Evidence for an extinct lineage of angiosperms from the Early Cretaceous of Patagonia and implications for the early radiation of flowering plants

Abstract

Summary The pinnately lobed Aptian leaf fossil Mesodescolea plicata was originally described as a cycad, but new evidence from cuticle structure suggests that it is an angiosperm. Here we document the morphology and cuticle anatomy of Mesodescolea and explore its significance for early angiosperm evolution. We observed macrofossils and cuticles of Mesodescolea with light, scanning electron and transmission electron microscopy, and used phylogenetic methods to test its relationships among extant angiosperms. Mesodescolea has chloranthoid teeth and tertiary veins forming elongate areoles. Its cuticular morphology and ultrastructure reject cycadalean affinities, whereas its guard cell shape and stomatal ledges are angiospermous. It shares variable stomatal complexes and epidermal oil cells with angiosperm leaves from the lower Potomac Group. Phylogenetic analyses and hypothesis testing support its placement within the basal ANITA grade, most likely in Austrobaileyales, but it diverges markedly in leaf form and venation. Although many Early Cretaceous angiosperms fall within the morphological range of extant taxa, Mesodescolea reveals unexpected early morphological and ecophysiological trends. Its similarity to other Early Cretaceous lobate leaves, many identified previously as eudicots but in some cases pre‐dating the appearance of tricolpate pollen, may indicate that Mesodescolea is part of a larger extinct lineage of angiosperms.

Fossil data do not support a long pre-Cretaceous history of flowering plants

“…To take two from families inferred to extend into the Jurassic, they place the Early Cretaceous lobate leaf Potomacapnos 5 in Papaveraceae (eudicots). However, the original description only cautiously compared it to Papaveraceae, and it shares more similarities in venation with the Early Cretaceous lobate leaf Mesodescolea , which appears to represent an extinct basal angiosperm line 6 . Similarly, Late Cretaceous flowers assigned to the mycoheterotrophic Triuridaceae (monocots) have smooth boat-shaped monosulcate pollen, unlike the spiny spherical inaperturate pollen of extant triurids 7 .…”

First fossil-leaf floras from Brunei Darussalam show dipterocarp dominance in Borneo by the Pliocene

“…However, the literature regarding out-of-Gondwana origins for dipterocarps seems to omit that Early Cretaceous deposits have been sampled across Gondwana for decades, and no fossil dipterocarps or likely relatives have been reported from hundreds of publications (among many others, Archangelsky, 1963 ; Banerji, 2000 ; Mohr & Friis, 2000 ; McLoughlin, Pott & Elliott, 2010 ; Nagalingum & Cantrill, 2015 ; Monje-Dussán et al, 2016 ). Importantly, angiosperms in Gondwanan Early Cretaceous floras are rare, show early stages in the evolution of leaf organization and other characters, and are not allied with derived eudicot families ( Mohr & Friis, 2000 ; Cúneo & Gandolfo, 2005 ; Nagalingum & Cantrill, 2015 ; Coiro et al, 2020 ; Pessoa, Ribeiro & Jud, 2021 ). All confirmed reports of fossil dipterocarps and related taxa in Africa and India ( e.g ., Ashton et al, 2021 ) are from much younger, post-Gondwanan strata, and even the Maastrichtian Dipterocarpus -type pollen from Sudan ( Morley, 2018 ) is ca.…”

A eudicot leaf from the Lower Cretaceous (Aptian, Araripe Basin) Crato Konservat‐Lagerstätte

“…First, some of these lobate eudicot‐like leaves predate the oldest occurrence of tricolpate pollen in their respective regions (Archangelsky et al, 2009; Puebla, 2009; Sun et al, 2011; Jud and Hickey, 2013; Jud, 2015; Coiro et al, 2020). Second, the Aptian herb Mesodescolea has lobate leaves with characters of the cuticle that are unusual for extant eudicots but common in the ANA lineages (Coiro et al, 2020). It is therefore possible that Mesodescolea and other early lobate angiosperms belong to one or more extinct groups among the ANA lineages or along the eudicot stem‐lineage prior to the evolution of tricolpate pollen (Doyle, 2012; Jud, 2015; Coiro et al, 2020).…”

“…Most examples of Early Cretaceous angiosperms with eudicot‐like foliage have been described from mid‐latitude deposits (Berry, 1911; Sun et al, 1998; Sun and Dilcher, 2002; Krassilov and Volynets, 2008; Archangelsky et al, 2009; Puebla, 2009; Sun et al, 2011; Jud and Hickey, 2013; Jud, 2015; Jud and Sohn, 2016; Golovneva et al, 2018; Coiro et al, 2020). The Crato Konservat‐Lagerstätte in Brazil is a late Aptian deposit in what was Northern Gondwana and an ideal place to look for low‐latitude examples of early angiosperms (Varejão et al, 2019, 2021; Mohr and Friis, 2000; Ribeiro et al, 2021).…”

“…Despite taphonomic bias in favor of perennial woody plants, most angiosperm macrofossils from Barremian–Aptian deposits for which habit may be inferred are the remains of herbaceous plants preserved in low‐energy wetland, riparian, or lacustrine deposits (Hickey and Doyle, 1977; Taylor and Hickey, 1990; Sun et al, 1998, 2002; Leng and Friis, 2003; Dilcher et al, 2007; Archangelsky et al, 2009; Puebla, 2009; Barral et al, 2013; Jud and Hickey, 2013; Jud, 2015; Du et al, 2021). Many are also characterized by complex lobate or compound leaves with ternate, twice pinnately lobed, or basipetal pedate organization typical of many herbaceous eudicots, but unusual outside of the clade (Puebla, 2009; Barral et al, 2013; Jud and Hickey, 2013; Jud, 2015; Coiro et al, 2020).…”