Diverse transitional giant fleas from the Mesozoic era of China

Abstract

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Giant fleas from the Middle Jurassic of Daohugou, China.
Figure 2: Line drawings of the Middle Jurassic period fleas of Taxon A.
Figure 3: Giant fleas from the Early Cretaceous period of Huangbanjigou.
Figure 4: Phylogeny of Siphonaptera and related clades.

References

  1. 1

    Grimaldi, D. & Engel, M. S. Evolution of the Insects (Cambridge Univ. Press, 2005)

    Google Scholar 

  2. 2

    Riek, E. F. Lower Cretaceous fleas. Nature 227, 746–747 (1970)

    CAS  ADS  Article  Google Scholar 

  3. 3

    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, 111–205 (1986)

    Google Scholar 

  4. 4

    Penny, N. D. A systematic study of the family Boreidae (Mecoptera). Univ. Kansas Sci. Bull. 51, 141–217 (1977)

    Google Scholar 

  5. 5

    Snodgrass, R. E. The skeletal anatomy of fleas (Siphonaptera). Smith. Misc. Coll. 104, 1–89 (1946)

    Google Scholar 

  6. 6

    Cheetham, T. B. Male Genitalia and Phylogeny of Pulicoidea (Koeltz Sci. Press, 1988)

  7. 7

    Kluge, N. J. The homology of mouthparts in fleas (Insecta, Aphaniptera). Entomol. Rev. [transl.]. 82, 1020–1026 (2002)

    Google Scholar 

  8. 8

    Ren, D. et al. A probable pollination mode before angiosperms: Eurasian, longproboscid scorpionflies. Science 326, 840–847 (2009)

    CAS  ADS  Article  Google Scholar 

  9. 9

    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, 1–68 (1997)

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    Whiting, M. F. Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zool. Scr. 31, 93–104 (2002)

    Article  Google Scholar 

  11. 11

    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, 50–74 (2010)

    Article  Google Scholar 

  12. 12

    Beutel, R. G., Friedrich, F. & Whiting, M. F. Head morphology of Caurinus (Boreidae, Mecoptera) and its phylogenetic implications. Arthropod Struct. Dev. 37, 418–433 (2008)

    Article  Google Scholar 

  13. 13

    Schneeberg, K. & Beutel, R. G. The adult head structures of Tipulomorpha (Diptera, Insecta) and their phylogenetic implications. Acta Zool. 92, 316–343 (2011)

    Article  Google Scholar 

  14. 14

    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, 346–367 (2008)

    Article  Google Scholar 

  15. 15

    Palmer, C. M. Diversity of feeding strategies in adult Mecoptera. Terrestr. Arthr. Rev. 3, 111–128 (2010)

    Article  Google Scholar 

  16. 16

    Azar, D., Veltz, I. & Nel, A. Mandibulate chironomids: primitive or derived? (Diptera: Chironomidae). Syst. Entomol. 33, 688–699 (2008)

    Article  Google Scholar 

  17. 17

    Whiting, M. F., Whiting, A. S., Hastriter, M. W. & Dittmar, K. A molecular phylogeny of fleas (Insecta: Siphonaptera): origins and host associations. Cladistics 24, 677–707 (2008)

    Article  Google Scholar 

  18. 18

    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, 209–228 (2008)

    Article  Google Scholar 

  19. 19

    Luo, Z.-X., Ji, Q. & Yuan, C. Convergent dental adaptations in pseudo-tribosphenic and tribosphenic mammals. Nature 450, 93–97 (2007)

    CAS  ADS  Article  Google Scholar 

  20. 20

    Meng, J., Hu, Y., Wang, Y., Wang, X. & Li, C. A Mesozoic gliding mammal from northeastern China. Nature 444, 889–893 (2006)

    CAS  ADS  Article  Google Scholar 

  21. 21

    Luo, Z.-X., Yuan, C., Meng, Q. & Ji, Q. A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 476, 442–445 (2011)

    CAS  ADS  Article  Google Scholar 

  22. 22

    Zhang, F., Zhou, Z., Xu, X., Wang, X. & Sullivan, C. A bizarre Jurassic maniraptoran from China with elongate ribbon-like feathers. Nature 455, 1105–1108 (2008)

    CAS  ADS  Article  Google Scholar 

  23. 23

    Ponomarenko, A. G. A new insect from the Cretaceous of Transbaikalia, a possible parasite of pterosaurians. Paleontol. J. 10, 339–343 (1976)

    Google Scholar 

Download references

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 information

Affiliations

Authors

Contributions

All authors participated in morphological studies. D.H., M.S.E. and A.N. prepared the manuscript.

Corresponding authors

Correspondence to Diying Huang or André Nel.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Text, Supplementary Table 1 and Supplementary Figures 1-4 with legends. (PDF 7455 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Huang, D., Engel, M., Cai, C. et al. Diverse transitional giant fleas from the Mesozoic era of China. Nature 483, 201–204 (2012). https://doi.org/10.1038/nature10839

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.