Late Permian seed-plant evolution The great evolutionary expansion of seed plants took place in the Mesozoic era, which began after the Permian mass extinction 252 million years ago. Blomenkemper et al. report the discovery of seed-plant fossils from Late Permian (252-million- to 260-million-year-old) deposits on the margins of the Dead Sea in Jordan. This area represents an equatorial habitat with pronounced dry seasons. These fossils, which include the earliest records of conifers, push back the ages of several important seed-plant lineages. Some of these lineages appear to span the mass extinction event at the end of the Permian, which suggests that the communities they supported may have been more stable than expected over this transition. Thus, early evolutionary innovations can occur in drought-prone tropical habitats—which rarely offer the conditions needed for fossil preservation. Science, this issue p. 1414

Abstract The latitudinal biodiversity gradient today has deep roots in the evolutionary history of Earth’s biota over geologic time. In the marine realm, earliest fossil occurrences at low latitudes reveal a tropical cradle for many animal groups. However, the terrestrial fossil record—especially from drier environments that are thought to drive evolutionary innovation—is sparse. We present mixed plant-fossil assemblages from Permian equatorial lowlands in present-day Jordan that harbor precocious records of three major seed-plant lineages that all became dominant during the Mesozoic, including the oldest representative of any living conifer family. These finds offer a glimpse of the early evolutionary origins of modern plant groups in disturbance-prone tropical habitats that are usually hidden from observation.

Tropical regions today harbor the greatest biodiversity on our planet, with species richness decreasing toward the poles (1). Explanations for this phenomenon lie not only in present-day climate gradients and continent configurations, but also in the deep evolutionary histories of organism groups over geologic time (2, 3). One hypothesis is that equatorial ecosystems function as “evolutionary cradles”—a term introduced by botanist G. Ledyard Stebbins (4)—that generate new lineages at higher rates than extratropical regions. Earliest originations in such equatorial cradles have been well documented for marine organisms (2, 3, 5, 6). To what degree the evolution of terrestrial biota follows a similar pattern, however, remains controversial (3, 7); paleobotanical evidence in particular (8–10) is subject to strong preservation bias, partly because drought-prone equatorial habitats that are thought to spawn plant evolutionary innovations rarely preserve fossils (3, 11, 12). Here, we report a Permian flora from the Middle East that holds the earliest records of three major seed-plant lineages, among these the oldest fossil record of any living family of conifers.

Toward the end of the Paleozoic, the vegetation of the supercontinent Pangea differentiated into four major floristic regions: the hot and dry equatorial expanse of central Pangea (Euramerica); a realm of humid tropical rainforest stretching mainly across the large island chains in the eastern Tethys (Cathaysia); and two temperate to cool realms in the northern (Angara) and southern (Gondwana) mid- to high latitudes (12). Permian plant-bearing deposits from coastal tropical lowlands, however, yield mixed floras with typical members from different floral provinces (12–14), indicating that these seemingly separate geographic realms were climate-controlled biomes with plant communities adapted to local habitat conditions (12, 13). From a macro-evolutionary perspective, the xeromorphic, drought-tolerant components of such mixed floras are especially interesting because these assemblages occasionally contain so-called “Methuselah taxa” (12)—rare and unexpectedly early occurrences that reveal new lineages and evolutionary innovations to be much older than previously thought and that normally elude detection in the fossil record because they thrived in drier environments with very limited preservation potential (11, 12, 15).

We collected plant-fossil assemblages from the Umm Irna Formation, an up to ~85-m-thick succession of Permian alluvial deposits exposed along the eastern shore of the Dead Sea in Jordan (fig. S1 and table S1). What makes these fossil assemblages notable among coeval mixed floras is the quality of preservation; many of the fossils are mummified with pristinely preserved cuticles (14, 16), the microscopic diagnostic features of which enable a systematic placement even in the absence of fertile organs (17). The Umm Irna Formation is intercalated with erosional contacts between the Cambrian Umm Ishrin Sandstone Formation below and the basal Triassic Ma’in Formation above. Independent evidence from plant macro- and microfossils (14, 16), from conodont and foraminifer biostratigraphy (18), from sequence stratigraphy (18), and from lithostratigraphic correlation with other well-dated successions on the Arabian Plate (16) together provides a robust age framework (19). The Permian-Triassic boundary occurs at or immediately above the base of the Ma’in Formation, and the underlying Umm Irna Formation is Lopingian (Late Permian), most likely Changhsingian (latest Permian), in age (18, 19). During that time, the region was an equatorial coastal lowland along the western Tethys margin at a latitude of about 15°S and had a hot, subhumid climate with pronounced dry seasons (14, 16, 18, 19). The depositional environment was a richly structured riverscape that harbored varied plant communities, depending on local habitat conditions (19). As a result, different sedimentary subenvironments have preserved distinct plant-fossil assemblages (19) (table S1).

Of particular note are fossil assemblages from point-bar and abandoned-channel deposits (19) that contain diverse accumulations of plant remains washed in from surrounding riparian forests and from drier habitats. These assemblages have now yielded the earliest bona fide records of three major seed-plant lineages that became dominant in the Mesozoic: Corystospermales, Bennettitales, and Podocarpaceae (Fig. 1). Previous reports of Dicroidium, a type of corystospermalean foliage, from the Umm Irna Formation remained controversial because the genus is traditionally regarded as an index fossil for the Gondwanan Triassic and because fertile organs were lacking (20). New material, including numerous large frond fossils (Fig. 1A) and the affiliated fertile organs (Fig. 1C), now unequivocally confirms the presence of corystosperms in the Permian of Jordan. So far, at least six Dicroidium species can be distinguished. Bennettitales is an extinct group of seed plants with a cycadlike growth habit and compound flowerlike reproductive organs. These plants have been known mainly from the Mesozoic, the earliest record being from the Middle Triassic (21). Because of their sophisticated mode of sexual reproduction, which in many ways resembled that of modern angiosperms, some authors consider Bennettitales to be basal members of the group of plants that gave rise to crown-group angiosperms more than 100 million years later (22, 23). We collected large fragments of entire-margined Nilssoniopteris leaves and of pinnate Pterophyllum fronds (Fig. 1, D and I), as well as dispersed cuticle pieces, all showing the syndetocheilic type of stomata (Fig. 1, J to M) diagnostic of Bennettitales (17, 21).

Fig. 1 Selected precocious records of iconic Mesozoic plant groups in the Late Permian Umm Irna Formation, Jordan. Pictured are Corystospermales (A to C), Bennettitales (D and I to M), Podocarpaceae (E to H), Elatocladus twigs (N and O), and zamiinean cycads (P to S). [(A) and (B)] Almost complete fronds of Dicroidium robustum (A) (sample JO15-4-120) and D. irnense (B) (JO15-4-4); (C) a Pteruchus pollen organ (JO17-7-63); [(D) and (I)] frond fragments of Pterophyllum [(D) JO15-5-115 and (I) JO15-5-71]; [(E) to (H)] a shoot fragment (E) (JO15-5-39), an isolated needle (F) (JO17-5-6), and in situ cuticles [(G) and(H)] (JO17-5-6SL-001 and -002) of an undescribed podocarp; [(J) and (L)] a bennettitalean cuticle with characteristic syndetocheilic stomata [(L) JO17-4B-92/94SL-001 to -005], obtained in situ from a Pterophyllum leaflet (JO17-4B-92); [(K) and (M)] a dispersed bennettitalean cuticle with syndetocheilic stomata (M) found among residues of bulk-macerated rock samples (JO15-5A-50SL-011, -SL-013, and -SL-014); [(N) and (O)] part and counterpart detail of an Elatocladus-type conifer branch [(N) JO15-5-52 and (O) JO15-5-71]; [(P) and (Q)] Ctenis-like cycad leaf with anastomosing veins (Q) (JO17-5A-27); [(R) and (S)] dispersed Pseudoctenis cuticles found among residues of bulk-macerated rock sample (JO15-5-52SL-003 and -005). Scale bars, [(A) and (B)], 2 cm; [(C) to (F), (I), and (N) to (P)], 1 cm; (Q), 1 mm; [(G), (J), (K), and (R)], 100 μm; (H), 50 μm; [(L), (M), and (S)], 20 μm.

Podocarpaceae is the second-largest extant family of conifers and was an important component of Mesozoic floras worldwide (17, 24). Before now, the earliest records of the group were from the Lower Triassic (24). Conifer twigs from Jordan bear helically arranged, single-veined needles that are twisted near the base to become flattened into a single plane (Fig. 1, E, N, and O). Their cuticles (Fig. 1, F to H) show overall smooth outer surfaces and longitudinally oriented, paratetracytic stomata in rows and tight chains (Fig. 1, G and H), a combination of macro- and micromorphological features that is diagnostic of Podocarpaceae (25). Other single-veined but shorter-leafed forms (Fig. 1, N and O) similar to the common Mesozoic foliage taxon Elatocladus may also belong to Podocarpaceae or to another modern conifer family (24). Further unexpected finds are various remains of zamiinean cycads such as Ctenis (Fig. 1, P and Q) and Pseudoctenis (Fig. 1, R and S), including leaflets whose characteristic epidermal anatomy (Fig. 1, R and S) agrees closely with those of Late Triassic forms (17, 26). Notably, however, all these precocious occurrences of typically post-Paleozoic seed-plant lineages occur intermixed with characteristic Paleozoic plant taxa, such as Noeggerathiales (Discinites), Nystroemiales (Nystroemia), rare gigantopterids, Laurasian Permian conifers (Quadrocladus and Otovicia), and putative ginkgophytes (Rhipidopsis) (fig. S2 and table S1) (17).

Plant assemblages from deposits representing permanently waterlogged back-swamp environments that occur locally in the Umm Irna Formation (19) are, by contrast, dominated by plants characteristic of the tropical ever-wet Cathaysian flora, including various gigantopterid seed ferns (Gigantopteris, Gigantonoclea, and Fascipteris), the sphenophyte Lobatannularia, and putative ginkgophytes (Saportaea and Rhipidopsis) (fig. S2 and table S1), with occasional occurrences of small Glossopteris leaves (fig. S2)—the classical index fossil of the Permian southern Gondwana flora (13, 17).

Altogether, the peculiar plant-fossil record of the Umm Irna Formation not only reveals a melting pot of plant communities considered typical of different Paleozoic floristic regions, but also yields precocious records of three major seed-plant lineages: the chiefly Mesozoic groups Bennettitales and Corystospermales, as well as Podocarpaceae, which marks the earliest fossil record of any living group of conifers. Before the discoveries from the Umm Irna Formation, all three groups were thought to have first appeared some time during the Early or Middle Triassic in the wake of the end-Paleozoic mass extinction (14, 16, 17, 21, 24).

The unexpectedly early fossil records for these groups will aid in calibrating the age framework of seed-plant phylogenies and push back divergence-age estimates for major lineages still deeper into the Paleozoic. Moreover, the biostratigraphic ranges of Bennettitales, Corystospermales, and Podocarpaceae alike can now be traced back across the Permian-Triassic boundary––the date that marks the greatest mass extinction of animal groups in Earth’s history (27). From a bottom-up perspective, our finds thus add at least three groups to the growing list of major plant lineages that did not vanish at the end of the Paleozoic, confirming that land plants—and perhaps terrestrial biotas as a whole—were less affected by global biotic crises than previously thought (28). Instead of a sudden, catastrophic extinction followed by a restoration of ecosystems with entirely new groups, the vegetation changes across the Permian-Triassic boundary appear more and more to reflect the gradual demise of particular groups and the takeover of vacated resource spaces by others that had already existed long before, but under conditions unfavorable for fossilization. In this respect, the later evolutionary trajectories of the various plant groups that occur side by side in the Umm Irna Formation reveal a distinct pattern of extinction selectivity: Competitively favored groups that dominated wetland floras in stable, mesic environments—including both Cathaysian (gigantopterid) and Gondwanan (glossopterid) taxa—would vanish with the warming climates in the aftermath of the end-Permian biotic crisis (29). More stressed and disturbance-prone habitats, by contrast, sheltered the evolutionary cradles for highly adaptable seed-plant groups that would not only persist through the crisis interval, but also emerge to become some of the most iconic plant groups of the Mesozoic. Bennettitales, Cycadales, and podocarp conifers persisted in equatorial latitudes and expanded their ranges “out of the tropics” (5, 6) during the Triassic, reaching worldwide distribution during the later Mesozoic (17, 24). The Dicroidium plants even appear to have abandoned their tropical cradle. They migrated southward and became the dominant canopy trees in temperate forests across the mid- to high-latitude regions of Gondwana during the Triassic (14, 16, 17), before they themselves would eventually disappear in the Jurassic and leave their youngest-known fossil remains in polar refugia of present-day Antarctica (30).

The Umm Irna Formation allows a glimpse into a rich evolutionary cradle of modern seed-plant lineages. The geological and paleoenvironmental setting of this fossil deposit renders a more precise search image for future paleontological exploration. We anticipate that targeted search in similar paleo-equatorial lowland settings will help uncover the early origins of evolutionary innovation.

Supplementary Materials www.sciencemag.org/content/362/6421/1414/suppl/DC1 Materials and Methods Supplementary Text Figs. S1 and S2 Table S1 References (31–63)

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Acknowledgments: We thank the University of Jordan (Amman) for support; N. S. and H. S. Badandi (Irbid, Jordan), F. Scholze and J. W. Schneider (Freiberg, Germany), and S. Voigt (Thallichtenberg, Germany) for fieldwork assistance; and S. McLoughlin (Stockholm, Sweden), M. Pole (Toowong, Australia), C. Pott (Münster, Germany), and three anonymous reviewers for helpful discussion. Funding: Financial support was provided by the German Science Foundation (DFG Emmy Noether grant BO3131/1-1, “Latitudinal Patterns in Plant Evolution,” to B.B. and DFG grants KE584/11-1+2 and KE584/20-1 to H.K.). Author contributions: All authors contributed equally to the work. Competing interests: The authors declare no competing interests. Data and materials availability: All data are available in the main text and the supplementary materials; all fossil material is housed in the palaeobotanical collections at the Institute of Geology and Palaeontology of the Westfälische Wilhelms-Universität (Münster, Germany).