Extreme adaptations for aquatic ectoparasitism in a Jurassic fly larva.

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.

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

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.

(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.

(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

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

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).

Figure 3—figure supplement 1.

Ecological restoration of Qiyia jurassica from the Middle Jurassic epoch of Daohugou, China.

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

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.

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.

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.”