Long-term Comprehensive Studies of Ectoparasitic Insects from the Middle Mesozoic Chinese Compression Fossils and Myanmar Amber

Published in Ecology & Evolution
Long-term Comprehensive Studies of Ectoparasitic Insects from the Middle Mesozoic Chinese Compression Fossils and Myanmar Amber
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Author: Dr.  Chungkun Shih and Dr. Dong Ren

Many extant insects have ectoparasitic lifestyles, while spending long time or even entire life (obligate) on the skin, hairs or feathers of warm-blooded vertebrates, sucking blood or feeding on skin debris, hairs or feathers of their hosts (1). Ectoparasitic insects cause discomforts or sickness of hosts, reduce production of livestock, and damage avian feathers, etc (2). More seriously, ectoparasites transmit diseases as vectors (3), having resulted in catastrophic illnesses (e.g. plague and typhus) and deaths in human history (4). Fossil studies of ectoparasitic insects such as Phthiraptera (true lice) and Siphonaptera (fleas) are of high interest from scientific community so that their early and basal morphological characters and evolutionary development can be discovered and elucidated. 

Our Capital Normal University (CNU) Team started research work on compression fossils of basal fleas in 2010 (5). In 2012, we reported several relatively huge “basal fleas”, assigned to a new family Pseudopulicidae Gao, Shih & Ren, 2012, from the Middle Jurassic (165 Mya) Jiulongshan Formation and the Lower Cretaceous (125 Mya) Yixian Formation in northeastern China (6). These specimens have stout and elongate sucking stylet mouthparts for piercing, reduced wingless thorax, row of ctenidia on the tibiae, pygidium, etc. All these characters suggest their close relationships with the modern lineages of fleas. These fossil insects are different from extant fleas by the absence of modified jumping hind legs and the body not laterally compressed. Large body sizes (up to 22.8 mm) and long serrated stylets (up to 5.15 mm) for piercing tough and thick skin suggest that these ancient basal fleas might have lived on relatively large hosts, such as contemporaneous medium to large-sized vertebrates (6, 7, 8). Gao et al. in 2013 placed Saurophthirus exquisitus in Saurophthiridae Ponomarenko, 1986, and suggested this group as extinct “transitional fleas” of Siphonaptera based on three well-preserved fossils from the Early Cretaceous of China (9). In 2014, Gao et al. described a female transitional flea, Pseudopulex tanlan of Pseudopulicidae from the Early Cretaceous of China, which has an extremely distended abdomen suggesting that it might have consumed its last meal before death (10). 

However, we could not find any fossil true lice in our CNU vast collection of compression fossils from the Yixian Formation and Jiulongshan Formation of northeastern China. In the literature, integument-feeding insects have never been reported from the Mesozoic. The earliest known fossil louse, Megamenopon rasnitsyni, is from the Eocene of Germany (44 Mya) (11, 12), and it is already fully modern in form and assigned within Amblycera. Due to a lack of Mesozoic fossil records, the origin and early evolution of the feather- and other integument-feeding insects in the Mesozoic thus remains obscure (11, 13), even though many feathered dinosaurs and early birds have been described from the Jurassic and Cretaceous (14).

In the summer of 2014, our CNU Team started to collect and conduct studies with insects preserved in Myanmar (Burmese) amber, mid-Cretaceous (99 Mya). We discovered and reported ten nymph specimens of a new lineage of insect, Mesophthirus engeli Gao, Shih, Rasnitsyn & Ren, 2019, assigned to Mesophthiridae Gao, Shih, Rasnitsyn & Ren, 2019 of order Incertae sedis, crawled and fed on two feathers preserved in two pieces of amber, AMBER No. 01 (Fig. 1) and AMBER No. 02 (Fig. 2) (15). 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. (Fig. 3). 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 and early birds.

Mesophthirus shares several putative synapomorphies with Liposcelidae + Phthiraptera for their apterous and dorsoventral flattening body, reduced eyes, short antenna under 10 antennomeres. However, different from living lice (Phthiraptera), Mesophthirus specimens have a few putative plesiomorphies, such as 4-segmented maxillary palpus, spiracles on meso- and metathorax and on the first two abdominal segments, relatively long and wide pronotum, two stiff and long setae on pretarsi and three clavate setae on the apex of antenna. Based on these characters, it is difficult to place Mesophthiridae to any known order within Insecta, therefore we identify the taxon as an order incertae sedis here, pending more new material to be found in the future to further confirm its phylogenetic position (15).

The link to our paper in Nature Communications is:

https://www.nature.com/articles/s41467-019-13516-4

Fig. 1. AMBER No. 01 with the specimens of Mesophthirus engeli Gao, Shih, Rasnitsyn & Ren, 2019 from the mid-Cretaceous of Myanmar. (a and b) Details of feather showing locations of the specimens. (c) Holotype specimen CNU-MA2016009. (d to f) Paratypic specimens CNU-MA2016001, CNU-MA2016004 and CNU-MA2016006. (g) Stars in black showing the large areas of damages.

Fig. 2. AMBER No. 02 with the paratype of Mesophthirus engeli Gao, Shih, Rasnitsyn & Ren, 2019 from the mid-Cretaceous of Myanmar showing the insect crawling on the feather. 

Fig. 3. Artist’s reconstruction of Mesophthirus engeli Gao, Shih, Rasnitsyn & Ren, 2019 of elder development stage feeding on the feather (Artwork by Dr. Chen Wang).

References:
1. Gullan, P. J. & Cranston, P. S. The Insects: An Outline of Entomology (Fifth Edition). (Wiley-Blackwell Publishing Ltd, Oxford, 2014).
2. Lehane, M. J. The Biology of Blood-Sucking in Insects. (Cambridge Universiy Press, Cambridge, 2005).
3. Krasnov, B. R. Functional and Evolutionary Ecology of Fleas: A Model for Ecological Parasitology. (Cambridge University Press, Cambridge, 2008).
4. Welford, M. & Bossak, B. H. Revisiting the medieval Black Death of 1347–1351: Spatiotemporal dynamics suggestive of an alternate causation. Geography Compass 4(6), 561–575 (2010).
5. Ren, D., Shih, C.K., Gao, T.P., Wang, Y.J., Yao, Y.Z. Rhythms of insect evolution – evidence from the Jurassic and Cretaceous in northern China. (Wiley Blackwell, New York, 2019)
6. Gao, T.P, Shih, C.K. Xu, X. et al. Mid-Mesozoic flea-like ectoparasites of feathered or haired vertebrates. Current Biology, 22 (8), 732–735. doi: 10.1016/j.cub.2012.03.012 (2012)
7. Zhou, Z., Barrett, P.M. and Hilton, J. An exceptionally preserved Lower Cretaceous ecosystem. Nature, 421, 807–814. doi:10.1038/nature01420 (2003)
8. Xu, X. and Zhang, F. A new maniraptoran dinosaur from China with long feathers on the metatarsus. Naturwissenschaften, 92, 173–177. (2005)
9. Gao, T.P., Shih, C.K., Rasnitsyn, A.P. et al. New transitional fleas from China highlighting diversity of Early Cretaceous ectoparasitic insects. Current Biology, 23 (13), 1261–1266. doi:10.1016/j.cub.2013.05.040 (2013)
10. Gao, T.P., Shih, C.K., Rasnitsyn, A.P. et al. The first flea with fully distended abdomen from the Early Cretaceous of China. BMC Evolutionary Biology, 14, 168. doi:10.1186/s12862-014-0168-1 (2014)
11. Dalgleish, R. C., Palma, R. L., Price, R. D. & Smith, V. S. Fossil lice (Insecta: Phthiraptera) reconsidered. Systematic Entomology. 31(4), 648–651 (2006).
12. Wappler, T., Smith, V. S. & Dalgleish, R. C. Scratching an ancient itch: an Eocene bird louse fossil. Proc. R. Soc. Lond. B. 271 (2004).
13. Rasnitsyn, A. P. & Zherikhin, V. V. First fossil chewing louse from the Lower Cretaceous of Baissa, Transbaikalia (Insecta, Pediculida = Phthiriaptera, Saurodectidae fam. n.). Russian Entomol. J. 8(4), 253–255 (1999).
14. Xu, X. et al. An integrative approach to understanding bird origins. Science 346, 1253293 (2014).
15. Gao, T.P., Yin, X.C., Shih. C.K., Rasnitsyn, A.P., Xu, X., Chen, S., Wang, C. & Ren, D. New insects feeding on dinosaur feathers in mid-Cretaceous amber. Nature Communication. 10:5424. https://www.nature.com/articles/s41467-019-13516-4 (2019)

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