Skip to main content
NCBI home page
eLife logoLink to eLife
. 2014 Jun 24;3:e02844. doi: 10.7554/eLife.02844

Extreme adaptations for aquatic ectoparasitism in a Jurassic fly larva

Jun Chen 1,†, Bo Wang 2,3,*,†, Michael S Engel 4,†, Torsten Wappler 2, Edmund A Jarzembowski 3,5, Haichun Zhang 3, Xiaoli Wang 1, Xiaoting Zheng 1, Jes Rust 2
Editor: Detlef Weigel6
PMCID: PMC4067894  PMID: 24963142

Abstract

The reconstruction of ancient insect ectoparasitism is challenging, mostly because of the extreme scarcity of fossils with obvious ectoparasitic features such as sucking-piercing mouthparts and specialized attachment organs. Here we describe a bizarre fly larva (Diptera), Qiyia jurassica gen. et sp. nov., from the Jurassic of China, that represents a stem group of the tabanomorph family Athericidae. Q. jurassica exhibits adaptations to an aquatic habitat. More importantly, it preserves an unusual combination of features including a thoracic sucker with six radial ridges, unique in insects, piercing-sucking mouthparts for fluid feeding, and crocheted ventral prolegs with upward directed bristles for anchoring and movement while submerged. We demonstrate that Q. jurassica was an aquatic ectoparasitic insect, probably feeding on the blood of salamanders. The finding reveals an extreme morphological specialization of fly larvae, and broadens our understanding of the diversity of ectoparasitism in Mesozoic insects.

DOI: http://dx.doi.org/10.7554/eLife.02844.001

Research organism: none

eLife digest

Parasites have been exploiting other organisms for millions of years. However, little is known about ancient parasitic insects, as it is rare to find fossils that are preserved well enough for them to be identified as parasites. This is particularly true for ectoparasitic insects, which live on the skin of their hosts. As a result, the only widely accepted ectoparasitic insect from the Mesozoic era is the giant flea, which infested dinosaurs, pterosaurs or mammals.

Now, Chen, Wang, Engel et al. have discovered a new genus and species of ancient aquatic fly, which may be the earliest currently known aquatic ectoparasitic insect. Named Qiyia jurassica—after the Chinese word for ‘bizarre’ and the Jurassic period when it lived—its larva has a combination of features that mark it out as a parasitic ancestor of modern water snipe flies. In addition, the well-preserved fossilised larvae used to identify Q. jurassica have some more unusual features.

The mouth of Q. jurassica had a structure commonly found in ectoparasites, designed to pierce skin and suck blood. The larva also had several features that were particularly well-adapted for gripping the host animal while underwater. The prolegs—stumpy fleshy structures found on the abdomen—were covered in bristles that pointed upwards, anchoring the larva in place. Q. jurassica also had an unusual sucker on its thorax that would have provided a firm grip that held its head still during feeding. Although many modern aquatic ectoparasites—like leeches—have suckers, the Q. jurassica sucker may be unique amongst insect larvae, as it has six large ridges and is covered in spines. Both features may have provided extra grip.

Chen, Wang, Engel et al. suggest that Q. jurassica feasted on the blood of salamanders, as many salamander fossils have been found in the same region. The larvae could have attached to unexposed areas of the salamander—behind the gills, for example—where feeding would also have been easier due to the rich supply of blood vessels, and the thinner, more easily pierced skin.

The wide range of features found on Q. jurassica suggests that Mesozoic ectoparasitic insects were more diverse than previously thought.

DOI: http://dx.doi.org/10.7554/eLife.02844.002

Introduction

The early evolution of insect ectoparasites and their associations with hosts are poorly known (Labandeira, 2002; Wappler et al., 2004; Grimaldi and Engel, 2005). Although several Mesozoic insects were regarded as putative ectoparasites, only giant fleas have been widely accepted as definite terrestrial ectoparasitic insects on dinosaurs, pterosaurs, or mammals (Gao et al., 2012, 2013b; Huang et al., 2012, 2013). Here we report on an aquatic ectoparasitic insect based on five well-preserved specimens from the Middle Jurassic Daohugou beds of China. These fossils are extremely rare among the approximately 300,000 fossil insects in the collections of the Nanjing Institute of Geology and Palaeontology and Shandong Tianyu Museum of Nature.

Results

Systematic paleontology

Order Diptera Linnaeus, 1758

Family Athericidae Stuckenberg, 1973

Qiyia jurassica gen. et sp. nov.

Etymology

Qiyia is from the Chinese ‘qiyi’ meaning bizarre; jurassica is a reference to the Jurassic age of the fossils.

Type material

Holotype STMN65-1. Paratypes STMN65-2, NIGP156982, NIGP156983, NIGP156984. All specimens are preserved as carbonaceous impressions on the surface of grey tuffaceous siltstone (Wang et al., 2013).

Locality and age

From the Middle Jurassic Daohugou beds (approximately 165 million years old) of Ningcheng County, Inner Mongolia, China (Liu et al., 2006).

Diagnosis

Three thoracic segments fused, with a ventral sucker; two pairs of dorsal spines on abdominal segments 1–7; abdominal segments 1–6 with paired ventral prolegs bearing upward directed bristles and apical crochets; extended seventh proleg; two pairs of anal papillae; sclerotized terminal processes with stiff setae.

Description

Body elongate, 18–24 mm long (Table 1). Head greatly reduced and partly retractile into thorax (Figure 1A,B); antennae and eyes not visible (Figure 1C); a pair of sclerotized tentorial rods (Figure 2B). Mandibles approximately 0.6 mm long, heavily sclerotized, sickle-shaped, oriented to move parallel to each other in vertical plane, with external groove on adoral surface extending whole length of mandible (Figure 1E). Thoracic segment swollen, slightly narrower than abdomen (Figure 2A). Sucker retractile, diameter about 2 mm, located ventrally on thoracic segment and consisting of a circular suction disc with central opening about one quarter of disc diameter; peripheral area of disc thin and flexible (Figure 1D). Six robust, sclerotized ridges on sucker, radially arranged, covered by soft skin with small spines (Figure 2D,E); distal part of each ridge thickened, probably with three processes embedded in musculature (Figure 2E). Three pairs of small spines with simple shafts on dorsolateral margins of thorax, two pairs on dorsolateral margins of abdominal segments 1–7, and one pair on abdominal segment 8 (Figure 2A). Abdomen with eight distinct segments, covered by many short setae. Abdominal segments 1–6 with a pair of cylindrical, ventral prolegs covered by stiff, upward directed bristles; each proleg nearly half width of body with two rows of six crochet hooks apically (Figure 1F); seventh proleg approximately three times longer than other prolegs with only three or four apical hooks; abdominal segment 8 with two pairs of slender, tapering anal papillae: first pair long, approximately quarter body length; second pair half the length of the first pair (Figure 1A,B); one pair of unsegmented, sclerotized terminal processes fringed with stiff setae, approximately one-tenth body length; each process with about 10 spiracles (Figure 1G, Figure 2C).

Table 1.

Measurements of specimens of Qiyia jurassica

DOI: http://dx.doi.org/10.7554/eLife.02844.003

Holotype STMN65-1 Paratype STMN65-2 Paratype NIGP156982 Paratype NIGP156983 Paratype NIGP156984
Orientation lateral lateral dorsal dorsal lateral
Body 23.8 22.1 22.9 ∼22 18.1
Head ∼1 ∼1 ∼1 – 0.8
Thorax 2.8 2.5 2.6 ∼2.5 2.3
Thoracic sucker diameter 2.0 1.9 – – 1.6
Ridge 0.6 0.6 – – 0.5
Abdominal segments 1–7 (average) ∼2.3 ∼2.2 ∼2.3 ∼2.2 ∼1.9
Prolegs 1–6 (average) ∼1.5 ∼1.5 ∼1.5 ∼1.5 ∼1.3
Seventh proleg 4.0 3.8 – – 3.0
First anal papilla 6.1 6.0 – ∼6 4.8
Second anal papilla 3.7 3.2 – – –
Terminal process 2.9 2.7 3.0 2.7 2.3
Open in a new tab

All measurements are in mm and lengths except where otherwise indicated.

∼: approximately; –: unknown.

Figure 1. Qiyia jurassica from the Middle Jurassic epoch of Daohugou, China.

Figure 1.

Open in a new tab

(A) Holotype STMN65-1. (B) Paratype STMN65-2 under alcohol (horizontal mirror image). (C) Head capsule of paratype STMN65-2. (D) Head and thorax of holotype STMN65-1. (E) Enlargement and reconstruction of the mandible of holotype STMN65-1; note the longitudinal groove. (F) Fifth proleg of holotype STMN65-1; note stiff, upward directed bristles which are distinctly longer than setae on body. (G) Last abdominal segment of holotype STMN65-1. ap, anal papilla; p, proleg; pr, process of ridge; tp, terminal process. (Scale bars: 5 mm in A, B, 1 mm in D, F, G, and 0.5 mm in C, E).

DOI: http://dx.doi.org/10.7554/eLife.02844.004

Figure 2. Qiyia jurassica from the Middle Jurassic epoch of Daohugou, China.

Figure 2.

Open in a new tab

(A) Paratype NIGP156982 under alcohol. (B) Head and thorax of paratype NIGP156982; note the underlying thoracic sucker. (C) Terminal processes of paratype NIGP156982. (D) Reconstruction of sucker. The sucker consists of a circular suction disc with central opening and thin peripheral area. Six robust, radially arranged ridges are covered by soft skin with small spines. (E) Head and thorax of paratype NIGP156984; note the deformed mandible. ap, anal papilla; p, proleg; pr, process of ridge; tp, terminal process; tr, tentorial rod. (Scale bars: 5 mm in A, 1 mm in B, C, E).

DOI: http://dx.doi.org/10.7554/eLife.02844.005

Discussion

Three specimens are laterally compressed (STMN65-1, STMN65-2, NIGP156984) and two are dorsoventrally compressed (NIGP156982, NIGP156983), thereby providing side and top views of the detailed morphology of the larva. Q. jurassica is attributed to the Tabanomorpha by the reduced and retractable head and sickle-shaped mandibles shifted into a vertical plane (Yeates, 2002; Zloty et al., 2005). It possesses two noticeably plesiomorphic features: mandibles with external grooves (Zloty et al., 2005) and well-developed anal papillae (Wichard et al., 1999), while sharing two potential synapomorphies with extant athericid larvae: paired prolegs with crochet hooks (Yeates, 2002; Kerr, 2010) and long terminal processes fringed with setae (Dobson, 2013). This combination of primitive and derived features demonstrates that Q. jurassica is a stem lineage representative of the Athericidae (water snipe flies), a family sister to the more familiar horse flies (Tabanidae). The earliest known Athericidae and Tabanidae (all represented by preserved adults) are from the Early Cretaceous of southern England (Mostovski et al., 2003). Our new fossils are the earliest record of athericid flies and extend the lineage back to the Middle Jurassic, an age which is consistent with predicted divergence times based on molecular studies (estimated at the Early or Middle Jurassic) (Wiegmann et al., 2011).

Q. jurassica displays adaptations to an aquatic habitat, much like extant Athericidae which are today aquatic predators in fast-flowing water (as adults some athericids feed on mammalian or amphibian blood) (Mostovski et al., 2003; Nagatomi and Stuckenberg, 2004). The paired sclerotized terminal processes are morphologically comparable to the modifications of beetle urogomphi in the aquatic larvae of some families such as Dytiscidae (Wichard et al., 1999). About 10 spiracles are present on each process of Q. jurassica (Figure 1G, Figure 2C), confirming that they were used for breathing air, functionally similar to the unsclerotized ones of extant athericid larvae (Nagatomi and Stuckenberg, 2004). Q. jurassica also possesses two pairs of anal papillae which are useful for extracting dissolved oxygen from water in aquatic flies and also play an important part in salt absorption to maintain ionic concentrations in the body fluids (Wichard et al., 1999). These organs are common in nematoceran larvae and in some lower brachyceran larvae, but are reduced in extant tabanomorphan larvae (Wichard et al., 1999; Dobson, 2013). In the case of the fossil larva, their development implies a plesiomorphic condition.

The most notable structure of these newly discovered fossils is the ridged thoracic sucker which is a unique evolutionary adaptation among holometabolous insects. The round sucker has six radial ridges which are considered to be highly modified thoracic legs (Figure 2D). These six robust, sclerotized ridges could increase both the suction area and surface friction, thus providing more adhesion and increasing lateral stability whilst reducing slippage, like the radial grooves in modern octopus suckers (Kier and Smith, 2002) and supporting ribs in man-made suction cups (Monkman et al., 2007). The dense vestiture of small spines may be used for better anchoring on the corrugated skin of a salamander, like the sucker-ring teeth and knobs on squid suckers (e.g., Miserez et al., 2009). To our knowledge, among insect larvae, only extant blepharicerids (Diptera) have six well-developed suckers, but these are small and without ridges on the abdominal sternites. As blepharicerid larvae graze on periphyton on rocks, they use the suckers to adhere to the substrate in fast-flowing streams (Frutiger, 2002). However, the excellent preservation of our new fossils suggests that Q. jurassica did not travel long distances and, unlike crown group Athericidae, most probably lived in still water near to or in the Daohugou palaeolake, a low-energy preservation environment (Wang et al., 2013). The thoracic sucker on Q. jurassica is strongly cephalad on the body so, when anchored to the substrate, it probably restricted the movement of the small, short head (Figure 1D, Figure 2E), a condition that is clearly suitable for piercing and sucking (Figure 3). Suckers are widespread in aquatic ectoparasites such as leeches, fish lice, and lampreys (Kearn, 2004) which require more suction power to avoid becoming dislodged; other aquatic ectoparasites without attachment organs embed themselves in skin or muscle, such as cyclopoid copepods (anchor worms) (Kearn, 2004). In addition to the sucker, the stiff, upward directed bristles and apical hooks on the prolegs (Figure 1F) are also specialized attachment structures. These morphological adaptations provide compelling evidence that Q. jurassica adhered to a host as an ectoparasite, providing further specialization for a dense, watery habitat.

Figure 3. Reconstruction of Qiyia jurassica in lateral view.

DOI: http://dx.doi.org/10.7554/eLife.02844.006

Figure 3.

Figure 3—figure supplement 1. Ecological restoration of Qiyia jurassica from the Middle Jurassic epoch of Daohugou, China.

Figure 3—figure supplement 1.

One larva is shown attached to the salamander. Larvae could be located on unexposed body zones, such as on the axil or behind the gill, where there are many blood vessels and the skin is thinner.
DOI: http://dx.doi.org/10.7554/eLife.02844.007
Open in a new tab

Bloodsucking is considered to have evolved independently at least 12 times in true flies (Lukashevich and Mostovski, 2003; Wiegmann et al., 2011). It started with free-living scavengers or predators which subsequently became opportunistic feeders on vertebrates, such as the notorious Congo floor maggot (Auchmeromyia) that consumes the blood of sleeping humans (Lehane, 2005). Bloodsuckers are present as adults in three families of extant Tabanomorpha (Nagatomi and Stuckenberg, 2004). Although hitherto known larval Tabanomorpha are mainly predators, some larvae suck the body fluids of vertebrates such as anurans (Jackman et al., 1983). Predatory fly larvae commonly have morphological and physiological adaptations (such as efficient protein-digesting enzymes and salivary glands), facilitating the switch to bloodsucking (Balashov, 1984; Lehane, 2005). Q. jurassica has a pair of sickle-shaped mandibles with external grooves (Figure 1E), which is a groundplan character of Tabanomorpha (Wichard et al., 1999; Yeates, 2002), forming a channel when the left and right mandibles are occluded (Zloty et al., 2005) and used for sucking blood or other body fluids (Marshall, 1981).

In the Daohugou deposits fish are completely absent but salamanders are extremely abundant (several thousand specimens recovered to date) (Liu et al., 2006). The most common salamanders at Daohugou, Chunerpeton tianyiensis and Jeholotriton paradoxus, have body lengths of 500 mm and 150 mm, respectively (Wang and Rose, 2005). Both species display neotenic features and are fully aquatic in all stages of their life cycle (Gao et al., 2013a). Salamander skin is glabrous and thin, and could easily have been penetrated by the mandibles of a larva such as Q. jurassica. The Daohugou salamanders match Q. jurassica well in size as well as co-occurrence, suggesting a possible parasite-host relationship. Some extant fly larvae parasitize anurans by burrowing into the skin, including Calliphoridae, Sarcophagidae, and Chloropidae (Hoskin and McCallum, 2007), and sometimes cause substantial mortality in their hosts (Bolek and Coggins, 2002). Q. jurassica, however, could simply have been anchored to the salamander skin using its sucker and prolegs (Figure 3—figure supplement 1), in a similar manner to leeches and fish lice (Kearn, 2004).

Despite a great taxonomic diversity of extant ectoparasitic insects (Marshall, 1981), previous definite Mesozoic records were confined to the terrestrial giant fleas from the Middle Jurassic and Early Cretaceous epochs (Gao et al., 2012, 2013b; Huang et al., 2012). Q. jurassica, which is arguably the earliest known aquatic ectoparasitic insect, reveals an unexpected morphological specialization of fly larvae and highlights the diversity of ectoparasitism in the Mesozoic.

Materials and methods

The specimens are housed in the Shandong Tianyu Museum of Nature (STMN), Pingyi, China, and Nanjing Institute of Geology and Palaeontology (NIGP), Chinese Academy of Sciences. Photographs were taken using a Zeiss Discovery V8 microscope system with specimens moistened in 95% alcohol or dry. The figures were prepared with CorelDraw X4 and Adobe Photoshop CS3.

Nomenclatural acts

The electronic edition of this article conforms to the requirements of the amended International Code of Zoological Nomenclature, and hence the new names contained herein are available under that Code from the electronic edition of this article. This published work and the nomenclatural acts it contains have been registered in ZooBank, the online registration system for the ICZN. The ZooBank LSIDs (Life Science Identifiers) can be resolved and the associated information viewed through any standard web browser by appending the LSID to the prefix ‘http://zoobank.org/’. The LSID for this publication is: urn:lsid:zoobank.org:pub: 99FE7164-CF29-4EAE-B7B2-40C727CAC4FA. The electronic edition of this work was published in a journal with an ISSN, and has been archived and is available from the following digital repositories: PubMed Central, CLOCKSS, Linyi University, Steinmann Institute at University of Bonn, and Nanjing Institute of Geology and Palaeontology (CAS). Printed copies are deposited in six major publicly accessible libraries including Linyi University, Nanjing Institute of Geology and Palaeontology (CAS), Steinmann Institute at University of Bonn, University of Kansas, Natural History Museum (London), and Muséum National d’Histoire Naturelle in Paris.

Acknowledgements

We are grateful to Xing Xu, Yuan Wang, Alexandr Rasnitsyn, and Junfeng Zhang for discussions on these specimens, Daran Zheng for his help in the preparation of specimens, Dinghua Yang for reconstructions, and André Nel and Enrique Peñalver for their constructive reviews.

Additional information

This research was supported by the National Basic Research Program of China (2012CB821900), National Natural Science Foundation of China (41272013, 41372014, J1210006), Natural Scientific Foundation of Shandong Province (ZR2013DQ017), CAS 2011T2Z04, and partially from US National Science Foundation grant DEB-0542909. BW was also supported by a Research Fellowship from the Alexander von Humboldt Foundation.

Funding Statement

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Funding Information

This paper was supported by the following grants:

  • Alexander von Humboldt Foundation CHN 1149090 STP to Bo Wang.

  • National Basic Research Program of China 2012CB821900 to Jun Chen, Bo Wang, Edmund A Jarzembowski, Haichun Zhang, Xiaoli Wang, Xiaoting Zheng.

  • National Natural Science Foundation of China (NSFC) FundRef identification ID: http://dx.doi.org/10.13039/501100001809 41272013, 41372014, J1210006 to Jun Chen, Bo Wang, Edmund A Jarzembowski, Haichun Zhang, Xiaoli Wang, Xiaoting Zheng.

  • Natural Scientific Foundation of Shandong Province ZR2013DQ017 to Jun Chen.

  • National Science Foundation (NSF) FundRef identification ID: http://dx.doi.org/10.13039/100000001 DEB-0542909 to Michael S Engel.

  • Chinese Academy of Sciences (CAS) FundRef identification ID: http://dx.doi.org/10.13039/501100002367 CAS 2011T2Z04 to Edmund A Jarzembowski.

Additional information

Competing interests

The authors declare that no competing interests exist.

Author contributions

JC, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article, Contributed unpublished essential data or reagents.

MSE, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article, Contributed unpublished essential data or reagents.

BW, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article, Contributed unpublished essential data or reagents.

TW, Analysis and interpretation of data, Drafting or revising the article.

EAJ, Analysis and interpretation of data, Drafting or revising the article.

HZ, Acquisition of data, Analysis and interpretation of data.

XW, Acquisition of data, Analysis and interpretation of data.

XZ, Acquisition of data, Analysis and interpretation of data.

JR, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article.

References

  1. Balashov Y. 1984. Interaction between blood-sucking arthropods and their hosts, and its influence on vector potential. Annual Review of Entomology 29:137–156. doi: 10.1146/annurev.en.29.010184.001033 [DOI] [PubMed] [Google Scholar]
  2. Bolek MG, Coggins JR. 2002. Observations on myiasis by the calliphorid, Bufolucilia silvarum, in the eastern American toad (Bufo americanus americanus) from southeastern Wisconsin. Journal of Wildlife Diseases 38:598–603. doi: 10.7589/0090-3558-38.3.598 [DOI] [PubMed] [Google Scholar]
  3. Dobson M. 2013. Family-level keys to freshwater fly (Diptera) larvae: a brief review and a key to European families avoiding use of mouthpart characters. Freshwater Reviews 6:1–32. doi: 10.1608/FRJ-6.1.450 [DOI] [Google Scholar]
  4. Frutiger A. 2002. The function of the suckers of larval net-winged midges (Diptera: Blephariceridae). Freshwater Biology 47:293–302. doi: 10.1046/j.1365-2427.2002.00814.x [DOI] [Google Scholar]
  5. Gao KQ, Chen JY, Jia J. 2013a. Taxonomic diversity, stratigraphic range, and exceptional preservation of Juro-Cretaceous salamanders from northern China. Canadian Journal of Earth Sciences 50:255–267. doi: 10.1139/e2012-039 [DOI] [Google Scholar]
  6. Gao TP, Shih C, Rasnitsyn AP, Xu X, Wang S, Ren D. 2013b. New transitional fleas from China highlighting diversity of Early Cretaceous ectoparasitic insects. Current Biology 23:1261–1266. doi: 10.1016/j.cub.2013.05.040 [DOI] [PubMed] [Google Scholar]
  7. Gao TP, Shih C, Xu X, Wang S, Ren D. 2012. Mid-Mesozoic flea-like ectoparasites of feathered or haired vertebrates. Current Biology 22:732–735. doi: 10.1016/j.cub.2012.03.012 [DOI] [PubMed] [Google Scholar]
  8. Grimaldi DA, Engel MS. 2005. Evolution of the insects. Cambridge: Cambridge University Press [Google Scholar]
  9. Hoskin CJ, McCallum H. 2007. Phylogeography of the parasitic fly Batrachomyia in the wet tropics of north-east Australia, and susceptibility of host frog lineages in a mosaic contact zone. Biological Journal of the Linnean Society 92:593–603. doi: 10.1111/j.1095-8312.2007.00862.x [DOI] [Google Scholar]
  10. Huang D, Engel MS, Cai C, Wu H, Nel A. 2012. Diverse transitional giant fleas from the Mesozoic era of China. Nature 483:201–204. doi: 10.1038/nature10839 [DOI] [PubMed] [Google Scholar]
  11. Huang D, Nel A, Cai C, Lin Q, Engel MS. 2013. Amphibious flies and paedomorphism in the Jurassic period. Nature 495:94–97. doi: 10.1038/nature11898 [DOI] [PubMed] [Google Scholar]
  12. Jackman R, Nowicki S, Aneshansley DJ, Eisner T. 1983. Predatory capture of toads by fly larvae. Science 222:515–516. doi: 10.1126/science.222.4623.515 [DOI] [PubMed] [Google Scholar]
  13. Kearn GC. 2004. Leeches, lice and lampreys. A natural history of skin and gill parasites of fishes. Dordrecht: Springer [Google Scholar]
  14. Kerr PH. 2010. Phylogeny and classification of Rhagionidae, with implications for Tabanomorpha (Diptera: Brachycera). Zootaxa 2592:1–133 [Google Scholar]
  15. Kier WM, Smith AM. 2002. The structure and adhesive mechanism of octopus suckers. Integrative and Comparative Biology 42:1146–1153. doi: 10.1093/icb/42.6.1146 [DOI] [PubMed] [Google Scholar]
  16. Labandeira CC. 2002. Paleobiology of predators, parasitoids, and parasites: death and accommodation in the fossil record of continental invertebrates. In: Kowalevski M, Kelley PH, editors. The fossil record of predation. Paleontological Society, Yale Printing Service; p. 211–249 [Google Scholar]
  17. Lehane MJ. 2005. The biology of blood-sucking in insects. New York: Cambridge University Press [Google Scholar]
  18. Liu YQ, Liu YX, Ji SA, Yang ZQ. 2006. U-Pb zircon age for the Daohugou Biota at Ningcheng of Inner Mongolia and comments on related issues. Chinese Science Bulletin 51:2634–2644. doi: 10.1007/s11434-006-2165-2 [DOI] [Google Scholar]
  19. Lukashevich ED, Mostovski MB. 2003. Hematophagous insects in the fossil record. Journal of Paleontology 37:153–161 [Google Scholar]
  20. Marshall AG. 1981. The ecology of ectoparasitic insects. London: Academic Press [Google Scholar]
  21. Miserez A, Weaver JC, Pedersen PB, Schneeberk T, Hanlon RT, Kisailus D, Birkedal H. 2009. Microstructural and biochemical characterization of the nanoporous sucker rings from Dosidicus gigas. Advanced Materials 21:401–406. doi: 10.1002/adma.200801197 [DOI] [Google Scholar]
  22. Monkman GJ, Hesse S, Steinmann R, Schunk H. 2007. Robot grippers. Weinheim: Wiley-VCH [Google Scholar]
  23. Mostovski MB, Jarzembowski EA, Coram RA. 2003. Horseflies and athericids (Diptera: Tabanidae, Athericidae) from the Lower Cretaceous of England and Transbaikalia. Journal of Paleontology 37:162–169 [Google Scholar]
  24. Nagatomi A, Stuckenberg BR. 2004. Insecta: Diptera, Athericidae. In: Yule CM, Sen YH, editors. Freshwater Invertebrates of the Malaysian Region. Kuala Lumpur, Malaysia: Academy of Sciences Malaysia; p. 791–797 [Google Scholar]
  25. Wang B, Zhang HC, Jarzembowski EA, Fang Y, Zheng DR. 2013. Taphonomic variability of fossil insects: a biostratinomic study of Palaeontinidae and Tettigarctidae (Insecta: Hemiptera) from the Jurassic Daohugou Lagerstätte. Palaios 28:233–242. doi: 10.2110/palo.2012.p12-045r [DOI] [Google Scholar]
  26. Wang Y, Rose C. 2005. Jeholotriton paradoxus (Amphibia: Caudata) from the Lower Cretaceous of south eastern Inner Mongolia, China. The Journal of Vertebrate Paleontology 25:523–532. doi: 10.1671/0272-4634(2005)025[0523:JPACFT]2.0.CO;2 [DOI] [Google Scholar]
  27. Wappler T, Smith VS, Dalgleish RC. 2004. Scratching an ancient itch: an Eocene bird louse fossil. Proceedings Biological Sciences/The Royal Society 271:s255–s258. doi: 10.1098/rsbl.2003.0158 [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wichard W, Arens W, Eisenbeis G. 1999. Atlas zur Biologie der Wasserinsekten. Berlin: Spektrum Akademischer Verlag [Google Scholar]
  29. Wiegmann BM, Trautwein MD, Winkler IS, Barr NB, Kin JW, Lambkin C, Bertone MA, Cassel BK, Bayless KM, Heimberg AM, Wheeler BM, Peterson KJ, Pape T, Sinclair BJ, Skevington JH, Blagoderov V, Caravas J, Kutty SN, Schmidt-Ott U, Kampmeier GE, Thompson FC, Grimaldi DA, Beckenbach AT, Courtney GW, Friedrich M, Meier R, Yeates DK. 2011. Episodic radiations in the fly tree of life. Proceedings of the National Academy of Sciences of the United States of America 108:5690–5695. doi: 10.1073/pnas.1012675108 [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Yeates DK. 2002. Relationships of extant lower Brachycera (Diptera): a quantitative synthesis of morphological characters. Zoologica Scripta 31:105–121. doi: 10.1046/j.0300-3256.2001.00077.x [DOI] [Google Scholar]
  31. Zloty J, Sinclair BJ, Pritchard G. 2005. Discovered in our backyard: a new genus and species of a new family from the Rocky Mountains of North America (Diptera, Tabanomorpha). Systematic Entomology 30:248–266. doi: 10.1111/j.1365-3113.2005.00270.x [DOI] [Google Scholar]
eLife. 2014 Jun 24;3:e02844. doi: 10.7554/eLife.02844.008

Decision letter

Editor: Detlef Weigel1

eLife posts the editorial decision letter and author response on a selection of the published articles (subject to the approval of the authors). An edited version of the letter sent to the authors after peer review is shown, indicating the substantive concerns or comments; minor concerns are not usually shown. Reviewers have the opportunity to discuss the decision before the letter is sent (see review process). Similarly, the author response typically shows only responses to the major concerns raised by the reviewers.

Thank you for sending your work entitled “Extreme adaptations for aquatic ectoparasitism in a Jurassic fly larva” for consideration at eLife. Your article has been favorably evaluated by Detlef Weigel (Senior editor) and 2 peer reviewers: André Nel and Enrique Peñalver.

The Senior editor and the reviewers discussed their comments before we reached this decision, and the Senior editor has assembled the following comments to help you prepare a revised submission:

This report of the earliest known aquatic ectoparasitic insect, from the Jurassic, is of great significance. The morphology and adaptations of these Jurassic larvae are fascinating. The specimens studied are impressive in their fine preservation, not leaving any doubt about their bizarre features. The paper is well written, the arguments are solid; the illustrations are nice and convincing. The detailed descriptions and their interpretations are completely convincing, despite all that seems very strange at first glance. It is a superb contribution to the knowledge of the paleobiology and evolution of the insects.

Minor comments:

1) Please indicate the family of these larvae. According to the main text “Our new fossils are the earliest record of athericid flies...” It appears that the adscription to this family is completely clear.

2) Maybe there is a more suitable word (currently teeth) to name the 6 strongly sclerotized structures on the ventral sucker...

3) The presence of a dense vestiture of small spines is in contradiction with a good functionality of a sucker due to difficulty to avoid the entrance of water (therefore, internal pressure loss), thus maybe for this reason the structure contains six “teeth” to improve the adherence.

4) Spiracles mentioned in the Discussion section are absent in the Description section.

5) The figure of the ecological restoration correctly reflects the authors' most plausible interpretation. One should to note that most probably these larvae could be located on salamander body zones that are not very exposed, since other salamanders could otherwise prey on them.

eLife. 2014 Jun 24;3:e02844. doi: 10.7554/eLife.02844.009

Author response

1) Please indicate the family of these larvae. According to the main text “Our new fossils are the earliest record of athericid flies...” It appears that the adscription to this family is completely clear.

Thanks. We have added it.

2) Maybe there is a more suitable word (currently teeth) to name the 6 strongly sclerotized structures on the ventral sucker...

Thanks. Done. We have changed “tooth” and “teeth” to “ridge” and “ridges” respectively.

3) The presence of a dense vestiture of small spines is in contradiction with a good functionality of a sucker due to difficulty to avoid the entrance of water (therefore, internal pressure loss), thus maybe for this reason the structure contains six “teeth” to improve the adherence.

We think a vestiture of small spines is not in contradiction with a good functionality of a sucker. These small spines may be used for better anchoring on a corrugated skin of a salamander, like the sucker-ring teeth and knobs on squid suckers, thus increasing the functionality of the sucker. We have added the following to the Discussion: “The dense vestiture of small spines may be used for better anchoring on a corrugated skin of a salamander, like the sucker-ring teeth and knobs on squid suckers (e.g., Miserez et al., 2009).”

4) Spiracles mentioned in the Discussion section are absent in the Description section.

Thanks a lot. We have added the description of spiracles: “each process with about ten spiracles.”

5) The figure of the ecological restoration correctly reflects the authors' most plausible interpretation. One should to note that most probably these larvae could be located on salamander body zones that are not very exposed, since other salamanders could otherwise prey on them.

We fully agree with the reviewers that these larvae could be located on unexposed body zones, such as on the axil or behind the gill, where there are many blood vessels and the skin is thinner. In the restoration, we put the larva on the area near the gills to help the reader see the larva and show the association between the larva and salamander. To clarify this, we have added the following to the figure legend: “Larvae could be located on unexposed body zones, such as on the axil or behind the gill, where there are many blood vessels and the skin is thinner.”

Articles from eLife are provided here courtesy of eLife Sciences Publications, Ltd

RESOURCES