Diverse transitional giant fleas from the Mesozoic era of China
´ Nel4 Diying Huang1, Michael S. Engel2,3, Chenyang Cai1, Hao Wu1 & Andre


Fleas are one of the major lineages of ectoparasitic insects and are now highly specialized for feeding on the blood of birds or mammals1. This has isolated them among holometabolan insect orders, although they derive from the Antliophora (scorpionflies and true flies). Like most ectoparasitic lineages, their fossil record is meagre and confined to Cenozoic-era representatives of modern families1, so that we lack evidence of the origins of fleas in the Mesozoic era. The origins of the first recognized Cretaceous stem-group flea, Tarwinia, remains highly controversial1. Here we report fossils of the oldest definitive fleas—giant forms from the Middle Jurassic and Early Cretaceous periods of China. They exhibit many defining features of fleas but retain primitive traits such as non-jumping hindlegs. More importantly, all have stout and elongate sucking siphons for piercing the hides of their hosts, implying that these fleas may be rooted among the pollinating ‘long siphonate’ scorpionflies of the Mesozoic. Their special morphology suggests that their earliest hosts were hairy or feathered ‘reptilians’, and that they radiated to mammalian and bird hosts later in the Cenozoic. The studied material (nine specimens) belongs to two different genera, one with two species from the Middle Jurassic Jiulongshan Formation at Daohugou (approximately 165 million years (Myr) ago), Ningcheng County, Inner Mongolia; and one monotypic genus from the Lower Cretaceous Yixian Formation (approximately 125 Myr old), at Huangbanjigou, Beipiao City, Liaoning Province. These fleas are extremely rare among the approximately 100,000 fossil insects in the collections of the Nanjing Institute of Geology and Palaeontology (Chinese Academy of Sciences). Males and females are known for the two genera. Taxonomic descriptions will be published elsewhere. Several characters are shared by these fleas. These wingless insects, with a dorsoventrally compressed body, are distinctly larger than Recent fleas, with body lengths of 14.0–20.6 mm in females (Fig. 1a, g, Supplementary Fig. 2a and Supplementary Information 1), 8.0–14.7 mm in males (Fig. 1e, Supplementary Fig. 1a, b and Supplementary Table 1). The females from the Middle Jurassic period bear several setae and scattered ctenidia on the body, particularly on the legs (Figs 1a, b, g, 2a–c, 3a, d and Supplementary Figs 1d, h–j, 2a, c, f–h, 3b, c, f), whereas modern Siphonaptera lack ctenidia on the metatibiae. The most impressive character is their long and serrate piercingsuctorial siphon, longer in the female (Figs 1a, d, g, i, 2b, Supplementary Figs 1g and 2a, d, e) than in the male (Figs 1f, 2c, 3a, b and Supplementary Fig. 1a, f). The abdomens are large and broad with sclerites that are more reduced in females than in males (probably an adaptation for absorbing liquids, as in modern bloodfeeders) (Figs 1a, e, g, 3a, d, Supplementary Figs 1a, b, 2a, c and 3e). The highly modified pretarsal claws are long, nearly perpendicular to the last tarsal segment, and slightly curved with a prominent basal lobe forming a deep notch (Fig. 1f, Supplementary Figs 1e and 2f–h), a specialization for avoiding entanglement among hairs or feathers. A more complete list of characters is given in the Supplementary Information.

These new fossils have a large and broad abdomen, a relatively small head and thorax, long legs, no wings, short and compact antenna, ctenidia on legs, probably long siphon-like mouthparts and male genitalia that are exposed and large1. This general body shape is shared with the younger, Aptian-aged Tarwinia flea from Australia1–3. Unlike our fossils, Tarwinia has a 15-segmented flagellum3 instead of 14- to 17-segmented (Fig. 1c, e, h, Supplementary Figs 1c, 2b and 3a, d) distinctive metatibial ctenidia1, and lacks stout, posteriorly directed setae. Saurophthirus, a genus of flea from the Early Cretaceous of Russian Transbaikalia, is also a parasitic insect that may have had siphonate mouthparts, compact antenna and posteriorly directed setae1. It probably has very close affinity with our fleas from the Mesozoic era. The most notable structure of these new fossils is their long siphonate mouthparts that are comprised of two sealed half-tubes of labial origin with segmentation that is apparently lost and a pair of very long lacinia (Figs 1d, i, 3b, Supplementary Figs 1g and 2a, d, e). These fossils differ from all of the paraneopteran orders in their five-segmented tarsi (Figs 2a–c, 3a and Supplementary Fig. 2f–h). The large and welldeveloped male genitalic structures (Figs 1e, 2c, 3a, c and Supplementary Fig. 1a, b) are reminiscent of the similarly prominent structures of many Antliophora and Amphismenoptera1,4. These structures are generally less developed in other Holometabola, and those of the modern fleas are reduced still further and do not project so markedly from the apex of the abdomen5,6. These Mesozoic insects differ from the Mecoptera in a set of characters that is shared by the modern fleas (Supplementary Fig. 4). These structures are correlated with haematophagy, and are present in several other insect groups such as the Phthiraptera (lice) and even among some true flies. Recent and Cenozoic fleas have puncturing, suctorial and posteriorly directed mouthparts without mandibles, long and sharp half-tube labial palps and long serrate lacinia, homologous to the mouthparts of the new fossils5,7. In the modern fleas the labial palps can be incompletely divided into segments, a feature that may correspond to the one-segmented labial palps in our fossils (Fig. 1d, i, Supplementary Fig. 1f and 2e). An apparent difference is that the mouthparts of modern fleas are relatively short compared to those of the Mesozoic fleas, but because they can extend as far as the apex of the thorax, they are proportionally about the same length relative to the overall body size, because the body structures of modern fleas are more compact. The mouthpart structures of these Mesozoic fleas closely resemble those of the Mesozoic siphonate mecopteran family Aneuretopsychidae (and probably those of the Mesopsychidae), except for their prognathous position. Even the ornamentation of the laciniae (bearing small teeth) is identical between the Mesozoic fleas (Fig. 1d, i and Supplementary Fig. 2e) and the Aneuretopsychidae8. Therefore, it is likely that the Mesozoic flea lineage is rooted near the nectar-feeding siphonate Mecoptera, if the Mesozoic fleas acquired new specializations in relation to their adaptation to haematophagy (listed in legend of Fig. 4).

State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China. 2Division of Entomology, Natural History Museum, University of Kansas, Lawrence, Kansas 66049-2811, USA. 3Department of Ecology & Evolutionary Biology, University of Kansas, Lawrence, Kansas 66049-2811, USA. 4CNRS UMR 7205, CP 50, ´um National d’Histoire Naturelle, Paris F-75005, France. Entomologie, Muse 8 M A R C H 2 0 1 2 | VO L 4 8 3 | N AT U R E | 2 0 1

©2012 Macmillan Publishers Limited. All rights reserved

Enlargement of a. e. Mouthparts of 154247a. Taxon A. siphon. male. China. b. antenna. general habitus. 154244a. female. 2 0 2 | N AT U R E | VO L 4 8 3 | 8 M A R C H 2 0 1 2 ©2012 Macmillan Publishers Limited. c. counter-imprint of a. female. gonocoxite. g. 154244b. fifth tarsomeres and claws. female. 154247a. a. e and g. 154245. b. general habitus. mesotibial ctenidia. labial palps. Gc. h and i. Mouthparts of 154244b.RESEARCH LETTER a c d e La b Lp Lp f g i Si Lp h La Lp Figure 1 | Giant fleas from the Middle Jurassic of Daohugou. mouthparts. gonostylus. Enlargement of e. a–f. 500 mm in b and c. Figure 2 | Line drawings of the Middle Jurassic period fleas of Taxon A. c. La. Si. 1 mm in d. h. g–i. Enlargement of g. 2 mm in a. Lp. d. male. All rights reserved . Taxon B. Enlargement of a. Scale bars. Scale bars. f. a. imprint. Gs. 154245. general habitus. f. 2 mm. i. laciniae. 154244a. antenna.

these Mesozoic species and modern fleas have very different chorologies. Clade A (Siphonaptera) is characterized by a complete absence of wings. Thus. Molecular studies have suggested that the scorpionflies are paraphyletic. Taxon C. posteriorly directed setae and distinctive ctenidia. absence of ocelli. general habitus. The clade that includes Aneuretopsychidae and Siphonaptera is supported by the presence of a stylate proboscis with serrate laciniae. whereas other basal families attack metatherians and rodent lineages. Clade B (Mesozoic fleas) is characterized by the presence of ctenidia on the tibiae. our Mesozoic species and the modern fleas. the adults of nearly all modern fleas are ectoparasites of mammals. as traditionally defined. although this clade is weakly supported by characters that are not visible in our fossils. the new fossils and the modern fleas. 154250a. correlating well with 8 M A R C H 2 0 1 2 | VO L 4 8 3 | N AT U R E | 2 0 3 ©2012 Macmillan Publishers Limited. the Boreidae have strong mandibles. The Nannochoristidae are currently considered ‘‘liquid feeders. and highly reduced external portions of the male genitalia (gonocoxae. and laterally compressed bodies. gonostyli).10.12. Although their larvae are generally detritivorous in the nests of their hosts. a. Modern fleas Holocene palps4. 1. male genitalia. saltatorial hindlegs. Clade C (modern fleas) is characterized by a laterally flattened body. a recent work suggests that the Boreidae are possibly the sister group of the Siphonaptera plus Diptera11.LETTER RESEARCH a b d c Gc Gs Figure 3 | Giant fleas from the Early Cretaceous period of Huangbanjigou. Hence. 3. 154249a. the affinities of the fleas and flies within the mecopteran ‘stock’ remain uncertain. 15). It also suggests that one lineage evolved early to become the Diptera during the Early Triassic period1 and that the second diversified into the nectar-sucking siphonate Mecoptera and the blood-sucking fleas during the Jurassic with a further specialization into the modern fleas during the Mesozoic and Palaeogene periods. The idea of a fleas–flies sister-group relationship implies that the two lineages that gave rise to the Diptera and the Siphonaptera separated during the Permian period. These associations have supported the idea that fleas diversified at the same time as the Theria. the molecular phylogenetic studies9. All rights reserved . 2. Enlargement of a. Scale bars. and as long ago as the Late Jurassic17. The alate siphonate Mecoptera are thought to have fed on ‘‘ovular secretions of extinct gymnosperms’’ (ref. male. perhaps because the fleas needed vertebrate hosts with fur or feathers that emerged in the Late Triassic.9. becoming nectarivous during the Cretaceous16. hindlegs with enlarged coxae and femora that are modified for jumping. 1 mm in b and c. Early Cretaceous fleas. and these resemble the siphon structures of the siphonate Mecoptera. most likely on nectar of flowers and/or juices of fruits’’ (ref. 15). a–d. female. the results of the molecular analyses do not a priori conflict with possible close affinities between the siphonate mecopteran lineage. mouthparts. Furthermore. However. The switch by the insects from feeding on plant fluids to haematophagy is paralleled in reverse by the haematophagous Ceratopogonidae. This is different from those features of modern adult fleas that facilitate movements among the feathers or fur of their hosts. Tarwinia. The Nannochoristidae have tube-like labial palps with elongate lacinia and very small mandibles14. 2 mm in a and d. a dorsoventrally compressed body. which were first haematophagous. all of which are plesiomorphies that do not correspond to the mouthpart structures of the modern fleas and to those of Mesozoic fleas. general habitus. It seems that the arrival of fleas in the Jurassic was delayed compared to the arrival of flies in the Triassic. b. Our Mesozoic giant fleas have dorsoventrally flattened bodies and unmodified metacoxae and metafemora. with multiple derived lineages shifting to birds in several higher families17. eyes that are highly reduced. a compact antennal flagellum. c. The most basal family of modern fleas (Tungidae) principally feed on sloths and armadillos. a sister group to the Chironomidae. subcuticular or lost. and largely desclerotized and membranous abdominal sternites in females. which corresponds well to the Mesozoic siphonate Mecoptera. Thus.10 ignore several fossil groups and particularly the extinct ‘long siphonate mecopteran’ families. A dipteran–nannomecopteran–siphonapteran clade rather than a Boreidae–dipteran–siphonapteran clade was recently supported13. Middle Jurassic fleas. and long pretarsal claws with a prominent basal lobe. Nevertheless. loss of or greatly reduced eyes. d. relatively short lacinia and labial Siphonoptera Quaternary Other Mecoptera Boreidae Aneuretopsychidae Diptera Pleistocene Pliocene Milocene Oligocene Eocene Paleocene Paleogene Cenozoic Neogene Nannochoristidae Cretaceous Late Early Mesozoic Jurassic Late Middle Early 3 125 Myr ago 2 165 Myr ago 1 B C Triassic Late Middle Early Lopingian ? Mesozoic fleas A Paleozoic Permian Guadalupian Cisuralian Figure 4 | Phylogeny of Siphonaptera and related clades. Enlargement of a. and this means that the Boreidae would be the living sister-group to the true fleas1.

& Wheeler. Longstanding entomological problem finally solved? Head morphology of Nannochorista (Mecoptera. D. 46. G. 6. D. it is possible that our Mesozoic fleas were ectoparasites of early therians or other early mammals such as multituberculates.H. Y. Mandibulate chironomids: primitive or derived? (Diptera: Chironomidae). J. 15. 33. F. & Engel. E. Aphaniptera). d. Financial support was provided by the National Natural Science Foundation of China. A. F. 1988). Q. E. Invertebrates. A new insect from the Cretaceous of Transbaikalia. D. This indicates that these Mesozoic species were living on hosts that were covered by fur or feathers. 1020–1026 (2002). G. K. The adult head structures of Tipulomorpha (Diptera. A Mesozoic gliding mammal from northeastern China. Meng. Thus. Assoc. (huangdiying@sina. F. 21. f. and A. Its very elongated and slender legs suggest that it probably lived on very different animals. J. Koonwarra Fossil Bed (Korumburra Group). Xu. Nature 227. 442–445 (2011). Carpenter. Geol. The fossils were prepared using a sharp knife. 119. Insecta) and possible phylogenetic implications. Xu. [transl. Y.. 1. Nature 476. Azar. Author Information Reprints and permissions information is available at www. posteriorly directed setae and the long curved claws with a prominent basal lobe are clearly specialized structures in which hairs may become firmly lodged. rather than on vertebrates with skin that was nude or covered with scales. Ren. Res. Mem.. Wang. accepted 6 January 2012.22.S. A. Zool. 418–433 (2008). Coll. J.nature. in contrast to the adults of their modern counterparts. Z. Wang. I. A probable pollination mode before angiosperms: Eurasian. 316–343 (2011). Indeed. like some modern earwigs that are epizoic on bats. Wang for discussions and S. 8. longproboscid scorpionflies. Misc. 31. 2. Fan for technical assistance. M. Kluge. W. Entomol. Zhou. Arthropod Struct.fr). Acta Zool. Assoc. W. Photographs were taken using the Zeiss Discovery V20 microscope system. 7.E. mainly insects. 339–343 (1976).. Wheeler. 23. C. Whiting. Correspondence and requests for materials should be addressed to D. D. 840–847 (2009).N. 209–228 (2008). F. Friedrich.. Nature 455. Cheetham. Q. C.RESEARCH LETTER the age of our fossils. Evolution of the Insects (Cambridge Univ.. L. 12. S. 51. 9..] 82. Z. Received 22 November 2011. 3. METHODS SUMMARY The material is housed at Nanjing Institute of Geology and Palaeontology. F. Supplementary Information is linked to the online version of the paper at www. Chinese Academy of Sciences (KZCX2-YW-QN104) and the US National Science Foundation (DEB-0542909).. A. Jell. 93–104 (2002). Syst. M.. R. M. Palmer. Readers are welcome to comment on the online version of this article at www. & Nel. Convergent dental adaptations in pseudo-tribosphenic and tribosphenic mammals. Benton. Ponomarenko. Rev. F. A. Dev. Wang for presenting specimen 154244. Davis and X. Supplementary Figs 1a. Snodgrass. Australas. C. prepared the manuscript. it is also possible that the hosts of these early fleas were among the feathered dinosaurs of the period that became wellknown from the same deposits18. but fed on a range of vertebrate lineages. P. & Beutel. J. Riek.. Victoria. F. Zoological Syst. This would suggest that these early fleas eventually shifted from non-mammalian hosts to the Theria and then became specialized further. A. 111–128 (2010). 3.com/nature. indicating diversity among Mesozoic vertebrate ectoparasites. 50–74 (2010). 889–893 (2006). Wang. Evol. J. T. 37. Whiting. X.-X.. Orr. & Yuan. S. A bizarre Jurassic maniraptoran from China with elongate ribbon-like feathers. 10.N. Evol. and such taxa are well represented in the Jurassic and Early Cretaceous of China at the same or adjacent localities18–21. Ji. 92. D. However. & Sullivan. & Baum. & Dittmar. Rev. 18. A molecular phylogeny of fleas (Insecta: Siphonaptera): origins and host associations. 2005). from the freshwater Lower Cretaceous. 1–68 (1997). 2 0 4 | N AT U R E | VO L 4 8 3 | 8 M A R C H 2 0 1 2 ©2012 Macmillan Publishers Limited. R. The authors declare no competing financial interests. M. 111–205 (1986). Terrestr. Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. J. Zhang. Press. Q. elongate. 22. Luo. Schneeberg. F.-X. Z. Syst. R. M. did not live exclusively on their host. 10. X. & Whiting. F. 3b. perhaps late in the Cretaceous period or in the earliest Cenozoic era. 1–89 (1946). 746–747 (1970). Nature 444. 93–97 (2007).. Syst. Beutel. making the large size of these Mesozoic species and the robustness of their mouthparts seem mismatched. L.. J. 17. The homology of mouthparts in fleas (Insecta. 11. B. Res. Saurophthirus was purportedly a pterosaur ectoparasite23. Male Genitalia and Phylogeny of Pulicoidea (Koeltz Sci. R. Head morphology of Caurinus (Boreidae. The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal sequences and morphology. Published online 29 February 2012. Lower Cretaceous fleas. 2b–d and 3a–d. M. All rights reserved . eventually giving rise to the plague-carrying species that have so markedly altered the course of human history.nature. and X. 1105–1108 (2008). 19.. Mecoptera) and its phylogenetic implications. National Basic Research Program of China (2012CB821900). & Kearns. M. Bull. Scr. M. Biol. Entomol. d–j.. Kansas Sci. J. 16. E. Alternatively. 14. Cladistics 24. Paleontol. Luo. 4.com/nature. Z. Veltz. A systematic study of the family Boreidae (Mecoptera). N. N. Zool.. The remarkable fossils from the Early Cretaceous Jehol Biota of China and how they have changed our knowledge of Mesozoic life. moistened with 70% alcohol (Figs 1c. Penny. Proc.. Univ.com) or A. Grimaldi. D. Zhang. R. K. C. Diversity of feeding strategies in adult Mecoptera. Zhang. Acknowledgements We are grateful to X. 5. f) and drawings were made using a camera lucida on a binocular Olympus SZX7. South Gippsland. 346–367 (2008). Whiting. Beutel. X. M. Friedrich.. Author Contributions All authors participated in morphological studies. Whiting. et al. Smith. The stiff. including early mammals. Press. M. 141–217 (1977). M. S.. 104. & Duncan. Hu. G. P. 13. Short. 20. G. The skeletal anatomy of fleas (Siphonaptera). 677–707 (2008). F. 46. C. which were diverse and abundant at the time. Meng. it is possible that these early fleas. Yuan. & Li. Nature 450. 48. C.. X. Y. P.H. the early mammals were small animals. & Ji. a possible parasite of pterosaurians. Palaeontol 3. The much later diversification of placental mammals (Eutheria) supported the substantial radiation of higher Eusiphonaptera and particularly of the diverse Neosiphonaptera (Ceratophyllomorpha and Pulicomorpha). Zhang. Arthr. G.nature. 688–699 (2008). Q. (anel@mnhn.com/reprints. A Jurassic eutherian mammal and divergence of marsupials and placentals. Science 326. Hastriter. D. C. Insecta) and their phylogenetic implications. & Beutel. The thoracic morphology of Nannochorista (Nannochoristidae) and its implications for the phylogeny of Mecoptera and Antliophora.