LETTER

Diverse transitional giant fleas from the Mesozoic era of China

doi:10.1038/nature10839

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 fleasgiant 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 14.020.6 mm in females (Fig. 1a, g, Supplementary Fig. 2a and Supplementary Information 1), 8.014.7 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, 2ac, 3a, d and Supplementary Figs 1d, hj, 2a, c, fh, 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 2fh), a specialization for avoiding entanglement among hairs or feathers. A more complete list of characters is given in the Supplementary Information.
1

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 Australia13. 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 2ac, 3a and Supplementary Fig. 2fh). 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 dHistoire 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

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a c d e

La

b
Lp Lp

Si

Lp

La Lp

Figure 1 | Giant fleas from the Middle Jurassic of Daohugou, China. af, Taxon A. gi, Taxon B. a, 154244a, female, general habitus. b, Enlargement of a, mesotibial ctenidia. c, Enlargement of a, antenna. d, Mouthparts of 154244b. e, 154245, male, general habitus. f, Enlargement of e, mouthparts, fifth

tarsomeres and claws. g, 154247a, female, general habitus. h, Enlargement of g, antenna. i, Mouthparts of 154247a. Scale bars, 2 mm in a, e and g, 1 mm in d, f, h and i, 500 mm in b and c. Gc, gonocoxite; Gs, gonostylus; La, laciniae; Lp, labial palps; Si, siphon.

Figure 2 | Line drawings of the Middle Jurassic period fleas of Taxon A. a, 154244a, female, imprint. b, 154244b, counter-imprint of a. c, 154245, male. Scale bars, 2 mm.
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a b d

Gc Gs

Figure 3 | Giant fleas from the Early Cretaceous period of Huangbanjigou. ad, Taxon C. a, 154249a, male, general habitus. b, Enlargement of a, mouthparts. c, Enlargement of a, male genitalia. d, 154250a, female, general habitus. Scale bars, 2 mm in a and d, 1 mm in b and c.

Molecular studies have suggested that the scorpionflies are paraphyletic, as traditionally defined, and this means that the Boreidae would be the living sister-group to the true fleas1,9,10. However, a recent work suggests that the Boreidae are possibly the sister group of the Siphonaptera plus Diptera11, although this clade is weakly supported by characters that are not visible in our fossils. Nevertheless, the Boreidae have strong mandibles, 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

Paleozoic Permian

Guadalupian Cisuralian

Figure 4 | Phylogeny of Siphonaptera and related clades. The clade that includes Aneuretopsychidae and Siphonaptera is supported by the presence of a stylate proboscis with serrate laciniae. Clade A (Siphonaptera) is characterized by a complete absence of wings, loss of or greatly reduced eyes, absence of ocelli, a compact antennal flagellum, posteriorly directed setae and distinctive ctenidia, and long pretarsal claws with a prominent basal lobe. Clade B (Mesozoic fleas) is characterized by the presence of ctenidia on the tibiae, a dorsoventrally compressed body, and largely desclerotized and membranous abdominal sternites in females. Clade C (modern fleas) is characterized by a laterally flattened body, saltatorial hindlegs, eyes that are highly reduced, subcuticular or lost, and highly reduced external portions of the male genitalia (gonocoxae, gonostyli). 1, Middle Jurassic fleas; 2, Early Cretaceous fleas; 3, Tarwinia.

Modern fleas

Holocene

palps4,12, all of which are plesiomorphies that do not correspond to the mouthpart structures of the modern fleas and to those of Mesozoic fleas. A dipterannannomecopteransiphonapteran clade rather than a Boreidaedipteransiphonapteran clade was recently supported13. The Nannochoristidae have tube-like labial palps with elongate lacinia and very small mandibles14, and these resemble the siphon structures of the siphonate Mecoptera, the new fossils and the modern fleas. The Nannochoristidae are currently considered liquid feeders, most likely on nectar of flowers and/or juices of fruits (ref. 15), which corresponds well to the Mesozoic siphonate Mecoptera. Hence, the affinities of the fleas and flies within the mecopteran stock remain uncertain. Furthermore, the molecular phylogenetic studies9,10 ignore several fossil groups and particularly the extinct long siphonate mecopteran families. Thus, the results of the molecular analyses do not a priori conflict with possible close affinities between the siphonate mecopteran lineage, our Mesozoic species and the modern fleas. The idea of a fleasflies sister-group relationship implies that the two lineages that gave rise to the Diptera and the Siphonaptera separated during the Permian period. 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. It seems that the arrival of fleas in the Jurassic was delayed compared to the arrival of flies in the Triassic, perhaps because the fleas needed vertebrate hosts with fur or feathers that emerged in the Late Triassic. The alate siphonate Mecoptera are thought to have fed on ovular secretions of extinct gymnosperms (ref. 15). The switch by the insects from feeding on plant fluids to haematophagy is paralleled in reverse by the haematophagous Ceratopogonidae, a sister group to the Chironomidae, which were first haematophagous, becoming nectarivous during the Cretaceous16. Our Mesozoic giant fleas have dorsoventrally flattened bodies and unmodified metacoxae and metafemora. This is different from those features of modern adult fleas that facilitate movements among the feathers or fur of their hosts; hindlegs with enlarged coxae and femora that are modified for jumping, and laterally compressed bodies. Thus, these Mesozoic species and modern fleas have very different chorologies. Although their larvae are generally detritivorous in the nests of their hosts, the adults of nearly all modern fleas are ectoparasites of mammals, with multiple derived lineages shifting to birds in several higher families17. The most basal family of modern fleas (Tungidae) principally feed on sloths and armadillos, whereas other basal families attack metatherians and rodent lineages. These associations have supported the idea that fleas diversified at the same time as the Theria, and as long ago as the Late Jurassic17, correlating well with
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the age of our fossils. Indeed, it is possible that our Mesozoic fleas were ectoparasites of early therians or other early mammals such as multituberculates, which were diverse and abundant at the time, and such taxa are well represented in the Jurassic and Early Cretaceous of China at the same or adjacent localities1821. However, the early mammals were small animals, making the large size of these Mesozoic species and the robustness of their mouthparts seem mismatched. The stiff, elongate, posteriorly directed setae and the long curved claws with a prominent basal lobe are clearly specialized structures in which hairs may become firmly lodged. This indicates that these Mesozoic species were living on hosts that were covered by fur or feathers, rather than on vertebrates with skin that was nude or covered with scales. Thus, 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 deposits18,22. Saurophthirus was purportedly a pterosaur ectoparasite23. Its very elongated and slender legs suggest that it probably lived on very different animals, indicating diversity among Mesozoic vertebrate ectoparasites. Alternatively, it is possible that these early fleas, in contrast to the adults of their modern counterparts, did not live exclusively on their host, like some modern earwigs that are epizoic on bats, but fed on a range of vertebrate lineages, including early mammals. This would suggest that these early fleas eventually shifted from non-mammalian hosts to the Theria and then became specialized further, perhaps late in the Cretaceous period or in the earliest Cenozoic era. The much later diversification of placental mammals (Eutheria) supported the substantial radiation of higher Eusiphonaptera and particularly of the diverse Neosiphonaptera (Ceratophyllomorpha and Pulicomorpha), eventually giving rise to the plague-carrying species that have so markedly altered the course of human history.
6. 7. 8. 9. Cheetham, T. B. Male Genitalia and Phylogeny of Pulicoidea (Koeltz Sci. Press, 1988). Kluge, N. J. The homology of mouthparts in fleas (Insecta, Aphaniptera). Entomol. Rev. [transl.] 82, 10201026 (2002). Ren, D. et al. A probable pollination mode before angiosperms: Eurasian, longproboscid scorpionflies. Science 326, 840847 (2009). Whiting, M. F., Carpenter, J. M., Wheeler, Q. D. & Wheeler, W. C. The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal sequences and morphology. Syst. Biol. 46, 168 (1997). Whiting, M. F. Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zool. Scr. 31, 93104 (2002). Friedrich, F. & Beutel, R. G. The thoracic morphology of Nannochorista (Nannochoristidae) and its implications for the phylogeny of Mecoptera and Antliophora. J. Zool. Syst. Evol. Res. 48, 5074 (2010). Beutel, R. G., Friedrich, F. & Whiting, M. F. Head morphology of Caurinus (Boreidae, Mecoptera) and its phylogenetic implications. Arthropod Struct. Dev. 37, 418433 (2008). Schneeberg, K. & Beutel, R. G. The adult head structures of Tipulomorpha (Diptera, Insecta) and their phylogenetic implications. Acta Zool. 92, 316343 (2011). Beutel, R. G. & Baum, E. Longstanding entomological problem finally solved? Head morphology of Nannochorista (Mecoptera, Insecta) and possible phylogenetic implications. J. Zoological Syst. Evol. Res. 46, 346367 (2008). Palmer, C. M. Diversity of feeding strategies in adult Mecoptera. Terrestr. Arthr. Rev. 3, 111128 (2010). Azar, D., Veltz, I. & Nel, A. Mandibulate chironomids: primitive or derived? (Diptera: Chironomidae). Syst. Entomol. 33, 688699 (2008). Whiting, M. F., Whiting, A. S., Hastriter, M. W. & Dittmar, K. A molecular phylogeny of fleas (Insecta: Siphonaptera): origins and host associations. Cladistics 24, 677707 (2008). Benton, M. J., Zhang, Z., Orr, P. J., Zhang, F. & Kearns, S. L. The remarkable fossils from the Early Cretaceous Jehol Biota of China and how they have changed our knowledge of Mesozoic life. Proc. Geol. Assoc. 119, 209228 (2008). Luo, Z.-X., Ji, Q. & Yuan, C. Convergent dental adaptations in pseudo-tribosphenic and tribosphenic mammals. Nature 450, 9397 (2007). Meng, J., Hu, Y., Wang, Y., Wang, X. & Li, C. A Mesozoic gliding mammal from northeastern China. Nature 444, 889893 (2006). Luo, Z.-X., Yuan, C., Meng, Q. & Ji, Q. A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 476, 442445 (2011). Zhang, F., Zhou, Z., Xu, X., Wang, X. & Sullivan, C. A bizarre Jurassic maniraptoran from China with elongate ribbon-like feathers. Nature 455, 11051108 (2008). Ponomarenko, A. G. A new insect from the Cretaceous of Transbaikalia, a possible parasite of pterosaurians. Paleontol. J. 10, 339343 (1976).

10. 11.

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13. 14.

15. 16. 17.

18.

19. 20. 21. 22.

METHODS SUMMARY
The material is housed at Nanjing Institute of Geology and Palaeontology. The fossils were prepared using a sharp knife. Photographs were taken using the Zeiss Discovery V20 microscope system, moistened with 70% alcohol (Figs 1c, d, f, 3b, Supplementary Figs 1a, dj, 2bd and 3ad, f) and drawings were made using a camera lucida on a binocular Olympus SZX7.
Received 22 November 2011; accepted 6 January 2012. Published online 29 February 2012. 1. 2. 3. 4. 5. Grimaldi, D. & Engel, M. S. Evolution of the Insects (Cambridge Univ. Press, 2005). Riek, E. F. Lower Cretaceous fleas. Nature 227, 746747 (1970). Jell, P. A. & Duncan, P. M. Invertebrates, mainly insects, from the freshwater Lower Cretaceous, Koonwarra Fossil Bed (Korumburra Group), South Gippsland, Victoria. Mem. Assoc. Australas. Palaeontol 3, 111205 (1986). Penny, N. D. A systematic study of the family Boreidae (Mecoptera). Univ. Kansas Sci. Bull. 51, 141217 (1977). Snodgrass, R. E. The skeletal anatomy of fleas (Siphonaptera). Smith. Misc. Coll. 104, 189 (1946).

23.

Supplementary Information is linked to the online version of the paper at www.nature.com/nature. Acknowledgements We are grateful to X. D. Wang for presenting specimen 154244, A. Short, X. Xu, F. C. Zhang, and X. L. Wang for discussions and S. Davis and X. Y. Fan for technical assistance. Financial support was provided by the National Natural Science Foundation of China, National Basic Research Program of China (2012CB821900), Chinese Academy of Sciences (KZCX2-YW-QN104) and the US National Science Foundation (DEB-0542909). Author Contributions All authors participated in morphological studies. D.H., M.S.E. and A.N. prepared the manuscript. Author Information Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests. Readers are welcome to comment on the online version of this article at www.nature.com/nature. Correspondence and requests for materials should be addressed to D.H. ([email protected]) or A.N. ([email protected]).

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