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New Insects Feeding on Dinosaur Feathers in Mid-Cretaceous Amber

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New Insects Feeding on Dinosaur Feathers in Mid-Cretaceous Amber ARTICLE https://doi.org/10.1038/s41467-019-13516-4 OPEN New insects feeding on dinosaur feathers in mid-Cretaceous amber Taiping Gao 1*, Xiangchu Yin2, Chungkun Shih1,3, Alexandr P. Rasnitsyn4,5, Xing Xu6,7, Sha Chen1, Chen Wang8 & Dong Ren 1* Due to a lack of Mesozoic fossil records, the origins and early evolution of feather-feeding behaviors by insects are obscure. Here, we report ten nymph specimens of a new lineage of 1234567890():,; insect, Mesophthirus engeli gen et. sp. nov. within Mesophthiridae fam. nov. from the mid- Cretaceous (ca. 100 Mya) Myanmar (Burmese) amber. This new insect clade shows a series of ectoparasitic morphological characters such as tiny wingless body, head with strong chewing mouthparts, robust and short antennae having long setae, legs with only one single tarsal claw associated with two additional long setae, etc. Most significantly, these insects are preserved with partially damaged dinosaur feathers, the damage of which was probably made by these insects’ integument-feeding behaviors. This finding demonstrates that feather- feeding behaviors of insects originated at least in mid-Cretaceous, accompanying the radiation of feathered dinosaurs including early birds. 1 College of Life Sciences and Academy for Multidisciplinary Studies, Capital Normal University, 105 Xisanhuanbeilu Haidian District, 100048 Beijing, China. 2 Northwest Institute of Plateau Biology, Chinese Academy of Sciences, 23 Xinning Road, 810008 Xining, China. 3 Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012, USA. 4 A. A. Borissiak Palaeontological Institute, Russian Academy of Sciences, Moscow, Russia 117647. 5 Natural History Museum, Cromwell Road, London SW7 5BD, UK. 6 Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 100044 Beijing, China. 7 Center for Excellence in Life and Paleoenvironment, Chinese Academy of Science, Beijing, China. 8 School of Health Administration and Education, Capital Medical University, No.10 Xitoutiao, You An Men, 100069 Beijing, China. *email: [email protected]; [email protected] NATURE COMMUNICATIONS | (2019) 10:5424 | https://doi.org/10.1038/s41467-019-13516-4 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-019-13516-4 any extant insects have ectoparasitic lifestyles, and these Cretaceous specimens: antenna with two apical long stiff Mspend lots of time or entire life (obligate) on the skin, setae and one short seta, leg with a single claw accompanied with hairs, or feathers of warm-blooded vertebrates, sucking two long clavate pretarsal setae. Based on these characters, it is blood or feeding on skin debris, hairs, or feathers of their hosts1. difficult to place Mesophthiridae to any known order within Ectoparasitic insects cause discomforts or sickness of hosts, Insecta, therefore we identify the taxon as an order incertae sedis reduce production of livestock, and damage avian feathers, etc2,3. here, pending more new material to be found in the future to More seriously, ectoparasites transmit diseases as vectors4, having further confirm its phylogenetic position. For more details resulted in catastrophic illnesses and deaths in human history3,5. concerning possible taxonomic position of the new family, see Two major groups of extant ectoparasites, Phthiraptera (true lice), “Discussion” section. and Siphonaptera (fleas), have attracted much attention from scientific community mainly due to their medical and agricultural Mesophthirus engeli Gao Shih, Rasnitsyn & Ren, sp. nov. significance. One lineage of the former group feed on feathers and (Figs. 1–3, Supplementary Figs. 1 and 2) soft skin of birds6,7. While blood-feeding insects have been described from the Jurassic and Cretaceous8–10, integument- Type species. Mesophthirus engeli Gao, Shih, Rasnitsyn & Ren, feeding insects have never been reported from the Mesozoic to sp. nov. our knowledge. The earliest known fossil louse, Megamenopon Etymology. The generic name is derived from the Greek prefix rasnitsyni, is from the Eocene of Germany (44 Mya)11,12, and it is “meso-” and Greek “phtheir” (latinized as phthirus) meaning already fully modern in form and assigned within Amblycera. lice. Gender masculine. The specific name “engeli” is dedicated The evolution of feather- and other integument-feeding insects in to Dr Michael S. Engel, for his outstanding contribution to the Mesozoic thus remains obscure11,13, even though many entomological research. feathered dinosaurs including early birds have been described Species included. Only the type species Mesophthirus engeli from the Jurassic and Cretaceous14. Gao, Shih, Rasnitsyn & Ren, sp. nov. Here, we report ten nymph specimens of an ectoparasitic insect Diagnosis. As for family because of monotypy. clade, Mesophthirus engeli Gao, Shih, Rasnitsyn & Ren, gen et. sp. Materials. All specimens are nymphs of two different devel- nov. assigned to Mesophthiridae Gao, Shih, Rasnitsyn & Ren, fam. opmental stages (see “Discussion” section below). The holotype, nov. of order Incertae sedis. These nymph insects crawled and fed CNU-MA2016009 (Fig. 1j and Fig. 2a–c), together with on two feathers preserved in two pieces of amber, AMBER No. 01 remaining six paratypes, CNU-MA2016001–CNU-MA2016003 and AMBER No. 02, from the mid-Cretaceous of Myanmar. (Fig. 1a–c), CNU-MA2016006—CNU-MA2016008 (Fig. 1g–i) AMBER No. 01 includes nine specimens and AMBER No. 02 has and CNU-MA2016010 (Fig. 3b–e) are in an elder stage, and only one specimen. The strata producing the Myanmar (Burmese) paratypes CNU-MA2016001 (Fig. 1a), CNU-MA2016004 amber was radiometrically dated at 98.79 ± 0.62 Ma15.Thedate (Fig. 1e) and CNU-MA2016005 (Fig. 1f) are in an earlier corresponds to the early Cenomanian, that is, the earliest Late stage. The locations of CNU-MA2016001—CNU-MA2016009 Cretaceous. However, displaying clear traces of redeposition, the with feather are displayed in Fig. 1, and more details about the Myanmar amber is considered to be older than enclosing rocks16. morphology of this group are shown in Fig. 2.Allthesespeci- Therefore, we refer the amber age informally as mid-Cretaceous. mens are deposited in the Key Lab of Insect Evolution and Environmental Changes, Capital Normal University, Beijing, Results China. Systematic paleontology. Locality and horizon. The amber specimen was collected from Kachin Province (Hukawng Valley) of northern Myanmar, Insecta Linnaeus, 1758 mid-Cretaceous; see “Methods” section for more information Order Incertae sedis about provenance of the specimens. Family Mesophthiridae Gao, Shih, Rasnitsyn & Ren, fam. nov. Type genus. Mesophthirus Gao, Shih, Rasnitsyn & Ren, gen. Description. Holotype, CNU-MA2016009 (Figs. 1a, j, and 2a–c). nov. (Figs. 1–3) Small nymph, just 229 µm long excluding antenna (Table 1), but Diagnosis. Based only on nymphs of elder developmental the largest one among these ten specimens. Head slightly thinner stages, while the adults unknown. Small insects, body wingless than the thorax in width, the length about 1/3 of the body length. and dorsoventrally flattened, head fully hypognathous, slightly Compound eyes reduced to single ommatidium, near globular narrower than thorax; eyes reduced; huge mandible with at shape, evidently protruding from both sides of head. Ocelli least four teeth; maxillary palp four-segmented; antenna with absent. Antenna short (46 μm) and robust, slightly shorter than five antennomeres, last antennomere slightly enlarged, with the width or length of head, with five antennomeres. Antennal two long setae and one short seta extending from apex, last scape slightly enlarged, shorter than pedicel, the first flagellomere antennomere longer than sub two antennomeres combined; shortest and thinnest, and the last or 5th one longest. Two long thorax equal to abdomen in length, with pronotum distinctly stiff setae, longer than the last flagellomere, together with a short longer than, and about as wide as mesonotum; tarsus with seta, fixed on the apex of the antenna (Fig. 2a, b). No annulations three tarsomeres, as long as tibia, basitarsus as thick as tibia, or other setulae visible. Chewing mouthpart area very clear, last (3rd) tarsomere very small, possessing a claw, and a pair of mandibles slightly extended vertically, enlarged and having four long and stiff setae. sharp teeth (Fig. 2b, c). The left and right mandibles apparently Genera included. Only the type genus, Mesophthirus Gao, can cross with each other. Maxillary palpus with four segments Shih, Rasnitsyn & Ren, gen. nov., described here. and tapered from base to top (Fig. 2c). Thorax equal to abdomen Remarks. Comparing with Phthiraptera, Mesophthiridae shows in width, but shorter than the latter. Pronotum clear, about as several plesiomorphies: toothed chewing mouthpart, robust wide as, and distinctly longer than either mesonotum or meta- thorax with pronotum not reduced in length and width, leg with notum. Legs short, about 92, 115, and 134 μm, referring to fore tarsus 3-segmented and spiracles present on meso- and meta- leg, middle leg, and hind leg, respectively. Fore legs with coxae thorax as well as on the first two abdominal segments. However, enlarged and nearly bulb shaped. Trochanter visible. Femora several putative morphological synapomorphies are shared by oval-shaped, much thicker and slightly longer than tibiae. Three 2 NATURE COMMUNICATIONS | (2019) 10:5424 | https://doi.org/10.1038/s41467-019-13516-4
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