Mesozoic larva in amber reveals the venom delivery system and the palaeobiology of an ancient lineage of venomous insects (Neuroptera)

doi:10.21203/rs.3.rs-4331518/v1

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Mesozoic larva in amber reveals the venom delivery system and the palaeobiology of an ancient lineage of venomous insects (Neuroptera)

https://doi.org/10.21203/rs.3.rs-4331518/v1

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published 24 Aug, 2024

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The larvae of Neuroptera are predators that feed by injecting bioactive compounds into their prey and then suctioning the fluids through modified mouthparts. We explore the evolutionary history of this feeding structure through the examination of a new fossil larva preserved in Late Cretaceous Kachin amber, which we describe as new genus and species, Electroxipheus veneficus gen et sp. nov. X-ray phase-contrast microtomography enabled us to study the anatomy of the larva in 3D, including the reconstruction of the structure of the mouthparts and of the venom delivery system. The specimen exhibited a unique combination of morphological traits not found in any known fossil or extant lacewing, including an unusual structure of the antenna. Phylogenetic analyses, incorporating a selection of living and fossil larval Neuroptera and enforcing maximum parsimony and Bayesian inference, identified the larva as belonging to the stem group Mantispoidea. The larva shows that the anatomy of the feeding and venom-delivery apparatus has remained unchanged in Neuroptera from the Cretaceous to the present. The morphology of the specimen suggest that it was an active predator, in contrast with the scarcely mobile, specialized relatives, like mantispids and berothids.

Biological sciences/Evolution

Biological sciences/Zoology

Cretaceous

Functional morphology

Holometabola

Neuropterida

Phylogeny

X-ray phase-contrast microtomography

During their long evolutionary history, insects evolved a diverse arsenal of biochemical weapons for both defence and attack. Envenomation systems independently appeared in different insect lineages, each exhibiting unique adaptations^1,2. Envenomation was evolved by a diverse array of predatory insects feeding on animal fluids through paralytic compounds, including Heteroptera, Diptera and in the larvae of Neuroptera and of some Coleoptera^2,3. Neuroptera, or lacewings, represent a relatively small (ca. 6000 described species) and ancient lineage of holometabolans dating back to the Permian^4,5. Lacewing larvae are predators exhibiting a moderate diversity of morphologies and life histories, ranging from predators of small arthropods to sponge feeders, passing through spider egg predators, and cryptic ambush hunters⁶. The predatory efficiency of lacewing larvae is also exploited in biocontrol, like in green lacewings (Chrysopidae). Despite their diversity and morphological disparity, all lacewing larvae share a piercing and sucking apparatus formed by the highly modified mouthparts, which also serves as venom-delivery system (the only exception being Sisyridae)^7,8. This piercing apparatus is composed of a ventrally grooved mandible that forms a suction channel by juxtaposition with the underlying dorsally grooved maxillary stylet. These two components maintain the function of the channel being held together by a seaming mechanism, consisting of a guide on the ventral side of the mandible and a prominent, apically folded, rail on the dorsal side of the maxillary stylet. The maxillary stylet is also provided with an internal lumen, or poison channel, which is ventrally coated at base with a layer of secretory cells, or maxillary gland^9–11. These glands are likely the source of bioactive peptides acting as paralyzing venoms once injected through the poison channel into the prey¹². Nevertheless, the chemical composition of the maxillary gland secretion, the transcription pathway, and the potential role of microbiota in venom production remain largely unknown².

Recent palaeontological progresses tremendously improved our knowledge of the past diversity of lacewings, especially at the larval stage, allowing to trace the evolution of anatomical and behavioral traits and their role in phylogenies. Late Cretaceous amber deposits document a phase of morphological experimentation among lacewings, improving our understanding of characters evolution and polarity during a period characterized by a peak in lacewing disparity^13–16. The amber from Myanmar (Late Cretaceous from Kachin state, 98 ± 0.6 Ma¹⁷) represents a Rosetta stone to decipher the evolutionary history of lacewings, preserving an exceptional array of lacewing larvae, often characterized by unusual morphologies^18–23. Here we describe a new larval morphotype from the Myanmar amber deposit. The overall morphology of this specimen resembles the living larvae of the Mantispoidea, i.e., the clade of Neuroptera including Berothidae, Rhachiberothidae and Mantispidae²⁴, albeit lacking their main synapomorphies, making its phylogenetic affinities ambiguous. We investigated the morphology of this fossil through synchrotron X-ray phase-contrast microtomography (XPCT), allowing us to reconstruct the finest details of its anatomy in 3Dand to unveil its phylogenetic affinities. XPCT is a nondestructive 3D imaging technique, resulting in a better image contrast and spatial resolution by detecting transparent or weakly absorbing samples, due to its sensitivity to phase shifts. So, this technique, increases the visibility of small structures undetectable in absorption mode²⁵.

XPCT is a cutting-edge technique for the study of fossil specimens, allowing to study anatomical features, such as bristles or wing details, of taxonomic importance but relatively small relative to the size of the whole organism²⁶.

Remarkably, our examination of the fossil larva revealed a largely intact mandibulo-maxillary stylet, preserving the venom-delivery system and suction channel of the specimen. The XPCT results allowed us to delve in the envenomation apparatus of a Mesozoic insect for the first time. Our findings suggest that i) functional features, such as the internal structure of the mouthparts, are highly conservative across the lacewing evolutionary history despite the high morphological disparity exhibited by fossils, and ii) stem group Mantispoidea were morphologically and ecologically diverse in the Mesozoic.

Systematic Palaeontology

Neuroptera Linnaeus, 1758

Mantispoidea Leach, 1815 (stem group)

Electroxipheus gen. n.

Zoobank [to be added]

Etymology. The genus name is masculine, and it is a composite word from Greek, with prefix “electro”, i.e. amber, and suffix “xipheus”, i.e. swordsman, hence “amber swordsman” after the sword shaped jaws of the larva.

Diagnosis. Larva campodeiform, elongate (Fig. 1). Head sclerotized, subrectangular. Mouthparts largely straight. Antenna thin, longer than stylets. Labial palp thin, as long as mouthparts. Head, thorax, and abdomen distinct. Thorax not sclerotized. Legs well developed, bearing trumpet-shaped empodia. Abdomen composed of ten segments.

Type species. Electroxipheus veneficus sp. n.

Electoxipheus veneficus sp. n.

(Fig. 1, 2, 3, 4, Supplementary Information Movie S1)

Zoobank [to be added]

Holotype. MZURPAL00112 (Museum of Zoology, Sapienza University of Rome). One specimen preserved in an amber piece.

Etymology. The specific epithet “veneficus” is a Latin masculine name meaning “poisoner”, after the well-preserved venom channel in the jaws.

Type locality and horizon. Northern Myanmar, Kachin Province, Hukawng Valley, c. 100 km west of the town of Myitkyina; Late Cretaceous (98 ± 0.6 Ma).

State of preservation. Specimen in good state of preservation, except for a fracture line crossing the cervical region and one prothoracic leg; thorax and anterior abdominal segments slightly damaged (Fig. 1).

Description. Measurements. Head length: 0.9 mm; head width: 0.8 mm; jaws length: 1.36 mm; body length: 5.76 mm.

Head capsule. Head capsule subquadrate, as long as wide, tapering toward cervical region. Head sub rectangular in lateral view and largely flattened dorsally (Supplementary Information Movie S1). Head dorsally sclerotized and ventrally mostly occupied by maxillary parts (Figs. 2A, 3). Anterior labial margin straight, without prominences (Fig. 3A, B, D). Frontal ecdysial suture distinct, encasing half of head anterior width; arms of frontal sutures converging at head mid-length, curved toward each other (Fig. 3A). Lateral and coronal ecdysial sutures absent. Antenna inserted laterally, on short tubercle, posterior to mandibular-maxillary stylet (Fig. 3A). Ocular region posterior to antenna insertion, marked with dark pigments, with six small stemmata arranged in an upper and a lower row, each of three stemmata (Fig. 3A, C). Long hair-like sensillum rising between stemmata.

Antenna. Antenna longer than mouthparts, with three main antennomeres. Second and third antennomeres with subsegments at apex (Fig. 2A, B, C). Basal antennomere cylindrical, three times longer than wide. Second antennomere long and thin, its diameter half that of first antennomere, cylindrical and over ten times longer than wide, with three subsegments, of which the first longer than remainders (Fig. 2B). Third antennomere cylindrical, thin, much longer than wide with a short, apical fusiform subsegment. Apical subsegment with a short apical sensillum (Fig. 2C). Antenna cuticle without ornamentations.

Mandibular-maxillary complex: suction and poison channels. Mandible and maxilla tightly associated, forming a single functional unit shaped like a straight, stylet-like sucking apparatus (Fig. 3). Blade-like section of mandibular-maxillary complex longer than head capsule, much wider at base, progressively narrowing toward apex. Apical section of mandibular- maxillary complex slightly curved outward and slightly bent downward in lateral view (Fig. 3A, B, C). Mandible narrower at base and much thinner than underlying maxilla, without teeth or serrations on internal margin. External margin of apex of mandible harpoon-shaped with a small inward tooth(Fig. 2D). Ventral surface of mandible concave, with a narrow groove running for almost its entire length, forming the roof of suction channel (Fig. 4). Suction channel externally delimited by a ridge, forming the protruding internal margin of a concave guide, in which fits the corresponding folded ridge on dorsal side of maxillary stylet (Fig. 4). Suction channel shifting dorsally in apical section of mandible, until it is almost by mandible surface (Fig. 4). Maxilla inserted ventrally, partly retracted, divided in basal elements, and maxillary stylet. Apical and basal maxillary elements distinct, subdivided by a median furrow (Fig. 3B). Apical maxillary element longer than basal one, separated by ventrolateral margin of dorsal sclerotization of head by furrow (Fig. 3C). Blade-like section of maxilla robust, wider at base. Maxillary stylet similar in shape to mandible, but thicker. Dorsal side of maxillary stylet grooved, corresponding to ventral floor of suction channel (Fig. 4). Lateral side of suction channel groove closed by an apically folded guiding ridge, fitting in corresponding groove of mandible and interlocking mandible and maxilla (Fig. 4). Maxillary stylet with poison channel, which is progressively more superficial toward tip and opens just before apex of maxilla (Fig. 4).

Labium. Labium composed by a distinct mentum and submentum. Mentum scute-like, subrectangular, with a pair of trichoid sensilla. Submentum trapezoidal, with a prominent median triangular process, and subdivided in a pair of diverging cylindrical palpomere-like elements (Fig. 2A, 3B). Labial palp thin, as long as mandibulo-maxillary stylet, composed of three palpomeres. Basal palpomere widest, cylindrical; second palpomere longest element of palp; third palpomere gently swelling apically (Fig. 2A). Third palpomere with a digitiform sensillum near apex (Fig. 2E).

Thorax. Cervical area collar-like, largely membranous. Thorax largely membranous (Fig. 1). Prothorax preserving traces of paired dorsal sclerotizations. Prothorax longer and narrower than meso- and metathorax.

Legs. Legs cursorial, of similar shape (Fig. 1). Prothoracic leg more robust than following pairs. Prothoracic leg with coxa cylindrical; trochantere as long as 1/3 of femur, with a ventral trichoid sensillum; femur cylindrical, robust, three times longer than wide; tibia short, ventral side of femur with three trichoid sensilla at 2/3 of length; tarsus short, conical; pretarsus with a short unguitractor-process with a pair of curved claws and a well-developed, elongated trumpet- shaped empodium (Fig. 2F).

Abdomen. Abdomen composed of ten segments (Fig. 1). Abdominal segments decreasing in size posteriorly but otherwise of similar shape and structure. Sternites and tergites without sclerotizations. Pleurae with a median protuberance with one apical thin seta. Tergites and sternites with few short and thin setae, progressively increasing in size posteriorly. 9th abdominal segment longer than wide. 10th abdominal segment conical, with traces of pygopodium (Fig. 2G).

Morphological remarks. Electroxipheus exhibits a combination of character states shared with Mantispoidea (i.e, Berothidae, Rhachiberothidae, Mantispidae): i) lack of lateral remnants of the frontoclypeal sulcus, ii) straight mandibulo-maxillary stylets, iii) presence of an unguitractor process on tarsus^27–29. Electroxipheus additionally exhibits a prominent median process on the prementum, a feature it shares with Berothidae. Coniopterygidae evolved a superficially similar labial process, although the broadly different anatomy of the labium in these clades suggests that they are not homologous. This structure is instead absent in Mantispidae³⁰. In Electroxipheus, the process of prementum is more prominent than in extant berothids and divides the prementum in two distinct cylindrical elements, widely diverging at base and resembling palpomeres in shape. Conversely, in extant berothids, the labial palps are in close contact and contiguous at the base³⁰. The condition observed in Electroxipheus resembles the organization of the prementum of the larvae of Myrmeleontiformia, in which the premental elements are widely separated and appears as palpomere-like^30,31. Despite the fossil larva shares with Mantispoidea most diagnostic characters, it lacks their apomorphies, i.e., the scale-like texture of the antennae and mouthparts, and the sensilla inserted in deep alveoli^29,30,32. Moreover, the head of Electroxipheus is wider than long, a marked difference from most mantispoids in which the head is much longer than wide at least in the first instar larva, except for Mantispidae Mantispinae. Electroxipheus also differs from Berothidae lacking the lateral sutures of head capsule. Most living mantispoid larvae are characterized by the reduction in the number of stemmata, which can be completely lost³³. However, Electroxipheus is equipped with six stemmata, as observed in other fossil mantispoid larvae and in the larva of the living Mucroberotha Tjeder^32,34,35. Electroxipheus also lacks a specialized terminal sensillum at the tip of the antenna, a character found in all mantispoids and several other clades of lacewings³⁰.

Phylogenetic analysis

The MP analysis under equal weights yielded 936 most-parsimonious trees (tree length = 368 steps; consistency index = 0.535; retention index = 0.854). The strict consensus cladogram is shown in Supplementary Information Fig. S1. When enforcing implied weights, the analyses generated different topologies according to the selected k-value of the default weighting function. The topology derived from the best-fitting k-value (k = 10.239) obtained by the “setk.run” algorithm was selected for discussing the relationships within Neuroptera and for reconstructing the affinities of the fossil larva and mapping the evolution of character states (Fig. 5, Supplementary Information Fig. S2). Under these conditions, the search yielded 2 most-parsimonious trees with a tree length of 370 steps and a total fit of 12.596.

The performed phylogenetic analyses differ in the reconstruction of the phylogenetic backbone of Neuroptera and in the resolution of some clades, although they were broadly consistent in recovering the affinities of Electroxipheus (Figs. 5, 6, Supplementary Information Figs S1, S2). The MP analysis under IW resulted in the best resolved phylogeny, while the reconstructions under both MP enforcing EW and under BI were largely unresolved. The monophyly of Neuroptera was strongly supported in all analyses (MP Bremer support: 6; BI Posterior Probability: 100). Under IW, Coniopterygidae emerged as the sister group to all remaining Neuroptera based on one unique synapomorphy (84:1, cervical sclerite and lateral abdominal tendon present). Instead, under both EW and BI, the relationships among lacewings clades were not resolved. The IW search found three main subclades encompassing all the remaining lacewings: clade A (Osmyloidea), clade B and clade F (Ithonidae + Myrmeleontiformia). Monophyletic Osmyloidea were supported by one unique synapomorphy (73:1, posterior tentorial pits not in contact with subgenal ridge, ventro-lateral to it) and included Nevrorthidae as sister to Osmylidae + Sisyridae. Osmyloidea were not recovered as monophyletic by both EW and BI, though both analyses recovered a poorly supported sister relationship between Osmylidae and Sisyridae (MP Bremer support: 1; BI posterior probability: 86). MP analyses under both weighting schemes recovered clade B (MP Bremer support: 1), which encompassed two clusters: clade C, comprising Hemerobiidae as sister to Chrysopoidea and clade D, including Dilaridae as sister to Mantispoidea. Clade C Monophyly of Chrysopoidea, including living Chrysopidae and Mesozoic Mesochrysopidae relied on one homoplasious synapomorphy (61:2) and obtained low supports (MP BS: 1), although both Chrysopidae (MP Bremer support: 1; BI posterior probabilities: 93) and Mesochrysopidae (MP Bremer support: 1; BI posterior probability: 79) were recovered as monophyletic. Monophyly of the clade IV (Dilaridae + Mantispoidea) was supported by two unique synapomorphies (31:1, lateral remnants of frontoclypeal sulcus absent; 31:1, mandibulo-maxillary stylets straight; 70:1, tentorial bridge reduced or absent) (MP Bremer support: 2; BI posterior probability: 96). Monophyly of Dilaridae relied on three unique (105:2, empodium stick-shaped; 107:1, pretarsal claws of prothoracic leg of different shape and size; 140:5, abdominal segment 10 with prominent paired cup-shaped adhesive pads) and three homoplasious synapomorphies and earned high supports (MP Bremer support: 4; BI posterior probability: 100). Mantispoidea, including Electroxipheus, were recovered as monophyletic based on one unique (104:1, unguitractor process present) and two homoplasious (20:2; 25:1) synapomorphies (MP Bremer support: 1; BI posterior probability: 96). Electroxipheus was consistently recovered as the sister group to all Mantispoidea in all analyses. The monophyly of the remaining Mantispoidea relied on one unique synapomorphy (3:1, head capsule > 1.5 times longer than wide). Under IW, the fossil specimen from Spanish amber MCNA9294 (Berothid_ Peñacerrada 1) was recovered as the sister group to all the remaining mantispoids, while monophyletic Mantispidae formed a dichotomy with a cluster (clade E) including Rhachiberothidae and living and fossil species of Berothidae. Instead, both EW and BI analyses found monophyletic Mantispidae emerging from a polytomy encompassing unresolved Berothidae and Rhachiberothidae. The monophyly of Mantispidae, which included Plega Navás (Symphrasinae) as sister to Mantispa Illiger (Mantispinae) and Ditaxis McLachlan (Drepanicinae), relied on two homoplasious apomorphies (25:0; 40:4; 51:1), with high supports (MP Bremer support: 4; BI posterior probability: 100). Under IW, Clade E was supported by one unique (79:1, lateral sutures of head capsule present) and comprised extant representatives of Rhachiberothidae (Mucroberotha) and Berothidae (Podallea Navás, Lomamyia Banks) and several fossil larvae assigned to the berothids from Cenozoic ambers (Berothid_Baltic_B, Berothid_Baltic_D, Berothoid_Rovno). Under IW, Ithonidae clusterized with Myrmeleontiformia based on two unique (22:0, antennomere 3 with short sensilli; 79:1, head-thorax articulation dorsal) and one homoplasious (61:2) synapomorphies. The monophyly of Ithonidae was supported also under EW and BI with high supports supports (MP Bremer support: 10; BI posterior probability: 100), despite a sister-group relationship to Myrmeleontiformia was not supported. Monophyly of Myrmeleontiformia, including living Myrmeleontoidea and their fossil relatives, was confirmed in all analyses (MP Bremer support: 1; BI posterior probability: 97).

Phylogenetic signal and fossil placement

Larvae of holometabolous insects have been a main source of information for classification and phylogenetic studies³⁶, especially for Neuropterida³⁷. Despite advances in genome- and transcriptome-based phylogenies, larvae remain crucial for understanding life histories, trait evolution tracing, and calibration points for divergence time estimation, as well as revealing ancient ecological networks. In this regard, Electroxipheus shed new light on the morphology of fossil Neuroptera, enabling to reconstruct the evolutionary history of mantispoid lacewings. The results of the current phylogenetic analysis under IW diverge from other morphology-based reconstructions by identifying Coniopterygidae as sister to all the other Neuroptera, Ithonidae as sister to Myrmeleontiformia and supporting the monophyly of Osmyloidea (Fig. 5). These clades are also supported in phylogenetic analyses based on mitogenomes and transcriptomes^38–41. However, the topology here retrieved was poorly resolved and the relationships obtained by enforcing IW were not corroborated under EW and BI (Fig. 6). Instead, in cladistic reconstructions, Nevrorthidae were recovered as sister to all Neuroptera, not supporting the monophyly of Osmyloidea, while both Coniopterygidae and Ithonidae were part of a diverse clade encompassing all lineages characterized by a “maxillary-head” configuration” (i.e., the Hemerobiiformia)^27,29,42,43. In agreement with previous cladistic reconstructions, the analyses recovered a sister group relationship between Hemerobiidae and Chrysopidae, and a clade encompassing Dilaridae and Mantispoidea, i.e., the “dilarid clade” ^{27,29,42–44}. However, molecular analyses consistently found Dilaridae as an isolated lineage and Hemerobiidae and Chrysopidae on different branches of the lacewing tree of life, though their phylogenetic affinities vary according to the dataset^38–41. The discrepancies between morphology-based and molecular-based phylogenies in reconstructing the affinities of these lineages, suggests that the morphological larval traits supporting these relationships are likely homoplasious. The Mesozoic Mesochrysopidae are confirmed as sister to living Chrysopidae, in agreement with the previous results¹⁴. Myrmeleontiformia emerge as a clade, in agreement with all phylogenetic studies^27,39,40,42 (Figs. 5, 6). The relationships between the lineages of Myrmeleontiformia and the placement of the fossil assigned to this clade agrees with the previous results of Badano et al. ^14,15. The monophyly of the lineages now included in Mantispoidea has long been recognized based on adult, larval and life-history characters and is supported in most phylogenetic analyses, although with major differences in morphology- and molecular based reconstructions^{24,29,39,42,45}. The present analyses consistently placed Electroxipheus as sister to all the other mantispoids, finding it as a stem-group unrelated to any living lineage, as also implied by its unusual combination of morphological traits. The performed analyses supported the monophyly of Mantispidae including Symphrasinae, while the monophyly of Berothidae was only supported under IW. In contrast, cladistic analyses based on adult characters and molecular-based phylogenies retrieved Symphrasinae as sister to either Rhachiberothidae or Berothidae^24,38,41. The analyses confirmed that the fossil mantispoids included in the dataset belong to Mantispoidea but they were not confidently placed in any clade within the family. The largely unresolved resolution within Mantispoidea is likely affected by the inadequate state of knowledge of their immatures because most of the larvae of this clade, except for Mantispinae, are still unknown. Our results suggest that our understanding of mantispoid larval diversity is still incomplete, hindering the reconstruction of the affinities of fossil larvae based on cladistic methods.

An unusual antenna

Drawing homologies between the segmentation of the antenna of the larvae of holometabolous insects and the main component of the antenna of the adult (i.e., scape, pedicel, flagellum) is notoriously challenging and the genetic pathway of the antenna subdivision is poorly understood⁴⁶. The larval groundplan of Neuroptera is characterized by an antenna with three main elements: a basal, an intermediate and an apical antennomeres (Fig. 7). The presence of intrinsic musculature in the basal and of a vestigial Johnston organ in the intermediate antennomere in the first instar larva of Dilar Rambur suggest that they are homologous to the scape and the pedicel, respectively⁴⁴. The antenna is distinctly three segmented in several lineages of lacewings, such as: Osmylidae, most Mantispoidea (Berothidae, Mantispidae), Hemerobiidae and Chrysopidae (Fig. 7)^27,29,30. Lacewing larvae with long antennae independently evolved adaptations to strengthen the second antennomere, which is usually the longest element. The larvae of Osmylidae are characterized by spiral sclerotization encircling and reinforcing the second element, while in Chrysopidae the second antennomere is annulated (Fig. 7) ³⁰. Instead, the antenna appears multisegmented in Nevrorthidae, Sisyridae, Dilaridae, Ithonidae and Myrmeleontiformia, because the second antennomere is followed by a series of short, often indistinct, irregular subsegments (Fig. 7)^{27,30,31,43,48}. In the larvae of Dilaridae, the first instar larva has a distinctly three segmented antenna, while later instars are characterized by a subdivision of the second antennomere in subsegments through ring-shaped desclerotizations^44,48,49. The segmentation pattern of the antenna of Dilaridae supports that the subsegments are not true antennomeres and are similar to the spirals and annulations of the antennae of Osmylidae and Chrysopidae. Conversely, the number of antennomeres is reduced in Coniopterygidae and Nemopteridae Nemopterinae (Fig. 7)^10,30,31. Amber-embedded lacewing larvae from the Mesozoic show that a similar diversity in antennal shapes and segmentation patterns also characterized stem-lineages^15,50. Electroxipheus differs from all the known larvae of Neuroptera in the segmentation of the antenna. In this specimen, the antenna consists of a robust basal antennomere (i.e, the scape), a long and thin second antennomere (i.e., the pedicel) followed by three short subsegments, and an apical antennomere with a short fusiform distal subsegment (Fig. 7). Therefore, the antenna of Electroxipheus differentiates from the three segmented antenna of most mantispoids. However, some poorly known fossil and living larvae of Rhachiberothidae and Berothidae are characterized by an apparently multisegmented antenna³⁵. Yet, none of these larvae exhibit the unique antennal structure of the Electroxipheus. Electroxipheus shares with other lacewing lineages with superficially multisegmented antenna (e.g., Sisyridae and Myrmeleontiformia) a long second antennomere, suggesting that the article-like subsegments originates from divisions of an ancestrally three segmented antenna.

Piercing, venom delivery and sucking system

The main apomorphy of Neuroptera is represented by the transformation of the larval mouthparts in a complex suction apparatus⁵¹. The present fossil larva offers unique insights into the functional morphology of the envenomation and sucking system of a Mesozoic stem-lineage of lacewings. The shape of the mouthparts of Electroxipheus closely resembles the structure of piercing straight stylets characterizing the larvae of Dilaridae and Mantispoidea (except for the curved-jawed larvae of Symphrasinae)^28,30. However, Electroxipheus stands apart from the latter families because the mouthparts are proportionally longer and slightly curved outward and bent downward, while in most extant Mantispoidea the stylets are usually short and straight^29,30. The maxillary stylet of Electroxipheus is thicker than the mandible, like all Neuroptera except for Myrmeleontiformia. The interlocking system between the mandible and the maxilla is well preserved and is similar to living species, consisting of a ventral guide on mandible and a corresponding rail on dorsal side of maxillary stylet (Fig. 4)⁵². In the apical-most section of the mouthparts, the suction channel of the fossil larva narrows and shifts dorsally, until it is almost completely encased by the mandible. A similar condition is present in the larvae of Osmylus Latreille near the channel opening at the mandible apex⁴⁷. The poison channel is also distinct, running for the entire length of the maxillary stylet. In the apical section of the stylet, the poison channel migrates dorsally but remains separated from the suction channel by the walls of the maxillary stylet (Fig. 4). The mouthpart structure of Electroxipheus is largely congruent with that of living species, suggesting that the anatomy of the sucking and venom delivery system is strongly conservative across Neuroptera for their whole evolutionary history.

Palaeobiology

Among Neuroptera, the life histories of Mantispoidea are arguably the most remarkable, showing unusual morphologies, bizarre developmental strategies, and peculiar specializations to highly specific prey. However, at the same time, their larvae are probably the less known among lacewings and life history and morphological data are available for a handful of species, except for Mantispidae Mantispinae³⁴. All the known Mantispoidea are characterized by physogastric later larval instars, a feature also documented in Burmese amber²³. All the living genera of Berothidae with known later larval instars (i.e., Isoscelipteron Costa, Lomamyia and Podallea) have termitophilous larvae living in termite nests, of which the second and the third instars are physogastric. The second instar is also immobile and does not feed ^34,53. Mantispidae Mantispinae and Symphrasinae exhibit more drastic ontogenetic changes between instars than berothids and the development is hypermetamorphic, with deep changes in the anatomy of the head and of the appendages^7,30. The larvae of Mantispidae Mantispinae feeds on spider eggs within the egg sacs and according to the species can directly penetrate the egg sac or to board the spider waiting for the sac production to enter in it^54,55. Instead, Symphrasinae (i.e., Anchieta Navás and Plega) feed on pupae of holometabolans and most species were obtained from nest of eusocial hymenopterans²⁸. However, the lack of data on the life history of most species of Berothidae, Rhachiberothidae and the other subfamilies of Mantispidae, impairs our understanding of the development strategies and larval diversity of the clade. Larvae of Mantispoidea are known in both Mesozoic and Cenozoic ambers and appear particularly well represented in Burmese amber^{21,34,35,56,57}. The inclusion of Electroxipheus in a phylogenetic context, coupled with high resolution XPCT imaging, allows us to place this specimen in the mantispoid phylogenetic tree and trace the evolution of life history and morphological traits across the lineage. The stem-group position of Electroxipheus offers valuable insights into the development of the unusual life strategies of Mantispoidea. Despite the challenge in ascertaining the instar of Electroxipheus, its body proportions suggest that it likely belongs to a non-physogastric second or third instar. The presence of short head capsule, long and thin antenna, long mandibulo-maxillary stylet and strongly developed basal maxillary elements indicate that Electroxipheus was an active predator. A predatory lifestyle is also suggested by comparisons with the larvae of unrelated lacewing lineages of active predators, such as Osmylidae, Chrysopidae and Hemerobiidae, to which it resembles in body proportions. The larva exhibits a remarkable convergence with the larvae of Osmylidae, both sharing elongated and curved outward mandibulo-maxillary stylets, although this feature is less prominent in Electroxipheus than in osmylids. Despite Electroxipheus shared its palaeoenvironment with a remarkable diversity of mantispoid larvae²¹, its phylogenetic position and functional morphology suggest it belongs to a lineage that diverged from other mantispoids before the evolution of the physogastric development strategy.

Data Matrix

The dataset of morphological trait was compiled by implementing and updating the matrix originally developed by Badano et al.^15,31 using Mesquite v.3.61 software⁵⁸. The updated dataset comprises 63 taxa, including four extinct taxa from Mesozoic and Cenozoic amber deposits, as well as two extant ones (Table 1). The final version of the dataset included 63 taxa and 142 characters, consisting of 109 binary and 33 multistate (Supplementary Information File S1). The morphological details of fossil taxa were obtained from literature (Table 1), while direct observations were used for the new larva.

Table 1

Fossil larvae of Mantispoidea included in the phylogenetic analysis.
Original specimen code or name	Type locality and age	Occurence	Classification	Reference	Name used in present dataset
MCNA9294	Peñacerrada 1, Basque-Cantabrian Basin	Cretaceous, late Albian: Spain	Berothidae	Pérez-de la Fuente et al.⁶¹	Berothid_ Peñacerrada 1
Berothid indet., larva B	Baltic amber	Eocene	Berothidae	Wedmann et al.³⁴	Berothid_Baltic_B
Berothid indet., larva D	Baltic amber	Eocene	Berothidae	Wedmann et al.³⁴	Berothid_Baltic_D
Berothoid	Rovno amber, Klesov deposit, Sarny district, Rovno Region, Ukraine	Late Eocene	Mantispoidea indet	Makarkin et al.³⁵	Berothoid_Rovno

Phylogenetic Analyses

Maximum parsimony (MP) analyses of the dataset were performed using the TNT v1.5 software⁵⁹ under both equal (EW) and implied (IW) weights. Heuristic tree explorations were conducted by setting the “traditional search option” under the following configurations: general RAM of 1000 Mbytes, memory se to hold 1 000 000 trees, 1000 replicates with tree bisection-reconnection (TBR) branch swapping and keeping 1000 trees per replicate. Under IW, the dataset was analyzed enforcing a wide spectrum of concavity k-values of the weighting function, from k = 3 to k = 20, while the most suitable one was found through the TNT script “setk.run”⁶⁰. Multistate characters were considered as unordered and zero-length branches were collapsed. Bremer support values under EW were computed in TNT from 10 000 trees up to ten steps longer than the shortest trees obtained under the “traditional search”, using the “trees from RAM” setting. Character state changes were plotted with WinClada v.1.00.08⁶¹. Consistency (CI) and retention (RI) indexes for matrix were calculated with Mesquite v.3.61 software. Ancestral State Reconstruction for character changes were perfomed with Mesquite v.3.61, with the likelihood ancestral state.

Bayesian Inference (BI) anayses were run in MrBayes v.3.2.7 on the Extreme Science and Engineering Discovery Environment at Cyberinfrastructure for Phylogenetic Research⁶². The analyses were performed under the Mk1 model⁶³ with scoring set for variable morphological characters. Four Markov chain Monte Carlo (MCMC) chains, of which one cold and three heated, were run for 10⁶ generations, setting a burn-in fraction of 50% and sampling the chains every 1000 generations. The convergence of independent runs was assessed through the average standard deviation of split frequencies (< 0.01) and potential scale reduction factors (approaching 1). Ancestral state reconstructions for characters ‘Antennomere 2 segmentation’ (17) was carried out in Mesquite 3.61⁵⁸ using maximum likelihood and plotted on the strict consensus IW tree.

Optical examination

Specimens were examined, photographed, and measured with a Zeiss Axio Zoom v.16 stereoscope.

XPCT measurements

The experiments were carried out at the TOMCAT beamline of the Swiss Light Source (Villigen, Switzerland). The incident monochromatic X-ray energy was of 20 keV. A PCO edge 5.5 camera coupled with optics resulting in a pixel size of 1.625 × 1.625 µm² and 0.32 × 0.32 µm² was set at a distance from the sample of 3 (exposure time = 90 ms) and 5 cm (exposure time = 220 ms), respectively. The tomographic images were acquired using the so-called half-acquisition mode, which allows to almost double the image field of view.

Data pre-processing, phase retrieval, and reconstruction (by using Filtered Back Projection (FBP) method) were performed on site using by means of ad hoc software based on the Paganin's phase retrieval algorithm. Image processing and 3D rendering were made with the software ImageJ (https://imagej.net/Fiji) and VG studioMax. The different electron densities of the tissues were rendered as grey levels in the phase tomograms images. For the 3D rendering, binarization was further applied over the reconstructed data.

Acknowledgments

The authors acknowledge the support of NBFC, funded by the Italian Ministry of University and Research, PNRR, Missione 4 Componente 2, “Dalla ricerca all’impresa”, Investimento 1.4, Project CN00000033. We thank the Willi Hennig Society for making the TNT software available. Special thanks to Roberto A. Pantaleoni (IRET CNR SS, Italy) for sharing and letting us use the photo of coniopterygid antenna. We acknowledge the Paul Scherrer Institut, Villigen, Switzerland, for provision of synchrotron radiation beamtime at the TOMCAT beamline X02DA of the Swiss Light Source and would like to thank Margie Olbinado and the whole staff of the beamline for assistance. Special thanks to Daniel Whitmore (Naturkunde Museum Stuttgart, Germany) for the critical revision and the English check of the manuscript.

Author information

Authors and Affiliations

Department of Life Science, University of Siena, Siena, Italy

Davide Badano

NBFC, National Biodiversity Future Center, Palermo, Italy

Davide Badano, Pierfilippo Cerretti

CNR-Nanotec (Rome Unit) c/o Department of Physics, Sapienza University of Rome, Rome, Italy

Michela Fratini, Laura Maugeri, Francesca Palermo, Nicola Pieroni

Department of Biology and Biotechnologies “Charles Darwin”, Sapienza University of Rome, Rome, Italy; Museum of Zoology, Sapienza University of Rome, Rome, Italy

Pierfilippo Cerretti

Contributions

Conceived and designed the experiments: D.B., P.C. Studied and described the material: D.B. Performed the experiment using XPCT and designed digital reconstructions and animations: M.F., L.M., F.P., N.P. Analyzed the data: D.B., P.C. Wrote the paper: D.B., M.F., P.C. All authors edited and checked the manuscript.

Corresponding author

Correspondence to Davide Badano

Data availability statement

The data that supports the findings of this study are available in the supporting information of this article.

Additional information

Competing interests

The authors declare no competing interests.

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No competing interests reported.

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Mesozoic larva in amber reveals the venom delivery system and the palaeobiology of an ancient lineage of venomous insects (Neuroptera)

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Abstract

Introduction

Results

Systematic Palaeontology

Zoobank [to be added]

Zoobank [to be added]

Phylogenetic analysis

Discussion

Phylogenetic signal and fossil placement

An unusual antenna

Piercing, venom delivery and sucking system

Palaeobiology

Materials and methods

Data Matrix

Phylogenetic Analyses

Optical examination

XPCT measurements

Declarations

References

Additional Declarations

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