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Convergent evolution of ramified antennae in insect lineages from the Early Cretaceous of Northeastern China

Taiping Gao

Taiping Gao

College of Life Sciences, Capital Normal University, 105 Xisanhuanbeilu, Haidian District, Beijing 100048, People's Republic of China

[email protected]

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Chungkun Shih

Chungkun Shih

College of Life Sciences, Capital Normal University, 105 Xisanhuanbeilu, Haidian District, Beijing 100048, People's Republic of China

Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012, USA

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Conrad C. Labandeira

Conrad C. Labandeira

College of Life Sciences, Capital Normal University, 105 Xisanhuanbeilu, Haidian District, Beijing 100048, People's Republic of China

Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012, USA

Department of Entomology and BEES Program, University of Maryland, College Park, MD 20742, USA

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Jorge A. Santiago-Blay

Jorge A. Santiago-Blay

Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012, USA

Department of Crop and Agroenvironmental Sciences, University of Puerto Rico, Mayagüez, PR 00681, USA

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Yunzhi Yao

Yunzhi Yao

College of Life Sciences, Capital Normal University, 105 Xisanhuanbeilu, Haidian District, Beijing 100048, People's Republic of China

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Dong Ren

Dong Ren

College of Life Sciences, Capital Normal University, 105 Xisanhuanbeilu, Haidian District, Beijing 100048, People's Republic of China

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Published:https://doi.org/10.1098/rspb.2016.1448

    Abstract

    Antennae are important, insect sensory organs that are used principally for communication with other insects and the detection of environmental cues. Some insects independently evolved ramified (branched) antennae, which house several types of sensilla for motion detection, sensing olfactory and chemical cues, and determining humidity and temperature levels. Though ramified antennae are common in living insects, occasionally they are present in the Mesozoic fossil record. Here, we present the first caddisflies with ramified antennae, the earliest known fossil sawfly, and a scorpionfly also with ramified antennae from the mid-Lower Cretaceous Yixian Formation of Northeastern China, dated at 125 million years ago (Ma). These three insect taxa with ramified antennae consist of three unrelated lineages and provide evidence for broad structural convergence that historically has been best demonstrated by features such as convergent mouthparts. In addition, ramified antennae in these Mid-Mesozoic lineages likely do not constitute a key innovation, as they are not associated with significantly increased diversification compared with closely related lineages lacking this trait, and nor are they ecologically isolated from numerous, co-occurring insect species with unmodified antennae.

    1. Introduction

    Antennae are important sensory organs for insects to communicate with other insects, detection of environmental cues [1], and are principally involved in activities such as locating potential mates [24], securing food, and targeting biological hosts [5]. Various types of antennal sensilla are located on individual antennal units, or flagellomeres, that collectively constitute the conspicuous part of the insect's antennae, the flagellum, and serve as chemoreceptors, mechanoreceptors, thermoreceptors, or hygroreceptors [68]. However, the principal sensilla on the antennal flagellomeres of most insects are involved in olfaction [5,9]. Some insects have evolved broadly ramified antennae, ranging from forms that are pectinate (a single row of comb-like rami, or branches, along the flagellum) or bipectinate (two rows of comb-like rami along the flagellum), and these each can be plumose (feathery) or flabellate (fan-shaped) [10]. The consequence of such intricate morphology is an overall expansion in the antennal surface area associated with an increase in the number of sensilla. Among extant insects, ramified antennae are present in a great variety of clades [1113].

    Recently, we recovered three new fossil species representing three orders of insects—Trichoptera (caddisflies), Mecoptera (scorpionflies), and Hymenoptera (sawflies, wasps, ants, bees)—each of which possesses comb-like ramified antennae deployed as pectinate, flabellate, and plumose variants. A new taxon is established for three specimens of the caddisflies (Trichoptera, uncertain family-level relationships) that display several distinctive characters of venation and bipectinate antennae with two rows of comb-like rami along the flagellum. A second new taxon is a long-proboscid scorpionfly (Mecoptera, Mesopsychidae) that represents a new species possessing pectinate antennae, with a single row of comb-like rami along the flagellum. The third new taxon is a new species of a previously described genus of sawfly (Hymenoptera, Megalodontesidae) that bears plumose (feathery) antennae, a group known for their serrate or pectinate antennae in the modern fauna. These three species originate from the mid-Lower Cretaceous Yixian Formation [14], of the uppermost Barremian to lowermost Aptian stages, pegged to a date of 125 Ma [15], and are the earliest records of insects with ramified antennae for their broader respective clades. They predate by about 10 Myr the biflabellate antennae borne by Atefia rasnitsyni Krogmann, Engel, Bechly and Nel, 2012, a compression fossil from the Lower Cretaceous Crato Formation, assigned to the upper Aptian Stage at 115 Ma [16]. The occurrence of biflabellate antennae in A. rasnitsyni was suggested to indicate the antiquity of insect usage of long-range female attractants [16].

    All extant scorpionflies and caddisflies have filiform and often setose antennae, except for Ramiheithrus virgatus Neboiss, 1974 (Trichoptera, Philorheithridae), which has pectinate rami on its basal 10–15 flagellomeres, although rami are lacking in the distal portion of the flagellum [17]. Most modern sawflies, with the exception of various species in the families Pergidae, Megalodontesidae, Tenthredinidae, and Diprionidae [18], lack branched antennae. The structurally convergent, elaborate antennal morphologies present in these three, Lower Cretaceous insect orders provide new data and insights into the antiquity and structural convergence of these distinctive antennae.

    2. Material and methods

    All type specimens are housed in the Key Laboratory of Insect Evolution and Environmental Changes at Capital Normal University, Beijing, China (CNUB; Dong Ren, curator). A Leica M165 C dissecting microscope was used for visual observation of the specimens, which were illustrated with the aid of a drawing tube. The specimens were photographed by dry or under surface wetting of 95% ethanol, under a dissecting microscope with an attached Leica DFC500 digital camera. Scanning electron microphotography (SEM) was carried out using an ESEM (Environmental Scanning Electron Microscope) (Quanta200F, FEI) in the Beijing Museum of Natural History. Line drawings were prepared using CorelDraw 12 graphic software and Adobe Photoshop Creative Suite.

    For Trichoptera, the terminology for wing venation follows that outlined by Holzenthal et al. [19]. For Mecoptera, the terminology of Novokshonov was used, as applied to the Mesopsychidae [20], updated by Rasnitsyn & Quicke [21]. For Hymenoptera, the system of Huber & Sharkey [22] was followed, particularly for terminology involving symphytan grade taxa.

    3. Results

    Systematic Paleontology

    Insecta Linnaeus, 1758

    (a) Trichoptera Kirby, 1815

    Integripalpia Martynov, 1924

    Family Incertae sedis

    Cathayamodus fournieri gen. et sp. nov. (figure 1 and electronic supplementary material, figure S1).

    Figure 1.

    Figure 1. The holotype male (CNU-TRI-LB-2009001p/c) representing Cathayamodus fournieri gen. et sp. nov. from the mid Early Cretaceous of Northeastern China (see also the electronic supplementary material, figure S1). (a) Photograph of the part under alcohol. (b) Photograph of the counterpart without alcohol. (c) Line drawing of (b). (d) Basal part of the antennae showing trichoid sensilla and trichobothria under alcohol. (e) The central region of the ramified antenna, showing rami. (f) The apical portion of the antenna showing sensilla on nine rami. (g,h) Scanning electron microscope (SEM) images of flagellomere rami with trichoid sensilla and trichobothria. (i) Reconstruction of C. fournieri (by Ms Chen Wang). Scale bars: (ac), 5 mm; (df), 0.5 mm; (g,h), 0.1 mm.

    Etymology. The generic name of Cathayamodus is a combination of Cathay, an ancient name for China that was anglicized from the original Chinese, Khitān, and modus, from the Latin, meaning, ‘measure’, ‘size’, or ‘standard of measurement.’ This refers to the regularly spaced distances between the antennal rami on the antennal flagellum. The specific epithet, ‘fournieri’, is in honour of Mr Dominique Fournier, for his guidance, motivation, and encouragement to CKS in his earlier palaeoentomological endeavours. The gender of the name is masculine.

    Holotype. CNU-TRI-LB-2009001p/c, part and counterpart, sex unknown (figure 1 and electronic supplementary material, figure S1c and g).

    Paratype. A well-preserved specimen with maxillary palpi, wings, and a portion of the legs and antennae; CNU-TRI-LB-2011001p/c, part and counterpart; sex unknown (electronic supplementary material, figure S1ac).

    Horizon and locality. Collected from the mid-Lower Cretaceous Yixian Formation, dated as latest Barremian to earliest Aptian, 125 Ma [15], at Huangbanjigou, near Chaomidian Village, in Shangyuan County, adjacent to Beipiao City, in Liaoning Province of China.

    Diagnosis for genus and species. Adult moderately large, entire body covered with dense setae; setal warts present on head and thorax (figure 1a–c). Antennal length slightly shorter than or equal to forewing length; scape stout; flagellum bipectinate, bearing lateral rami on each side (figure 1dh). Wings elongate; discoidal cell and median cell closed in forewings. Apices of F1 and F2 located between one-third and one-fourth of wing length to the wing apex; apices of F3 and F4 cells about one-fourth of wing length to the wing apex. Cu1a forking at the level of F3. Crossveins absent in hind wings.

    Description, dimensions, and material. See the electronic supplementary material.

    (b) Mecoptera Packard, 1886

    Mesopsychidae Tillyard, 1917

    Vitimopsyche Novokshonov & Sukatsheva, 2001

    Type species. Vitimopsyche torta Novokshonov and Sukatsheva 2001

    Other included species. V. kozlovi Ren, Labandeira, and Shih, 2010, V. pristina Lin, Shih, Labandeira, and Ren, 2016, and V. pectinella sp. nov.

    Emended diagnosis. Antennae pectinate; hind wing MP originating from stem of MP + CuA before or after Rs + MA origin from R1 (figure 2b).

    Figure 2.

    Figure 2. Holotype of Vitimopsyche pectinella sp. nov. (part, CNU-MEC-LB-2012088p) from the mid Early Cretaceous of Northeastern China (see also the electronic supplementary material, figure S2). (a,b) Photograph and line drawing of the entire specimen. (c) Photograph of the head, antennae, and mouthparts. (d) Left antenna. (e) Enlargement of the central region of (d). (f) Details of the elongate mouthparts. Scale bars: (a,b), 5 mm; (c,d), 2 mm; (e,f), 1 mm.

    Vitimopsyche pectinella sp. nov. (figure 2 and electronic supplementary material, figure S2).

    Etymology. The specific epithet is taken from the diminutive of the Latin word ‘pectin’, meaning ‘little comb’.

    Holotype. CNU-MEC-LB-2012088p/c, part and counterpart, sex unknown (figure 2 and electronic supplementary material, figure S2).

    Horizon and locality. Same as those of Cathayamodus fournieri.

    Diagnosis. Forewing Sc with one anterior branch; Rs forking distally, terminating in two, short branches; crossvein mp4-cua present. Hind wing with Sc long, reaching anterior wing margin distad MP bifurcation into MP1+2 and MP3+4; Rs with two short branches; MP originating from MP + CuA stem distad origin of Rs + MA from R1.

    Description, dimensions, and material. See the electronic supplementary material.

    (c) Hymenoptera Linnaeus, 1758

    Pamphilioidea Cameron, 1890

    Megalodontesidae Konow, 1897

    Jibaissodes Ren, 1995

    Type species. Jibaissodes giganteus Ren, 1995

    Other included species. J. bellus sp. nov.

    Jibaissodes bellus sp. nov. (figure 3 and electronic supplementary material, figure S3).

    Figure 3.

    Figure 3. Holotype of Jibaissodes bellus gen. et sp. nov. (part, CNU-HYM-LB-2011009p) from the mid Early Cretaceous of Northeastern China (see also the electronic supplementary material, figure S3). (a,b) Photograph and line drawing of entire specimen. (c) Right antenna. (d) Apical portion of the counterpart antenna; arrows show flagellar articulations, from each of which arises a plumose (penniform) annular ramus extended from the apex of each flagellomere. (e) Basal region of antenna (part). (f) Antenna under SEM imaging. (g) Right forewing with important veins labelled. Scale bars: (a,b), 2 mm; (cg), 0.4 mm.

    Etymology. The specific epithet ‘bellus’ is from Latin, meaning ‘beautiful’.

    Holotype. Male; CNU-HYM-LB-2011009p/c, part and counterpart (figure 3 and electronic supplementary material, figure S3).

    Horizon and locality. Same as those of Cathayamodus fournieri.

    Diagnosis. Antenna plumose (feathery rather than serrate), with more than 30 flagellomeres, flagellum slightly longer than width of head; flagellomeres with plumose apical rami. Metanotal cenchri comparatively narrow and small. Forewing with costal cell apically widened, broader than pterostigmal base at origin of Rs; first abscissa of M (M1) and that of Rs (Rs1) forming a nearly straight line; basal vein confluent with 1cu-a; M + Cu straight with first free abscissa of Cu (Cu1); marginal cell apex broadly rounded, reaching nearly to wing apex (rather than blunt, attributable to strong arching of apical Rs towards anterior wing margin). Abdominal terga without lateral creases (figure 3g).

    Description, dimensions, and material. See the electronic supplementary material.

    4. Discussion and conclusion

    (a) The selection process involving ramified antennae

    Antennae function as a complex arrangement of multiple types of receptors in three-dimensional space [23,24] and collectively serve as the primary olfactory and sensory organ of an insect [25]. Ramified antennae occur in a variety of extant insect species and are represented sporadically across many holometabolous insect lineages such as Coleoptera (beetles) [26,27], Diptera (true flies) [28], Megaloptera (dobsonflies) [29], Lepidoptera (moths and butterflies) [30], and in the Trichoptera, Mecoptera, and Hymenoptera that also occur in the mid Early Cretaceous of Northeastern China [11]. Each antennal type houses thousands to tens of thousands of mechanoreceptors and chemoreceptors that constitute the four basic types of insect sensilla: the relatively large trichoid sensillum for sensing motion, the basiconic sensillum for apprehending olfactory inputs such as smell, the coeloconic sensillum for detecting odorants and other volatilized chemicals, and the relatively rare placoid sensillum that also recognizes odorants [3,24,25]. In addition, exceptionally large trichoid sensilla, the trichobothria, often occur as prominent spinose bristles that can detect ambient air movement and surface contact [11].

    Occasionally, sensilla can be recognized in the fossil record such as those on well-preserved antennae in amber [31], but are rarely discernible in most compression fossils [32]. This indetectability results from silt-sized or coarser particles of matrix that are larger than the observed structures, thus obscuring resolution of microstructural details of individual sensilla [31]. Based on the preserved antennae of the five specimens examined, several types of sensory structures were identified: (i), rigid, spinose bristles, perhaps basiconic sensilla, frequently present on the basal and distal regions of the antennae in Cathayamodus fournieri (figure 1df), (ii), trichoid sensilla on the flagellomeres of Jibaissodes bellus (figure 3cf), and (iii) long, pilose, and non-tapering trichobothria present on almost all antennal regions of the three taxa (figures 1gh, 2de and 3f). Although chemoreceptive sensilla were not discernible (but see above), we infer that many non-trichoid sensilla were used in a chemosensory role to facilitate detection of targeted airborne molecules, such as conspecific sex pheromones or volatile secondary compounds indicating the presence of a food resource [11,24].

    Given the biological functions of ramified antennae in modern relatives of these mid Early Cretaceous insects, increased antennal surface area and increased sensory capacity likely was maintained in populations through differential selection, a phenomenon observed in modern insects [33,34]. The ramified antennae of Cathayamodus are rare among caddisflies. Modern caddisflies tend to emerge in large numbers from aquatic habitats, such that prospective mates are largely within close proximity [35,36]. Accordingly, the appearance of specialized, sensilla-rich, ramified antennae would result in a minimal selective advantage necessary for mate searching [12,37]. The ramified antennae of Vitimopsyche pectinella, for example, do not occur in extant Mecoptera and likely were lost with the extinction of Mesopsychidae during the mid Early or Late Cretaceous. This suggests that mesopyschid biology was quite different from the several modern lineages of scorpionflies. In particular, the maintenance of ramified antennae in their populations resulted from ecologically dispersed populations in fragmented landscapes, attributable to reliance on a spatially uncommon or otherwise rare resource that imposed a functional need for increased sensory capacity [38,39]. The ramified antennae observed in Jibaissodes bellus are present in a variety of extant sawfly taxa, including the phytophagous Megalodontesidae, invoking a similar explanation.

    (b) The evolutionary development of ramified antennae

    To the best of our knowledge, the Yixian insect fauna provides the earliest examples of ramified antennae in the fossil record, although somewhat younger, Mid-Cretaceous amber deposits contain several beetle and strepsipteran taxa also have this condition [40,41]. It does not appear that any Amphiesmenoptera (Trichoptera + Lepidoptera) taxa with ramified antennae occur prior to the mid Early Cretaceous of the Yixian Fm., including Necrotaulidae, suspected as belonging to an amphiesmenopteran paraphyletic assemblage of species that existed from the Late Triassic to Early Cretaceous [21,42]. The related and earliest known modern caddisfly, Liadotaulius maior, found in mid-Lower Jurassic strata of Germany [43,44], lacks ramified antennae. Similarly, Early Lepidoptera lack ramified antennae [45], and the earliest taxa possibly with such antennae, the Tineoidea (bagworms and relatives) and Gelechioidea (curved-horn moths), may have been present at ca 100 Ma, during the Early Cretaceous–Late Cretaceous boundary interval. By contrast, Bombycoidea (silk moths and relatives) also possess bipectinate antennae, but likely originated later during the Palaeocene [46]. Thus, Cathayamodus, possessing very similar bipectinate antennae (figure 1 and electronic supplementary material, figure S1) to some modern lepidopteran lineages, has representatives during the mid Early Cretaceous that nevertheless predates these moth fossils by at least 25 Myr. These ramified antennae likely indicate evolutionary convergences that were displaced in time and space.

    For Mecoptera, Lichnomesopsyche gloriae, L. daohugouensis, L. prochorista, and Vitimopsyche pristina from the latest Middle Jurassic of Inner Mongolia, China, and Vitimopsyche kozlovi from the mid Early Cretaceous of Hebei Province, China [15,47,48], have structurally distinctive mouthparts with elongate proboscides that indicate feeding on pollination drops for pollinating contemporaneous gymnosperm plant hosts [15]. Males and females of L. gloriae, L. daohugouensis, and L. prochorista bear short and filiform-like antennae [15,47,48], in which the flagellomere is gracile and extends in length to approximately mid-proboscis. However, V. pristina lacks preserved antennae [48], as does V. kozlovi, although a fragment of pectinate antenna, ca 1.39 mm long, was reported near the head of V. kozlovi (see [15], figure 1R). The shape and dimensions of the above-mentioned antennal fragment is identical to that of V. pectinella; therefore, we believe that V. kozlovi also possessed pectinate antennae. Because of the absence of preserved genitalic terminalia to inform us of the reproductive biology of V. kozlovi and V. pectinella, a conclusion regarding the function of their pectinate antennae is premature at this time.

    Extant sawfly lineages display a considerably more eclectic distribution of ramified antennae. Four extant sawfly families have pectinate or bipectinate antennae: Diprionidae, Pergidae, Tenthredinidae, and Megalodontesidae [18]. Unlike the related Pamphiliidae, the antennae of megalodontesids range from serrate to pectinate, and some taxa with serrate antennae have elongated serrations that could be described as either rather short rami or deep serrations [18]. However, the pectinate condition of Megalodontesidae may be an exaggerated form of a serrated antennal structure. These extinct species likely used their antennae for functions that are known in modern species with or without such modifications. From these data, it appears that the selective advantage of ramified antennae is bolstered by their iterative evolutionary appearance (and disappearance) among independently originating lineages not only of the three Cretaceous insect orders, but also their broad distribution in diverse, unrelated lineages of today.

    (c) When is a new structure not a key innovation?

    Although many morphological features come and go during macroevolutionary time scales, true evolutionary innovations are facilitated by a sequence of processes and events [49]. An essential prerequisite is the persistence of a biological feature in the face of internal (biological) or external (environmental) perturbation [50]. This persistence results in one or more sufficiently optimal solutions that become available, such that a particular phenotype (or structure) becomes fixed [50]. Additionally important for the evolvability of the phenotype is that its structural and functional scope becomes expanded [51].

    For example, many physiological innovations in insects attributable to gene duplication are associated with novel functions [52]. Also, important structures typically originate and proliferate following periods of extensive evolutionary diversification. During these intervals, populations expand, as does the breadth of their genotype networks and their phenotype products. It is in subsequent periods of significant decreases in diversity that phenotypes are culled and a significantly better structure, such as a particular ramified antenna type, assumes an additional function [53]. For insects, the most commonly cited innovations are wings and complete metamorphosis, presumably associated with increases in diversification rates [54]. A recent study [55], however, indicates that innovations insects accrued in narrowly circumscribed clades and include the origin of the elytrum in Coleoptera and development of the parasitoid life habit in Hymenoptera. Accordingly, the establishment of a new structure, or innovation, such as the elytrum, parasitoid life habit or ramified antenna, is a likely consequence of the boom-and-bust diversity cycle of lineages.

    Nevertheless, ramified antennae lack two conditions for being considered a key innovation [56]. They are: (i) a significant increase in diversification for the lineage possessing the novel structure, when compared with its sister group or other closely related lineages that lack the trait, and (ii) the success of those lineages that possess the trait such as occupation of a distinctive, ecological niche that would allow a marked advantage over other such lineages that live in different habitats but lack the trait. For these reasons, it appears that branched antennae never rose to the level of a key innovation.

    Ethics

    The authors declare that the study makes no use of humans, clinical tools, and procedures, vertebrate and regulated invertebrate animal subjects and/or tissue, and plants.

    Data accessibility

    Data forming the basis of this research and the details of analyses are available in the electronic supplementary material linked to this article.

    Authors' contributions

    T.P.G., C.K.S., C.C.L., J.A.S.-B., and D.R. designed research; all authors contributed equally in performing research and analysing data; and T.P.G., C.K.S., C.C.L., J.A.S.-B., and D.R wrote the paper, and all authors discussed, reviewed, and revised the manuscript.

    Competing interests

    The authors declare that there are no financial competing interests (political, personal, religious, ideological, academic, intellectual, commercial, or any other), nor are there other competing interests in the production of this manuscript.

    Funding

    D.R. was supported by grants from the National Natural Science Foundation of China (grant nos. 31230065 and 31672323), Program for Changjiang Scholars and Innovative Research Team at University (IRT13081); T.P.G. was supported by the National Natural Science Foundation of China (31401993). This is contribution 310 of the Evolution of Terrestrial Ecosystems consortium of the National Museum of Natural History, in Washington, D.C.

    Acknowledgements

    We are grateful for the preliminary taxonomic work by Xiaoguang Yang and Yan Gao during their graduate studies at Capital Normal University, in Beijing. We thank David Yeates of the Australian National Museum in Canberra for supplying specimens of the modern caddisfly Ramiheithrus virgatus and Ms Chen Wang for the reconstruction in figure 1i. We thank three anonymous reviewers for their constructive comments in improving the manuscript. We gratefully acknowledge Dr Michael S. Engel at The University of Kansas for his valuable suggestions and critical modifications, and Kellie K. Magill Engel for assistance and support during the production of an earlier draft of the manuscript.

    Footnotes

    Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.3469749.

    Published by the Royal Society. All rights reserved.

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