Cretaceous fire-resistant angiosperms

doi:10.21203/rs.3.rs-494355/v1

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Cretaceous fire-resistant angiosperms

https://doi.org/10.21203/rs.3.rs-494355/v1

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published 31 Jan, 2022

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Background: Flowering plants (angiosperms) dominate most global ecosystems today, but their rapid Cretaceous diversification has remained poorly understood ever since Darwin referred to it as an ‘abominable mystery’. Although numerous Cretaceous fossil flowers have been discovered in recent years, most are represented by incomplete charcoalified fragments that do not preserve delicate structures such as complete petals and surface textures, which means that their similarity to living forms is often difficult to discern. The scarcity of information about the ecology of early angiosperms makes it difficult to test hypotheses about the drivers of their diversification. Among other factors, frequent fires in the Cretaceous have been postulated as having possibly facilitated the rise of angiosperms. However, to date no early fossil angiosperms displaying fire-adapted traits have been known, making the role of fire in shaping Cretaceous floras uncertain.

Results: We report the discovery of two exquisitely preserved fossil flower species, one identical to the inflorescences of the extant crown eudicot genus Phylica and the other recovered as a sister group to Phylica, both preserved as inclusions in Cretaceous amber from northern Myanmar (~99 Ma). These specialized flower structures, named Phylica piloburmensis sp. nov. and Eophylica priscastellata gen. et sp. nov., were adapted to surviving frequent wildfires, providing the earliest evidence of fire-resistance in angiosperms. The fossils suggest that fire was a significant selective force in Cretaceous angiosperm floras and that adaptations to fire resistance in some eudicot clades have been conserved for at least 99 Ma. This morphological stasis encompasses a range of floral characters, including the production of ‘pseudo-flowers’, and characteristic fruit and pollen architecture. Given its morphological distinctiveness, the Eophylica-Phylica clade represents one of the first well-documented angiosperm ‘living fossil’ genera from the Cretaceous.

Conclusion: Our study suggests that core eudicots with specialised flower morphology displaying hallmarks of fire resistance and identical to those of the extant south African genus Phylica, had originated by the mid-Cretaceous (~99 Ma). Palaeoenvironmental reconstructions indicate that these plants lived in conditions similar to those of present-day southern Africa where 70% of taxa survive frequent burning, and that fire resistance was probably widespread in the fire-prone Cretaceous. The results also provide new insights into the biogeographic origin of at least one element of the highly endemic Greater Cape Region biodiversity hotspot flora biota.

Plant Physiology and Morphology

Plant Molecular Biology and Genetics

early flowers

angiosperm evolution

living fossil

Cretaceous

Myanmar amber

wildfire

Gondwanan origin

Fynbos flora

Cretaceous Terrestrial Revolution

Fire is a pervasive force across terrestrial biomes, shaping ecosystem composition and distribution. While fire was more prevalent in some periods of the Earth’s past and is thought to have played a pivotal role in the Cretaceous diversification of flowering plants, little is known about the responses of ancient vegetation to fire. Here we describe new flowers from Cretaceous amber (~99 Ma) that display hallmarks of fire resistance, highlighting the role of fire in shaping the diversity of the earliest angiosperms. Eophylica and fossil Phylica demonstrate that despite the seemingly ephemeral and disturbance-dominated nature of periodically burnt habitats, fire-prone angiosperm clades can persist over long geological timescales.

The diversification of flowering plants was one of the major episodes in the history of life that transformed global ecosystems, bringing about the diversification of insects, amphibians, mammals, early birds¹^–⁵, and other clades, ultimately marking the first time in geological history when life on land became more diverse than life in the sea⁶. The rapid radiation of angiosperms, between ~135 Ma and ~65 Ma, that led flowering plants to dominate many land environments by the end of the Cretaceous and replace the incumbent gymnosperms, has fascinated evolutionary biologists starting with Darwin who famously referred to the angiosperm radiation as an “abominable mystery”. However, our knowledge of the early angiosperm’s most distinctive feature, the flower, is scarce owing to its delicate construction and thus low fossilization potential. Much of what is known about early angiosperm floral diversity comes from flowers that were rendered biologically inert through burning and conversion to charcoal⁹, but this mode of preservation is only partial, reducing the flower core with petals and surface features to mere stubs. In the absence of fine morphological detail, there has been a tendency to reconstruct such remains with the presumption that such flowers must have been simpler than extant forms. As a result, the ecology of early angiosperms remains poorly known, hampering attempts at disentangling the potential drivers of their diversification. Diverse ecological explanations have been proposed to account for the rapid radiation of angiosperms in the Cretaceous, including co-diversification with insect pollinators, high growth rates, adaptation to new fire regimes, and evolution of novel dispersal modes¹⁰, but many of these remain hardly testable without a better appreciation of the ecological diversity of early flowering plants.

Amber, fossilized resin of ancient plants that often preserves flowers with life-like fidelity alongside their pollen and fruits, offers an alternative but little-explored window into early angiosperm diversity. Here we document two types of fossil flowers, one identical to those of extant Phylica (Rhamnaceae) and another sister to the genus, preserved in Cretaceous amber from the Hkamti and Tanaing mines (Supplementary Figs. 1–3) in northern Myanmar dated to at least 99 Ma (Supplementary notes)¹¹^–¹⁴. These fossil flowers were previously misidentified as conifers¹⁵ or green algae¹⁶, and are quite common in the Tanaing mines, where the flora is dominated by gymnosperms including the extinct Bennettitales (Supplementary Fig. 4) and accompanied by diverse angiosperms¹⁷^–¹⁹. The exceptionally preserved flowers possess linear pubescent xeromorphic leaves (seemingly needle-like and tightly clustered with densely stellate or linear hairs) typical of fire-prone vegetation adapted to dry conditions (Fig. 1). Our results provide the first direct evidence of fire-resistant angiosperms from the Cretaceous, supporting the hypothesis that fire represented a biologically significant selective pressure in some Cretaceous ecosystems. The fossils demonstrate that specialized floral adaptations associated with resistance to frequent burning arose early in angiosperm evolution and remained more or less unchanged for over 99 Ma in Rhamnaceae. Extant Phylica is restricted to the South African Cape biodiversity hotspot and represents one of the most characteristic members of the endemic Fynbos flora²⁰^,2¹. The finding of inflorescences related to and even identical with Phylica in a mid-Cretaceous Gondwanan deposit backdates the origin of a key component of the Fynbos by ~70 Ma²² and suggests that at least this distinctive element of the Fynbos flora may represent an ancient type similar to the floras of the fire-prone Cretaceous²³.

Ecomorphological conservatism in fire-resistant Rhamnaceae

Our fossils preserve the primary reproductive features characteristic of extant Phylica, a diverse genus within the Rhamnaceae, in which all ~150 extant species are endemic to southern Africa²⁴^,²⁵. Specifically, leaves clustered at the twig tip surrounding either a flower, or a ‘pseudo-flower head’, is a feature unique to Phylica (Fig. 1 and Supplementary Figs. 7–20 and Supplementary Video 1)²⁶. Based on the presence or absence of petals, the number of sepals, and the form of hairs of the indumentum, we assign our fossils to two new species: Eophylica priscastellata gen. et sp. nov. (Figs. 2–3) and Phylica piloburmensis sp. nov. (Fig. 4 and Supplementary Fig. 6), the first character reflecting morphologies seen in extant Phylica²⁶. A close relationship between Eophylica and Phylica is supported by comparative morphological and phylogenetic reconstruction based on flowers, fruits, and pollen grains (Figs. 2–4 and Supplementary Figs. 21–31 and Supplementary Videos 2–3). Eophylica can be distinguished from Phylica on the basis of the number of sepals and the absence of petals. The second species is morphologically indistinguishable from extant Phylica, and our phylogenetic analyses recovered the species as robustly nested within the Phylica clade. Given the completeness of our observed character suite, with the exceptional fidelity of amber preservation, that flower morphology is the greatest source of data for ascribing species to supraspecific taxa, and the robustness of our phylogenetic results, we have placed this species in the extant genus Phylica. This greatly extends the age of this clade and represents the first extant angiosperm genus documented from the Mesozoic. While this seems controversial, we believe the extraordinary nature of these fossils and the data compel such a conclusion. Extant species in Myanmar amber are exceptionally rare, but are known to occur, and believe future data shall corroborate our conclusions regarding the identity of P. piloburmensis. We provide formal descriptions of the new fossil taxa in the Supplementary Material.

The clustered, needle-like dry leaves are typical of fire-prone angiosperms (Fig. 1)^16,23. Taxonomically, needle-like leaves clustered around the stems of a small shrub (Fig. 1 and Supplementary Figs. 7–20) are typical of Phylica and quite distinct from other genera of Rhamnaceae²⁶. Non-Phylica species in Rhamnaceae have broader leaves, except for some species in the genera Trymalium, Siegfriedia, and Colletia. Specialised narrow leaves have been considered an adaptation to the relatively dry Cape climate²⁷, and frequent wildfires²⁸. Many Fynbos angiosperms (e.g., Erica (Ericaceae), Aspalathus (Fabaceae), Ruschia (Mesembryanthemaceae), and Agathosma (Rutaceae)²⁰) and some non-Fynbos clades (e.g., Brunia and Berzelia (Bruniaceae)) also have narrow, clustered leaves. However, species of Phylica differ in having one or more of the following²⁶: leaves at the tip of the stem form ‘pseudo-flower heads’ unique to the genus (Fig. 1); leaves and flowers are covered by dense hairs; unarmed but villous-pubescent, branched twigs; the absence of stipules, and leaves with only one main vein (Supplementary Figs. 7–20).

Importantly, the typical pseudo-flower head in these fossils is distinctive within angiosperms²⁶. It is exclusive to some extant species of Phylica (e.g., P. pubescens and P. plumosa; Supplementary Fig. 10e–j)²⁶^,²⁹, where it represents an intermediate developmental stage from vegetative growth to the flowering phase (Fig. 1 and Supplementary Figs. 7–20 and Supplementary Video 1). The head comprises many tightly clustered scale-like leafy bracts, with mature leaves or bracts (below the true flower) developing later. Despite having a similar ‘head’ shape, the pseudo-flower bracts are morphologically distinct from those of the true flower (Fig. 2m).

True flowers of Phylica are small (~1.0 mm), capitated, 5(4)-merious, have an inferior ovary, and are densely pubescent. They combine the following diagnostic characters (Figs. 2–4 and Supplementary Figs. 21–26 and Supplementary Video 2)^26,29,30: flowers are terminal/solitary and include leafy or scale-like bracts; the flowers are semi-opened; sepals are enlarged and triangular; sepals have a prominent median vein; receptacles are turbinate in shape; the petals are either small and alternate with the sepals or are completely absent; stamens are opposite the petals; the disc is intrastaminal, thin to more or less fleshy; the ovary is below the disc and completely fused to the receptacle; the style is columnar, simple, shorter than the calyx tube; and the stigma is slightly lobed. In extant Phylica, such tubular flowers are pollinated by long-proboscid flies^26,30. Both fossils presented herein have a lengthened calyx tube (Figs. 2 a, c–h, 4e–g and Supplementary Figs. 21–24, 26), corresponding with coeval long-proboscid flies and scorpionflies known from Myanmar amber^31,32.

The fruits of the two new fossil species are typical capsules (Supplementary Figs. 3f, 4k, 27–28 and Supplementary Video 3). Although capsule-like fruits are common in Rhamnaceae, Phylica fruit morphologies are shaped by their specific flower characters (such as the lengthened calyx tube and dense hairs). Differing from other capsules that lack sepal elements and usually have an exposed mature pistil, fruits of Phylica and Eophylica are crowned by the persistent calyx (or sepal) that includes a hidden pistil (Figs. 3f–h, 4k–l). The pericarp develops from the base of the persistent calyx, and in the fossil fruit appears hard, ribbed (Fig. 3f and Supplementary Fig. 27), or covered with thick hairs originating from the flower (Fig. 4k and Supplementary Fig. 28). As in extant species²⁶, fossil fruits of Eophylica and P. piloburmensis are significantly larger than the flower (≥5 mm wide) (Supplementary Figs. 27, 28). Similar fruits occur in the genus Rosa in Rosaceae, but those fruits have the achenes inside, rather than having septal polycarpels as in our fossils and extant Phylica (Fig. 4m and Supplementary Fig. 27 m, n). As in extant Phylica²⁶, petals are either present or absent in our fossil flowers, with E. priscastellata lacking petals (Fig. 3a,b) and P. piloburmensis possessing petals (Fig. 4a).

Several pollen grains of similar morphology exist within our flower specimens (Figs. 2n, 4b and Supplementary Fig. 29). Although we failed to resolve a clear exine pattern, these grains exhibit characters similar to those of extant Phylica (Fig. 2t–v and Supplementary Fig. 29), namely single grains with an isopolar, 3-colporate, oblate-spheroidal, and triangular in polar view. An affinity with the Rhamnaceae is further supported by the following features³³: (i) medium-sized with polar axes of 21–24 μm and equatorial diameters of 18–21 μm (P/E ratio: 1.2); (ii) colpi long, narrow and with blunt ends; and (iii) the middle of the aperture lalongate, with two ends connected with a thinned part of the exine to form an H-shape (Fig. 2q–v and Supplementary Fig. 29).

Our fossils also preserve several other features whose combination is diagnostic of the family Rhamnaceae³⁴. As in our fossils, extant Phylica is a morphologically divergent clade of the Rhamnaceae that exhibits only some plesiomorphic characters seen in the family²⁶. Although a lengthened cyathiform calyx tube and enfolding sepals and petals are important flower characteristics of living Phylica, they obscure important internal Rhamnaceae characters (i.e., four- or ﬁve-parted with a single whorl of stamens opposite the petals). We used micro-XCT scanning to show that our fossils preserve simple leaves, small flowers with 5(4)-merious sepals (five in P. piloburmensis and eight (2 × 4-merious) in E. priscastellata), which are valvate in the bud (Figs. 2b,l and 4e–g); five or eight (2 × 4-merious; E. priscastellata) stamens, that alternate with the sepals and opposite the petals and anthers, which are tightly enfolded by the hooded petal apices (if petals are present; P. piloburmensis) (Fig. 4a and Supplementary Figs. 21n, 22l,m and 23k); and the presence of an intrastaminal disc (Fig. 2b)³³. These features, combined with crowding leaves (Fig. 1), are characteristic of Rhamnaceae³⁵.

Our new fossil species exhibit other features common to extant Phylica. In E. priscastellata, the leaves and twigs are like those of extant P. pubescens or P. ambigua (Supplementary Fig. 10), but the presence of stellate hairs and absence of petals distinguish it. Its fruits lack a covered indumentum as in extant P. parviflora (Supplementary Fig. 27 m, n). Moreover, the leaves, flower and fruit characteristics of P. piloburmensis are also present in many other extant species of Phylica (represented by P. axillaris; Fig. 4 c, h–j, m, n)²⁶. Overall, the unique combination of characters in our fossil flowers and fruits suggest that they represent an early form of Phylica, rather than other angiosperm clades³⁶.

Phylogenetic analysis integrating morphological and molecular partitions (Supplementary notes) confirmed crown-group membership of both fossil species (Supplementary Fig. 30). One major character (the presence of stellate hairs) makes the fossil E. priscastellata different from all extant species of Phylica (Supplementary Table 1). Ancestral-state reconstruction based on the phylogenetic tree shows stellate hairs were present in the common ancestor of the tribes Phyliceae and Pomaderreae (Supplementary Fig. 31). Since extant species of Pomaderreae are only distributed in Australia and New Zealand (i.e., Gondwana)²⁹, this demonstrates a common origin of stellate hairs in these two Gondwanan clades. All in all, our fossils provide evidence of a remarkable case of morphological, and probably also ecological, conservatism within a crown-eudicot clade since the mid-Cretaceous.

Early origin of fire resistance in the Cretaceous

The mid-Cretaceous (Albian–Turonian; 112–90 Ma) was anomalously warm, with some of the highest temperatures in Phanerozoic geological history³⁷ and a relatively shallow temperature gradient between the poles and the tropics. Elevated atmospheric oxygen levels in the Cretaceous (23–29% compared with 21% at present) and abundance of charred plant fossil remains in the rock record suggest that fires were frequent during this period. Some hypotheses of angiosperms diversification highlight that Cretaceous fire regimes may have opened land up for the first flowering plants, whose rapid colonization of regeneration gaps may have provided an advantage over the then-dominant gymnosperms that are intrinsically slower growing^40,41. By providing a new source of fuel, angiosperms may have also substantially altered the existing fire regimes, to the disadvantage of gymnosperm trees. However, the role of fire in fuelling the diversification of angiosperms has proven difficult to test. In fact, the earliest angiosperms have been reconstructed as weedy understory herbs, shrubs and small trees growing in humid and aquatic habitats⁴⁴, making it unclear how these plants may have benefited from Cretaceous fire regimes.

Previous molecular clock studies have inferred a Cretaceous origin of fire-proneness in some gymnosperm (Pinaceae) and angiosperm (Proteaceae, Myrtaceae, Haemodoraceae, and Restionaceae^–) lineages. However, direct palaeontological evidence of fire-adapted traits (i.e., those that that promote survival or reproductive success in the presence of wildfire⁵¹), are scarce, primarily because such traits evidently have low preservation potential. Cones that open to release seeds in the presence of fire (serotiny), have been reported from mid-Cretaceous gymnosperms, namely Widdringtonia (Callitroideae; Cenomanian), Protodammara, Sphenolepis, and Dammara (Cupressaceae; Cenomanian–Turonian⁵¹). To our knowledge, no Cretaceous angiosperms possessing fire-adapted traits have been known to date. While charcoal (fusain) and fire scars⁵⁴ on fossil trees indicate the antiquity of fire-proneness, these lines of evidence do not show if ancient fire regimes were sufficient to have an evolutionary impact on early flowering plants and whether these plants possessed fire-adapted traits⁵⁵.

Fossil Eophylica and Phylica inflorescences preserve unambiguous morphological hallmarks of fire resistance. Fire causes direct, or indirect, fatal damage to plant hydraulic systems, and the burned plants ultimately die of drought⁵⁶. Many fire tolerance plants are ‘drought-resisters and Eophylica-Phylica belong to this group. Numerous Cape species (such as species in families Ericaceae and Proteaceae) that are drought-resisters are able to produce new growth after fires, from buds on buried lignotubers at the base of killed stems⁵⁶. In contrast, some broad-leaved plants (such as banana) are typically adapted to a moist environment but are quite sensitive to heating, and quickly die after suffering significant water stress immediately post-fire⁵⁶. Phylica are small shrubs whose clustered, needle-like dry leaves are typical of fire-prone vegetation; these characters in turn ensure relatively rapid renewal after fire and confer resistance to severe drought. Phylica flowers are surrounded by several leaves, which may provide protection from direct heat during fire. While some extant members of the genus Phylica typically do not survive wildfires, which may in itself have an adaptive value in environments that burn frequently⁵⁷, their seeds accumulate in the soil and germinate after fire⁵⁸. Their relatively small and rounded seeds are easily incorporated into the soil and reach greater depths, which is linked to their ability to form long-term persistent seed banks. The discovery of unambiguous morphological adaptations to fire tolerance make Eophylica and P. piloburmensis the earliest fire-adapted angiosperms in the fossil record. This pushes the origin fire resistance in crown angiosperms back to 99 Ma, into the mid-Cretaceous.

While the exquisitely preserved Eophylica and Phylica flowers support the hypothesis that Cretaceous fire regimes did exert a significant selective pressure on early angiosperms, the extent to which Cretaceous fire regimes may have promoted the spread of early angiosperms remains open to testing. Palaeofire models suggest that intense Cretaceous fires supported by novel fuels from weedy flowering plants may have enabled fast-growing angiosperms to outcompete tall gymnosperm trees⁴². However, since the drivers of angiosperm diversification appear to be largely clade-specific, it is likely that the changing fire regimes were just one of many factors associated with angiosperm radiation. Future discoveries of exquisitely preserved plants in Cretaceous amber deposits may shed further light on the how widespread fire-related traits were in early angiosperms.

An early Gondwanan origin for the Fynbos

Fossil Eophylica and P. piloburmensis flowers are distinct from those of any angiosperms that grow in the subtropics of northern Myanmar today. Phylica is endemic to the fire-prone Fynbos flora of the South African Cape. The Fynbos represents one of the most remarkable global floral biodiversity ‘hotspots’, characterized by unique species richness and endemism, with over 9,000 recorded plant species restricted to a small geographic area (±90,000 km²), of which almost 70% are endemic⁶¹. Much of this diversity is due to a handful of speciose clades, the ‘Cape ﬂoral clades’^25,62,63, mostly consisting of plants with short, needle-like leaves such as Phylica^20,21, that have traditionally been regarded as having originated and radiated within the Cape^25,62,63. Our discovery of a fossils identical to Phylica from the Cretaceous of southeast Asia challenges the traditional interpretation that the fire-adapted Fynbos flora is of a relatively recent origin^20,21,⁶⁴^–⁶⁶ and arose in the aftermath of climatic drying near the Miocene-Pliocene boundary^65,67. Paleomagnetic studies⁶⁸ and fossil evidence⁶⁹^–⁷³ indicate that the West Burma Block is of a Gondwanan origin; it rifted from north-western Australia between the late Triassic and late Jurassic and was an isolated landmass in the Tethys Ocean in the mid-Cretaceous^68,74. As such, our results demonstrate that a key element of the xeromorphic Fynbos vegetation existed as long as 99 Ma ago, supporting the great antiquity of open fire-prone vegetation in Gondwana. Given that southern Gondwana during the middle Cetaceous (Albian–Turonian; 112–90 Ma) was arid to semi-arid^75,76, possessing a similar climate as the South African Cape today, the Fynbos could provide a recent proxy for understanding fire-prone plant communities in the Cretaceous²³ (Fig. 5). Whether the Fynbos biome itself dates to the Cretaceous remains to be tested with the aid of further plant fossils. Coetzee and Muller⁷⁷ noted that the Miocene pollen assemblages from southwestern Cape are comparable with Australian floras, although some of these Gondwanan elements were lost after the climatic changes at the end of the Miocene. Taken together, these lines of evidence point towards a much more ancient and complex history of the Fynbos biome than previously thought.

The Myanmar amber tropical forest palaeoenvironment

The presence of abundant fire-prone vegetation in amber from northern Myanmar has important implications for interpreting the palaeoenvironment of this key Mesozoic Konservat-Lagerstätten. Myanmar amber harbours perhaps the most diverse Cretaceous amber biota known to date⁷⁸, famous for its well-preserved vertebrate remains and abundant insect fossils. The Myanmar amber palaeoenvironment is most often reconstructed as a hot tropical forest⁷⁸, with a near-equatorial climate⁶⁸ located in the vicinity of brackish water and the seashore¹³, perhaps akin to modern swamp forests⁸¹. Eophylica and Phylica fossils suggest that the Myanmar amber forest may have been prone to seasonal fires, similar to some tropical peat swamp forests in more recent geological history⁸². Major fires and subsequent draught may have been associated with some amber deposits, such as Cretaceous New Jersey amber that contains abundant charred remains of plants and insects⁸³. It is possible that seasonal fires may have also played a role in the production of Myanmr amber, one of the largest amber deposits in the world, since resin secretion can be triggered by wounding⁸⁴, as well as any stresses that impact water uptake (e.g., insect infestation, drought, etc⁸⁵.). Notably, burned plant remains are abundant in our ambers (Supplementary Fig. 5) although it is not clear if these remains were charred prior to entrapment in resin or are the consequence of post-burial taphonomic processes. Abundant seasonal fire may also partly explain the abundance of amber in the Cretaceous rock record, as fossiliferous ambers of older age are exceedingly rare and largely occur only as traces⁸⁶.

Amber provides a complementary window of early angiosperm diversity

The unique floral architecture preserved in Eophylica and Phylica fossils is identical to that seen in extant members of the genus Phylica, predating molecular clock estimates for the genus by at least 70 Ma²². This makes Eophylica-Phylica one of the best documented ‘living fossil’ genera in the angiosperm fossil record. It is not generally possible to assign Mesozoic flower compression fossils and charcoalified fragments to extant genera with high confidence¹⁰. Our study demonstrates that amber provides a complementary window into the early evolution of flowering plants, by overcoming some biases inherent to compression and carbonified fossils that make up the majority of the early angiosperm fossil record. Firstly, most compression fossils are preserved primarily in wetlands, while amber paleoenvironments range from warm forests to seashores⁸³, capturing a different set of palaeoenvironments. Secondly, amber inclusions are often preserved with extreme fidelity, comparable to the inflorescences of modern plants. The discovery of further well-preserved angiosperm fossils in Cretaceous amber deposits may eventually backdate other crown angiosperm clades, helping to provide more calibration points for understanding the tempo of Cretaceous angiosperm radiation and ultimately contributing to reconciling the often-perceived incongruence between the angiosperm fossil record and molecular clock estimates^87,88.

Fossil Provenance and Ethical Statement

The material described herein originates from two amber mines, Tanaing and Hkamti, located in the Hukawng Valley, Kachin State in northern Myanmar¹¹. The mines are introduced in Supplementary Text 1.1. The amber has been radiometrically dated to the earliest Cenomanian, ~99 Ma, and was not produced earlier than the late Albian^12,13. Our study was initiated in 2015 and all amber specimens were acquired from local sellers before December 2016, prior to the escalation of the humanitarian crisis in the region (https://doi.org/10.6084/m9.figshare.13317890.v1). The present fossils were briefly introduced in a lecture and poster presentation at the XIX International Botanical Congress (IBC) in ShenZhen, China, July 2017 (lecture title ‘Mid-Cretaceous Seed Plant Diversity in Burmese Amber’, presented by Shuo Wang).

Authenticity of the 21 amber pieces studied herein was verified by the National Gemstone Testing Center (NGTC) of China with Certificate Numbers XCXNo20200903 to XCXNo20200923. These tests included examination of physical and chemical properties of the specimen such as colour, density, optical character, refractive index, amber flow characteristics, and absorption spectrum.

All 21 pieces of amber pieces, preserving 22 fossils, are curated at the Qingdao University of Science and Technology under the collection numbers QUST-AM20501–12, QUST-AM32413–17 and QUST-AM33310 for E. priscastellata sp. nov., and QUST-AM32127, QUST-AM33311, QUST-AM20513–14 for P. piloburmensis sp. nov. (Supplementary Fig. 6). Of the 21 pieces of amber in this study, 19 originate from the ‘Tanaing’ amber mine in Hukawng Valley, except for QUST-AM20511 and QUST-AM32414 which originate from the nearby ‘Hkamti’ mine, which is further shown in (Supplementary Figs. 1–3 and 6).

Photography

Fossils were photographed with a digital camera (Fujifilm GFX 50 R with Laowa C11625 2.6 X, Cambo Actar 105 hr or Mitutoyo 5-10 X lens) fitted to a macro rail (Cognisys). For every photograph, 30 to 200 images were stacked with Combine ZP and Photoshop CS4. Some specimens were also photographed using Leica DVM6 and M205FA microscopes (Leica AG, Heerbrugg, Switzerland).

To examine internal structures of the flowers, fossils were scanned with Xradia Versa Micro-XCT 620 (Carl Zeiss X-ray Microscopy Inc., Pleasanton, USA) housed in the Advanced Materials Research Institute of Yangtze Delta. All specimens were scanned with the same beam energy of 40 kV, 3 W, and the LE1 filter, but with different exposure times and pixel sizes that depended on the sample size and condition. Of the 22 fossil specimens, clear scanned images were obtained for 20, but the other 2 samples lack sufficient contrast for scanning. The obtained image stacks were reconstructed with Dragonfly (Ors, Montreal, Canada). Final figures were prepared with Photoshop CS5 and Illustrator CS5 (Adobe, San Jose, USA).

Morphological description

Family Rhamnaceae Jussieu 1789

Tribe Phyliceae Reissek ex Endl. 1840

Genus Eophylica Shi, Wang, et Engel gen. nov.

Type species: Eophylica priscastellata Shi, Wang, et Engel sp. nov.

Etymology: The generic name is a combination of the Greek words, Ēṓs (Ἠώς, meaning “dawn”) and the extant genus Phylica L. (itself derived from Greek: phyllikos, meaning, “leafy”). The gender of the name is feminine.

Generic diagnosis: Identical to Phylica except with eight sepals (2 × 4-merious) (versus five in Phylica), lacking petals (present in most Phylica, although secondarily reversed independently in several crown species), and indumentum composed of stellate Rhamnaceous hairs (simple in Phylica). Additionally: Ovary inferior, fused to receptacle. Style columnar, simple. Fruit a typical capsule, obovoid, about 5.0 mm long, crowned with persistent base of calyx with a convex calyx-area. A complete description is provided in the Supplementary Material.

Species Eophylica priscastellata Shi, Wang, et Engel sp. nov.

Holotype (hic designatus): No. QUST-AM32413 (Fig. 2a–b, l, n–v and Supplementary Fig. 21, deposited in the collection of the Qingdao University of Science and Technology, Qingdao, China.

Paratypes (17 specimens): No. QUST-AM20501–QUST-AM20512, QUST-AM32414–QUST-AM32417 and QUST-AM33310, same repository as holotype.

Type locality and age: No. QUST-AM20501–QUST-AM20510, QUST-AM20512, QUST-AM32413, QUST-AM32415–QUST-AM32417 and QUST-AM33310 are from Tanaing mines, earliest Cenomanian, 98.79 Ma ± 0.62 (ca. 99) Ma. QUST-AM20511 and QUST-AM32414 are from ‘Hkamti’ mines, early Albian, 109.7 ± 0.4 (ca. 110) Ma.

Etymology: The specific epithet is a combination of the Latin terms priscus (meaning, “ancient”) and stellatus (meaning, “starry”).

Species diagnosis: Plants covered in stellate and linear hairs. Leaves long linear, spirally arranged. Head of flower terminal surrounded by interior spreading, sub-incurved, linear leafy bracts. Bracts about twice as long as flower. Flower single on twig tip. Disc epigynous and covering inside of calyx tube. Sepals 8 (2 × 4-merious). Petals absent. A complete description is provided in the Supplementary Material.

Genus Phylica L. 1753

Species Phylica piloburmensis Shi, Wang, et Engel sp. nov.

Etymology: The specific epithet is a combination of the Greek term pîlos (πῖλος, meaning, “hair”) and burmensis (itself a combination of Burma and the Latin suffix –ensis, denoting place).

Holotype (hic designatus): No. QUST-AM32127 (Fig. 4a–g and Supplementary Fig. 26, deposited in the collection of the Qingdao University of Science and Technology, Qingdao, China.

Paratypes (3 specimens): No. QUST-AM33311, QUST-AM20513–QUST-AM20514, same repository as holotype.

Type locality and age: Tanaing mines, earliest Cenomanian, 98.79 Ma ± 0.62 (ca. 99) Ma.

Species diagnosis: Leaves slightly wider (1.5–2.0 mm wide, 4.5–8.0 mm long) and both ad- and abaxial sides covered with simple linear hairs. Flowers not single but forming a corymb. Petals present. Fruit covered with dense indumentum. A complete description is provided in the Supplementary Material.

Character scoring and phylogenetic analysis

Morphological characters scored from leaf, habit, flower, fruit, and pollen were compiled from previous studies^29,30,89 and are described in the Supplementary notes. The combined phylogenetic tree was reconstruction based on morphological characters and molecular data following the method of Wilf et al.⁹⁰; the procedure is further described in the Supplementary notes.

Data availability: The Micro-XCT scanning data are available from Zenodo database (https://doi.org/10.5281/zenodo.3997200). Videos of the 3D reconstruction of internal and external structures of the fossil specimens are available from the Figshare database (https://doi.org/10.6084/m9.figshare.12865859.v4). High resolution images of all the figures are available from Figshare database (https://doi.org/10.6084/m9.figshare.12845144).

Acknowledgements

We thank Prof. Zhe-kun Zhou, Prof. Patrick Herendeen, Prof. Steven R. Manchester, Prof. Yao-wu Xing, Prof. Gong-le Shi, Prof. Hai-lu You, Prof. Carina Hoorn, Prof. Gang Li, Prof. Zhuo Feng, Prof. Dong Ren, Prof. Bo Wang, and Prof. Zhong-jian Liu for their valuable advice on earlier versions of this manuscript; Mr. Ji-an Xia for his help with drawing the palaeoenvironment reconstruction; and Mr. Fang-cheng Zheng for his aid with micro-CT data analyses. This study was supported by the National Natural Science Foundation of China (NO.31801022 and NO.31701090) and Start-up funds for high-level talents of Qingdao University of Science and Technology. This work is a contribution to UNESCO-IUGS IGCP Project 679.

Author Contributions

S.W. and C.S. conceived the study and wrote the paper. R.A.S., M. S. E., H. S., E.T., S.W., C. C., and C. S. revised the paper. C.S., S.W., H.P., N.L., X.L., Q.P.X., Z.T.Z., C.L.L., Y.D.W., D.Z.L., Z.K.Z., X.C.Z., and H. S. performed specimen identification and morphological analyses. H.H.C., X.X.L., H.R.Z., J.Y., R.X.J., Q.F., W.C.S., H.Y.H., X.F.L., and J.P.Z. performed fossil photograph and Micro-XCT data analyses. All authors discussed the results and commented on the manuscript.

Competing interests

The authors declare no competing interests.

Data availability

The Micro-XCT scanning data are available from Zenodo (doi: 10.5281/zenodo.3997200). Videos of the 3D reconstruction of internal and external structures of the fossil specimens are available from Figshare database (doi: 10.6084/m9.figshare.12865859). High resolution images of all the figures are available from Figshare database (doi: 10.6084/m9.figshare.12845144).

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Cretaceous fire-resistant angiosperms

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