Cycads (Cycadales) are a non-speciose group of ancient living seed plants with remote roots in the Permian []. They are remarkable gymnosperm remnants, dominating terrestrial ecosystems during the Mesozoic and dwindling to their current diversity of approximately 330 species as angiosperms rose to dominance []. Cycads are dioecious gymnosperms, and most, if not all, share obligate mutualisms with specialist insect pollinators such as beetles (Coleoptera) and thrips (Thysanoptera) []. Understanding pollination modes of Mesozoic cycads is significant for elucidating the early diversification of cycads and insect-plant associations before angiosperm dominance.

With >380,000 named living species constituting almost 25% of all known lifeforms on our planet, beetles exhibit an astonishing morphological, taxonomic, and ecological diversity []. The beetle family Boganiidae is a small, monophyletic, and relict cucujoid group, with six extant genera and 15 species restricted to southern Africa, southwestern and eastern Australia, and New Caledonia []. Adult boganiids, characterized by head frons with median endocarina and mandibles with a dorsal setose cavity near the base, are distinctive among Cucujoidea []. Boganiidae currently comprise two subfamilies: Boganiinae (two genera) and Paracucujinae (four genera). In Paracucujinae, two closely related but geographically widely separated genera, Metacucujus and Paracucujus (tribe Paracucujini), feed on cones of the cycad tribe Encephalarteae (Zamiaceae) in southern Africa and the southwest of Western Australia []. This distribution suggests a Gondwanan vicariance during the Middle Jurassic resulting in the isolated distribution for these poorly dispersing beetles and their cycads []. Here, we report on a cucujoid beetle belonging to the Boganiidae preserved within a piece of mid-Cretaceous Burmese amber (approximately 99 Ma []), which also harbors many cycad pollen grains alongside the beetle. The phylogenetic placement of the beetle along with the presence of specialized mandibular cavities known in modern cycad-pollinating boganiids for the transport of pollen reveal the fossil to be an early-cycad-visiting species. This specialized beetle-gymnosperm association represents the first probable insect pollination mode for Cycadales during the mid-Mesozoic.

Phylogeny and placement of Boganiidae (Coleoptera, Cucujoidea) with a review of Australian and New Caledonian taxa.

Phylogeny and placement of Boganiidae (Coleoptera, Cucujoidea) with a review of Australian and New Caledonian taxa.

Phylogeny and placement of Boganiidae (Coleoptera, Cucujoidea) with a review of Australian and New Caledonian taxa.

The generic name is a combination of creto- and the genus Paracucujus. The specific epithet is a combination of Greek kykas (meaning, cycad) and philia (meaning, friendly love or affection).

Cretoparacucujus is distinguished from other boganiids by the following combination of characters: upper body surface sub-glabrous; head large, slightly wider than pronotum; antenna filiform, without antennal club; clypeus sub-triangular, apex widely notched medially; frontal carina meeting frontoclypeal sulcus; mandible long, nearly straight; maxillary palpus elongate, with maxillary palpomere 4 much shorter than palpomere 3; protibial apex not expanded; and elytral punctation seriate.

Description

Refer to Data S1 for a complete description.

11 Kirejtshuk A.G. Paranrexidae fam. nov., Jurassic beetles of the infraorder Cucujiformia (Coleoptera, Polyphaga). 7 Escalona H.E.

Lawrence J.F.

Wanat M.

Ślipiński A. Phylogeny and placement of Boganiidae (Coleoptera, Cucujoidea) with a review of Australian and New Caledonian taxa. 12 Crowson R.H. Relationships to cycads. 13 Crowson R.A. A new genus of Boganiidae (Coleoptera) from Australia, with observations on glandular openings, cycad associations and geographical distribution in the family. 13 Crowson R.A. A new genus of Boganiidae (Coleoptera) from Australia, with observations on glandular openings, cycad associations and geographical distribution in the family. The most impressive feature of Cretoparacucujus is the large prognathous head with large compound eyes, sharp mandibles, and extremely long maxillary palpi ( Figures 1 A, 1B, 1F, S1 D, S1F, and S2 A). These features, close to those of Paracucujus ( Figures 1 E, S1 E, and S1G) and the Jurassic Parandrexis (Parandrexidae), probably suggest an open habitat, and most likely habitation on the surface of the strobiles of gymnosperms []. The mandible of Cretoparacucujus bears a dorsal, round, and setose cavity ( Figures 1 D and S1 D) near its base, and the clypeus is basally constricted ( Figure 1 D), making the mandibular cavity clearly visible in dorsal view. This specialized modification of the mandible ( Figure 1 C) has been known to function in containing and most likely transporting pollen grains, as both adults and larvae of extant Boganiidae feed on pollen []. In Cucujoidea, similar analogous mandibular cavities are known in the extant pollen beetles (Nitidulidae: Meligethinae), which are pollenophagous and possible pollinators []. Observations of the mandibles of some extant boganiids such as Athertonium and Boganium have provided direct evidence that the peculiar mandibular cavities are capable of carrying a few pollen grains []. As in most boganiids, the tarsi of Cretoparacucujus have dense normal adhesive setae on the ventral surfaces of the basal three tarsomeres ( Figures 1 G and S2 F), which is a specialization for holding and climbing on the surfaces of plants. In addition, the maxilla of Cretoparacucujus, with an apically expanded and densely setose galea ( Figure S2 D), is typical of many modern boganiids, and it may be used to collect small particles such as pollen and direct them into the mouth.

7 Escalona H.E.

Lawrence J.F.

Wanat M.

Ślipiński A. Phylogeny and placement of Boganiidae (Coleoptera, Cucujoidea) with a review of Australian and New Caledonian taxa. 7 Escalona H.E.

Lawrence J.F.

Wanat M.

Ślipiński A. Phylogeny and placement of Boganiidae (Coleoptera, Cucujoidea) with a review of Australian and New Caledonian taxa. 8 Suinyuy T.N.

Donaldson J.S.

Johnson S.D. Insect pollination in the African cycad Encephalartos friderici-guilielmi Lehm. 14 Suinyuy T.N.

Johnson S.D. Geographic variation in cone volatiles and pollinators in the thermogenic African cycad Encephalartos ghellinckii Lem. 7 Escalona H.E.

Lawrence J.F.

Wanat M.

Ślipiński A. Phylogeny and placement of Boganiidae (Coleoptera, Cucujoidea) with a review of Australian and New Caledonian taxa. 13 Crowson R.A. A new genus of Boganiidae (Coleoptera) from Australia, with observations on glandular openings, cycad associations and geographical distribution in the family. 3 Terry I.

Tang W.

Blake A.S.T.

Donaldson J.S.

Singh R.

Vovides A.P.

Jaramillo A.C. An overview of cycad pollination studies. 13 Crowson R.A. A new genus of Boganiidae (Coleoptera) from Australia, with observations on glandular openings, cycad associations and geographical distribution in the family. 7 Escalona H.E.

Lawrence J.F.

Wanat M.

Ślipiński A. Phylogeny and placement of Boganiidae (Coleoptera, Cucujoidea) with a review of Australian and New Caledonian taxa. 4 Labandeira C.C.

Kvaček J.

Mostovski M.B. Pollination drops, pollen, and insect pollination of Mesozoic gymnosperms. 9 Labandeira C.C. The paleobiology of pollination and its precursors. In Paracucujinae, the life history of Dzumacium (New Caledonia) is unknown, and their feeding habit remains elusive. Adults of Athertonium from eastern Australia are pollenophagous, associated with angiosperms such as Lauraceae, Elaeocarpaceae, Cunoniaceae, and Meliaceae []. Species of Metacucujus from South Africa are dependent on male cones of various cycads in the genus Encephalartos []. There is evidence indicating that Metacucujus encephalarti, as well as an erotylid beetle, are probably the main pollinators of Encephalartos []. The monotypic genus Paracucujus from southwestern Australia occurs in large numbers on male cones of Macrozamia riedlei and sometimes in sticky traps on female cones []. As such, Paracucujus rostratus is probably a pollinator of Macrozamia riedlei []. Recent phylogenetic analyses indicated that the extant Metacucujus and Paracucujus are close extant sister groups [], as are the two associated cycad host-plant genera, which belong to the same tribe, Encephalarteae (Zamiaceae). This remarkable distribution indicates a Gondwanan vicariance that began during the Middle Jurassic for these poorly dispersing beetle and cycad pairs []. Apparently, the beetle-cycad interaction was established during the Mesozoic as supported by the disjunct distribution of the beetle and cycad pairs. Our discovery of a Paracucujus-related genus from the Cretaceous suggests that Cretoparacucujus may have a similar feeding habit to that of Paracucujus, feeding on pollen grains of cycads, as this seems to be a biological trait for the clade as a whole.

1 Taylor T.N.

Taylor E.L.

Krings M. Paleobotany: The Biology and Evolution of Fossil Plants. 15 van Konijnenburg-van Cittert J.H. In situ gymnosperm pollen from the Middle Jurassic of Yorkshire. 15 van Konijnenburg-van Cittert J.H. In situ gymnosperm pollen from the Middle Jurassic of Yorkshire. 16 Dehgan B.

Dehgan N.B. Comparative pollen morphology and taxonomic affinities in Cycadales. It is remarkable that several aggregations of exquisitely preserved pollen grains are located along the left side of the fossil beetle and with two pollen grains close to the head ( Figure 2 ). All pollen grains associated with C. cycadophilus are boat shaped, prolate, and monosulcate. They display an elliptical outline and rounded polar margin in polar view and subcircular shape in equatorial view. Average polar axis length and equatorial diameter of the palynospecies (N = 21) are 20.65 μm (20.07–21.04 μm) and 14.30 μm (14.20–14.37 μm), respectively. The length-width ratios range from 1.1 to 1.4. The sulcus is elongate, extending almost the entire length of the grain. The sulcus exhibits rounded ends and it is much broader at their ends (∼4.62 μm) than at the mid-point (∼2.12 μm). The ornamentation is psilate, and the pollen exine is approximately 1 μm thick. Based on a combination of the shape, sulcus structure, and ornamentation, the pollen can be referred to Cycadopites, a form-genus of polyphyletic origin occurring in sediments from the late Palaeozoic to Holocene [], which can be also produced by modern cycads. It is challenging to affiliate Cycadopites that are taphonomically deformed to a particular group of gymnosperms, as they are comparable to pollen grains of a wide range of plants, including Bennettitales, Cycadales, Czekanowskiales, Ginkgoales, Peltaspermales, Pentoxylales, and a few basal angiosperm lineages. However, these amber-entombed pollen grains exhibit three-dimensional features with high fidelity that allow for a more accurate systematic attribution. These pollen grains differ from those of Ginkgoales by their oval outline, rounded ends, and the colpus form []. Some pollen grains of extinct Bennettitales also belong to Cycadopites, but they are distinguished by their large size and a more spindle-like outline []. The present pollen grains are comparatively small in size (∼21 μm long), close to some species of Cycas, Macrozamia, and Zamia, but considerably smaller than those of Encephalartos and Lepidozamia [].

17 Hall J.A.

Walter G.H. Does pollen aerodynamics correlate with pollination vector? Pollen settling velocity as a test for wind versus insect pollination among cycads (Gymnospermae: Cycadaceae: Zamiaceae). 18 Timerman D.

Greene D.F.

Ackerman J.D.

Kevan P.G.

Nardone E. Pollen aggregation in relation to pollination vector. Another fact supporting this beetle-mediated pollination is that these Cycadopites pollen grains are in multiple aggregations, which comprise 3–14 grains in the specimen ( Figures 2 A’ and 2B–2D). Many modern entomophilous cycad pollens and pollens of insect-pollinated angiosperms adhere in large aggregations, whereas wind-pollinated, or anemophilous, pollens are dispersed as single grains, or monads []. The Burmese amber has yielded a diverse Cretaceous flora including moss, liverworts, ferns, conifers, and angiosperms, but cycads remain unknown. Our discovery of the Cycadopites pollen represents the first evidence of cycads from Burmese amber.

19 König M.

Jokat W. The Mesozoic breakup of the Weddell Sea. 9 Labandeira C.C. The paleobiology of pollination and its precursors. 20 Salas-Leiva D.E.

Meerow A.W.

Calonje M.

Griffith M.P.

Francisco-Ortega J.

Nakamura K.

Stevenson D.W.

Lewis C.E.

Namoff S. Phylogeny of the cycads based on multiple single-copy nuclear genes: congruence of concatenated parsimony, likelihood and species tree inference methods. 7 Escalona H.E.

Lawrence J.F.

Wanat M.

Ślipiński A. Phylogeny and placement of Boganiidae (Coleoptera, Cucujoidea) with a review of Australian and New Caledonian taxa. Figure 4 Geographic Distribution of the Known Entomophilous Cycads of the Tribe Encephalarteae and Their Boganiid Pollinators Show full caption The phylogenetic relationships and divergence time of the widely separated lineages within Boganiinae are shown. The arrow indicates the divergence time estimated by separation of Gondwana in the Jurassic. Abbreviations: AU, Australia; MM, Myanmar; ZA, South Africa. See also Figure S3 and Table S1 Given the feeding functional morphology and phylogenetic placement of Cretoparacucujus, as well as the identification of the associated cycad pollen aggregations, the Cretaceous C. cycadophilus, like the related P. rostratus, was probably a cycad pollen feeder and most likely a pollinator for Macrozamia-related cycads that belong to the tribe Encephalarteae ( Figure S3 ). Moreover, the establishment of this type of boganiid-cycad association may be significantly older, probably extending back prior to the eventual breakup of Gondwana during the Early Jurassic, some 167 million years ago []. The hypothesis is also supported by the remarkable vicariance of two poorly dispersing cycad-host and beetle-herbivore pairs from widely separated Gondwanan continents ( Figure 4 ) []. The species of Encephalartos from southern Africa and Macrozamia riedlei from Western Australia, belonging to the same tribe Encephalarteae (Zamiaceae), are closely related [], so are their corresponding pollenophagous beetles: Metacucujus and its modern sister group, Paracucujus [].

21 Pott C.

McLoughlin S.

Lindström A. Late Palaeozoic foliage from China displays affinities to Cycadales rather than to Bennettitales necessitating a re-evaluation of the Palaeozoic Pterophyllum species. 1 Taylor T.N.

Taylor E.L.

Krings M. Paleobotany: The Biology and Evolution of Fossil Plants. 22 Wilf P.

Stevenson D.W.

Cúneo N.R. The last Patagonian cycad, Austrozamia stockeyi gen. et sp. nov., early Eocene of Laguna del Hunco, Chubut, Argentina. 23 Feng Z.

Lv Y.

Guo Y.

Wei H.B.

Kerp H. Leaf anatomy of a late Palaeozoic cycad. 23 Feng Z.

Lv Y.

Guo Y.

Wei H.B.

Kerp H. Leaf anatomy of a late Palaeozoic cycad. 22 Wilf P.

Stevenson D.W.

Cúneo N.R. The last Patagonian cycad, Austrozamia stockeyi gen. et sp. nov., early Eocene of Laguna del Hunco, Chubut, Argentina. 22 Wilf P.

Stevenson D.W.

Cúneo N.R. The last Patagonian cycad, Austrozamia stockeyi gen. et sp. nov., early Eocene of Laguna del Hunco, Chubut, Argentina. Cycads have a rich fossil record, extending to the earliest Permian [] and peaking in diversity during the Jurassic and Cretaceous periods []. Unfortunately, fossil cycads are usually preserved as fragmentary stems or leaves, and rarely with reproductive organs, which yield non-overlapping character datasets, hindering phylogenetic analyses []. The earliest cycad with an affinity to Zamiaceae, Plagiozamites oblongifolius, comes from Late Permian of China []. Its stomatal architecture, especially the prominent thickenings of the subsidiary cells, resembles that of some extant Macrozamia and Encephalartos [], both belonging to the entomophilous Encephalarteae. More convincing fossils placed in Encephalarteae are from the Cretaceous of Antarctica, India, and Patagonia []. Cenozoic representatives of Encephalarteae from the early Eocene of Patagonia and the middle Eocene of Australia suggest that the tribe occurred widely across Gondwanan landmasses until the final breakup of the former supercontinent [].

2 Nagalingum N.S.

Marshall C.R.

Quental T.B.

Rai H.S.

Little D.P.

Mathews S. Recent synchronous radiation of a living fossil. 20 Salas-Leiva D.E.

Meerow A.W.

Calonje M.

Griffith M.P.

Francisco-Ortega J.

Nakamura K.

Stevenson D.W.

Lewis C.E.

Namoff S. Phylogeny of the cycads based on multiple single-copy nuclear genes: congruence of concatenated parsimony, likelihood and species tree inference methods. 24 Condamine F.L.

Nagalingum N.S.

Marshall C.R.

Morlon H. Origin and diversification of living cycads: a cautionary tale on the impact of the branching process prior in Bayesian molecular dating. 2 Nagalingum N.S.

Marshall C.R.

Quental T.B.

Rai H.S.

Little D.P.

Mathews S. Recent synchronous radiation of a living fossil. 20 Salas-Leiva D.E.

Meerow A.W.

Calonje M.

Griffith M.P.

Francisco-Ortega J.

Nakamura K.

Stevenson D.W.

Lewis C.E.

Namoff S. Phylogeny of the cycads based on multiple single-copy nuclear genes: congruence of concatenated parsimony, likelihood and species tree inference methods. 24 Condamine F.L.

Nagalingum N.S.

Marshall C.R.

Morlon H. Origin and diversification of living cycads: a cautionary tale on the impact of the branching process prior in Bayesian molecular dating. 2 Nagalingum N.S.

Marshall C.R.

Quental T.B.

Rai H.S.

Little D.P.

Mathews S. Recent synchronous radiation of a living fossil. 2 Nagalingum N.S.

Marshall C.R.

Quental T.B.

Rai H.S.

Little D.P.

Mathews S. Recent synchronous radiation of a living fossil. 20 Salas-Leiva D.E.

Meerow A.W.

Calonje M.

Griffith M.P.

Francisco-Ortega J.

Nakamura K.

Stevenson D.W.

Lewis C.E.

Namoff S. Phylogeny of the cycads based on multiple single-copy nuclear genes: congruence of concatenated parsimony, likelihood and species tree inference methods. 24 Condamine F.L.

Nagalingum N.S.

Marshall C.R.

Morlon H. Origin and diversification of living cycads: a cautionary tale on the impact of the branching process prior in Bayesian molecular dating. 19 König M.

Jokat W. The Mesozoic breakup of the Weddell Sea. 23 Feng Z.

Lv Y.

Guo Y.

Wei H.B.

Kerp H. Leaf anatomy of a late Palaeozoic cycad. 25 Wang X.

Li N.

Wang Y.

Zheng S. The discovery of whole-plant fossil cycad from the Upper Triassic in western Liaoning and its significance. Recent fossil-calibrated molecular dating estimates produced various ages for the origin of crown cycads, ranging from ca. 200 Ma (Early Jurassic) to 274.5 Ma (Late Permian), but all suggested that the extant diversity of cycads derives from mostly Miocene radiations and postdates the Cretaceous-Paleogene boundary []. Encephalarteae, as traditionally defined based on morphology, was recovered as a monophyletic group by almost all recent molecular phylogenies [], except in a maximum-likelihood analysis based on a single nuclear gene []. It is unexpected that these molecular divergence estimates suggested an origin of stem-group Encephalarteae during the Late or Early Cretaceous []. This young age for origin appears to be unlikely, because at that time Africa (western Gondwana) was widely separated from eastern Gondwana, which comprises Antarctica, India, Madagascar, Australia, and New Zealand []. Considering the low dispersal ability of early cycads and their potential beetle pollinators, Encephalarteae and their cycad-beetle associations were most likely established before the separation of the Gondwanan landmasses, a time during the Early Jurassic or earlier. Additionally, fossil evidence of late Permian cycad cuticles and a late Triassic whole-plant from China [], both with apomorphies of modern Encephalarteae, suggest a much longer evolutionary history for the tribe than implied by methods relying solely on indirect inferences from molecular clocks.

3 Terry I.

Tang W.

Blake A.S.T.

Donaldson J.S.

Singh R.

Vovides A.P.

Jaramillo A.C. An overview of cycad pollination studies. 3 Terry I.

Tang W.

Blake A.S.T.

Donaldson J.S.

Singh R.

Vovides A.P.

Jaramillo A.C. An overview of cycad pollination studies. 4 Labandeira C.C.

Kvaček J.

Mostovski M.B. Pollination drops, pollen, and insect pollination of Mesozoic gymnosperms. 26 Peñalver E.

Labandeira C.C.

Barrón E.

Delclòs X.

Nel P.

Nel A.

Tafforeau P.

Soriano C. Thrips pollination of Mesozoic gymnosperms. 27 Oberprieler R.G. The weevils (Coleoptera: Curculionoidea) associated with cycads. 2. Host specificity and implications for cycad taxonomy. 28 Klavins S.D.

Kellogg D.W.

Krings M.

Taylor E.L.

Taylor T.N. Coprolites in a Middle Triassic cycad pollen cone: evidence for insect pollination in early cycads?. 28 Klavins S.D.

Kellogg D.W.

Krings M.

Taylor E.L.

Taylor T.N. Coprolites in a Middle Triassic cycad pollen cone: evidence for insect pollination in early cycads?. 28 Klavins S.D.

Kellogg D.W.

Krings M.

Taylor E.L.

Taylor T.N. Coprolites in a Middle Triassic cycad pollen cone: evidence for insect pollination in early cycads?. 29 Kirejtshuk A.G. A current generic classification of sap beetles (Coleoptera, Nitidulidae). 30 Vitali F. Diplocoelus probiphyllus n. sp., the first known fossil false skin beetle (Coleoptera: Biphyllidae). 31 Alekseev V.I.

Bukejs A. First fossil representatives of Pharaxonothinae Crowson (Coleoptera: Erotylidae): indirect evidence for cycads existence in Baltic amber forest. 32 Liu Z.

Ślipiński A.

Lawrence J.F.

Ren D.

Pang H. Palaeoboganium gen. nov. from the Middle Jurassic of China (Coleoptera: Cucujoidea: Boganiidae): the first cycad pollinators?. 32 Liu Z.

Ślipiński A.

Lawrence J.F.

Ren D.

Pang H. Palaeoboganium gen. nov. from the Middle Jurassic of China (Coleoptera: Cucujoidea: Boganiidae): the first cycad pollinators?. 33 Cai C.

Beattie R.

Huang D. Jurassic olisthaerine rove beetles (Coleoptera: Staphylinidae): 165 million years of morphological and probably behavioral stasis. 34 Seton M.

Müller R.D.

Zahirovic S.

Gaina C.

Torsvik T.

Shephard G.

Talsma A.

Gurnis M.

Turner M.

Maus S.

Chandler M. Global continental and ocean basin reconstructions since 200 Ma. Earth-. 3 Terry I.

Tang W.

Blake A.S.T.

Donaldson J.S.

Singh R.

Vovides A.P.

Jaramillo A.C. An overview of cycad pollination studies. 35 Hall J.A.

Walter G.H.

Bergstrom D.M.

Machin P. Pollination ecology of the Australian cycad Lepidozamia peroffskyana (Zamiaceae). 28 Klavins S.D.

Kellogg D.W.

Krings M.

Taylor E.L.

Taylor T.N. Coprolites in a Middle Triassic cycad pollen cone: evidence for insect pollination in early cycads?. 4 Labandeira C.C.

Kvaček J.

Mostovski M.B. Pollination drops, pollen, and insect pollination of Mesozoic gymnosperms. 9 Labandeira C.C. The paleobiology of pollination and its precursors. 12 Crowson R.H. Relationships to cycads. 5 Peris D.

Pérez-de la Fuente R.

Peñalver E.

Delclòs X.

Barrón E.

Labandeira C.C. False blister beetles and the expansion of gymnosperm-insect pollination modes before angiosperm dominance. 6 Grimaldi D.

Engel M.S. Evolution of the Insects. 36 Barba-Montoya J.

Dos Reis M.

Schneider H.

Donoghue P.C.J.

Yang Z. Constraining uncertainty in the timescale of angiosperm evolution and the veracity of a Cretaceous Terrestrial Revolution. 37 Grimaldi D. The co-radiations of pollinating insects and angiosperms in the Cretaceous. 22 Wilf P.

Stevenson D.W.

Cúneo N.R. The last Patagonian cycad, Austrozamia stockeyi gen. et sp. nov., early Eocene of Laguna del Hunco, Chubut, Argentina. Modern cycads are principally pollinated by beetles, and rarely by thrips or moths []. Their beetle pollinators mainly include cucujoids (Biphyllidae, Boganiidae, Erotylidae, and Nitidulidae), weevils (Anthribidae, Belidae, Brentidae, and Curculionidae), and, unusually, tenebrionids []. Cycadothrips, a lineage of basal thrips, participate in the pollination of some species of Macrozamia in Australia. Based on the biogeography of Cycadothrips and the antiquity of the family to which it belongs (Aeolothripidae), thrips were most likely among the earliest pollinators of these plants [], although fossil evidence is lacking. Weevil pollinators of cycads, as revealed by extensive comparative studies, are probably derived from angiosperm-dwelling ancestors, rather than from the older gymnosperm feeding weevils [], and are therefore correspondingly and comparatively younger in age. It is noteworthy that the Triassic obrieniids with a weevil-like rostrum (nose) and their frequent co-occurrence with cycad remains have been hypothesized as evidence of a potential Triassic beetle-cycad association []. Such early interactions have been exemplified by a Middle Triassic cycad cone that contains pollen-laden coprolites possibly produced by beetles []. This find provides the earliest evidence for a cycad-insect interaction, illuminating the early stage in the establishment of complex entomophily in cycads []. Among the cucujoid pollinators, Nitidulidae have their oldest known fossil records from the Early Cretaceous, whereas Biphyllidae and Erotylidae date back to the mid-Eocene []. By contrast, the first boganiid fossil, Palaeoboganium jurassicum, has been recently documented from the Middle Jurassic (approximately 165 Ma) of northeastern China []. Morphology-based phylogenetic analyses recovered Palaeoboganium as a sister group to Metacucujus + Paracucujus, which implied the fossil beetle as “a good candidate” for a pollinator of cycads []. The feeding habits of P. jurassicum are undoubtedly difficult to determine due to the insufficient preservation of compression fossils (e.g., lacking details of mandible and gut contents), and its position as basal to the two genera pollinating cycads leaves its biology somewhat ambiguous. Nevertheless, P. jurassicum demonstrates that Boganiidae were present during that period, originating at least as early as the Middle Jurassic, and were more widespread than initially believed. Biogeographically, Boganiidae may have also occurred across Gondwana during the Middle-Late Jurassic, as similar distribution patterns have been observed in multiple beetle lineages as shown by fossils from the Jurassic of China and Australia []. The Boganiidae-Encephalarteae association was probably established during the Early-Middle Jurassic, and the specific beetle-herbivore and cycad-host pairs were probably widespread on Gondwana, at least in what would become southern Africa, southwestern Australia, and Antarctica, the last then connecting the former two continents []. Like boganiids, the present global distribution of pollinating erotylids in Africa, Asia, Australia, and North and Central America [] suggests an early development of an erotylid-cycad relationship before late-Mesozoic continental drift []. Collectively, the preliminary cycad-insect associations are probably ancient, extending to the Triassic or earlier [], whereas insect pollination of cycads may be as early as the Early Jurassic [], long before the origin and diversification of major groups of angiosperms and the concomitant diversification of angiosperm pollinators such as moths, flies, and bees later in the Cretaceous []. Moreover, such an ancient association was probably widespread at least across Gondwana in the Mesozoic, as evidenced by Cretaceous cycads of the Encephalarteae from Antarctica, India, and South America [].