diversity and distribution matter

“…Contributions to this collection also show how building solid phylogenomic frameworks (Villaverde et al ., 2023) and integrating phylogenies and fossils (Coiro et al ., 2023) – in addition to improved taxonomic and geographical information – hold the future for more reliable and precise inferences of plant macroevolution.…”

Evolutionary and ecological trends in the Neotropical cycad genus Dioon (Zamiaceae): An example of success of evolutionary stasis

“…The cycads (order Cycadales) represent one of the most ancestral lineages of seed plants (Coiro et al, 2023;Condamine et al, 2015;Crisp & Cook, 2011;Liu, Wang, et al, 2022;Nagalingum et al, 2011). They originated in the Carboniferous, around 270 Ma ago, as a sister lineage of the Ginkgoales (Liu, Wang, et al, 2022;Rudall & Bateman, 2010;Wu et al, 2013).…”