New Fossil Data and Phylogenetic Inferences Shed Light on the Morphological Disparity of Mesozoic Sinoalidae (Hemiptera, Cicadomorpha)

Organisms Diversity & Evolution (2019) 19:287–302 https://doi.org/10.1007/s13127-019-00399-y

ORIGINAL ARTICLE

New fossil data and phylogenetic inferences shed light on the morphological disparity of Mesozoic Sinoalidae (Hemiptera, Cicadomorpha)

Jun Chen1,2 & Bo Wang2,3 & Yan Zheng1,2 & Hui Jiang2,4 & Tian Jiang5 & Junqiang Zhang1 & Baizheng An1 & Haichun Zhang2

Received: 30 July 2018 /Accepted: 27 February 2019 /Published online: 9 March 2019 # Gesellschaft für Biologische Systematik 2019

Abstract Like many fossil insect groups, the systematic framework of extinct ‘Homoptera’ is mainly based on venational traits of isolated wings; most taxa of Mesozoic Sinoalidae, however, were erected with whole-bodied specimens. On the basis of new fossil data and phylogenetic analyses, this froghopper family is herein chosen as a case study to discuss the potential influence of the absence and/or neglect of body information in palaeoentomological studies. Mesodorus orientalis ChenetWang,gen.etsp.nov.,foundinthemid- Cretaceous Burmese amber, bears a venational topology of fore- and hindwings similar to that of the genus Fangyuania from the same horizon and locality, but distinctly differs from the latter and other known sinoalids in possessing a series of unique body characters. Given the similar wing features, Jiania crebra and J. gracila were proposed to be synonyms in a recent study; these two congeners, however, are apparently discernable in their ovipositor and so the synonym should be rejected. Three main clades were recovered within the Sinoalidae in our cladistic analyses, including Clade I (Stictocercopis + Chengdecercopis), Clade II (Huabeicercopis + Luanpingia + Sinoala + Jiania + Shufania), and Clade III (Fangyuania + Mesodorus), and their relationship is as following: Clade I + (Clade II + Clade III). The Jurassic Clade I, as the basal lineage, is remarkably different from other sinoalids in bearing wings with complex venation, but similar to the Jurassic Clade II in body structures. The Cretaceous Clade III possessesareducedwingtopologysimilartoClade II, but differs from the latter in possessing a series of novel body characteristics for each taxon (i.e., Fangyuania and Mesodorus). Unsurprisingly, our finds confirm that the information from body structures, vital to understanding the biodiversity and evolutionary history of extinct insects, should not be ignored in palaeoentomological studies.

Keywords Hemiptera . Body structure . Phylogeny . Morphological disparity . Burmese amber

Introduction * Jun Chen [email protected] ‘ ’ * Haichun Zhang As a long-standing tradition, the Homoptera (true hoppers, [email protected] aphids, scale insects, et cetera) and Heteroptera (true bugs) are usually treated as separate groups, having the rank of order or as 1 Institute of Geology and Paleontology, Linyi University, Shuangling suborders within Hemiptera; the ‘Homoptera,’ however, is now Road, Linyi 276000, China generally abandoned due to its paraphyly with Heteroptera and 2 State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing this taxonomic unit is divided into five suborders: the extinct Institute of Geology and Palaeontology and Center for Excellence in Paleorrhyncha and the extant Fulgoromorpha, Cicadomorpha, Life and Paleoenvironment, Chinese Academy of Sciences, 39 East Beijing Road, Nanjing 210008, China Sternorrhyncha, and Coleorrhyncha (Shcherbakov and Popov 2002;Forero2008;Szwedo2018). The history of Hemiptera is 3 Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, 1, Beichen West Road, supposed to date back to the mid-Carboniferous (~ 330 Ma) Beijing 100101, China with lots of fossil records (Nel et al. 2013; Song and Liang 4 University of Chinese Academy of Sciences, Beijing 100049, China 2013;Szwedo2018), but the reported fossil hemipterans are 5 mostly represented by isolated wings, especially the State Key Laboratory of Biogeology and Environmental Geology, ‘ ’ China University of Geosciences, Xueyuan Lu 29, Beijing 100083, Homoptera (see Carpenter 1992). The two monophyletic sub- China orders Cicadomorpha and Fulgoromorpha are collectively 288 Chen J. et al. called true hoppers (Auchenorrhyncha; Bartlett et al. 2018). fossil specimens from the Daohugou Beds, and the two mono- Although true hoppers have similar habitus and ecological specific genera Luanpingia and Huabeicercopis, based on an habits, the monophyly of this hemipteran group remains disput- isolated tegmen impression and a whole-bodied fossil respec- ed (Sorensen et al. 1995; Cryan and Urban 2012;Songetal. tively, from Middle-Upper Jurassic Jiulongshan Formation 2012;Beuteletal.2014). (Hong 1983), were also ascribed to the family (Fig. 1). The All extant cicadomorph lineages (Cercopoidea, monobasic genus Hebeicercopis, established based on an iso- Cicadoidea, and Membracoidea) and their common stem lated hindwing by Hong 1983, was also assigned to group (Hylicelloidea) constitute the clade Clypeata. These Sinoalidae, but its validity at genus and species level was insects are distinct with a greatly enlarged postclypeus with treated as an open problem, needing more fossils with tegmina transverse grooves to accommodate the muscles of the and hindwings articulated (Wang et al. 2012). Chen et al. cibarial pump needed to ingest xylem fluids that are under (2017) revised this family and reported some new material negative pressure (Shcherbakov and Popov 2002;Wang from the same horizon and locality as the type genus, with a et al. 2012;Chenetal.2014; Bartlett et al. 2018). In the remarkable genus and species Shufania hani erected. Fu et al. Permian, the extinct superfamily Hylicelloidea firstly ap- (2017)reportedanewspeciesLuanpingia daohugouensis and peared, and then derived into the three modern proposed that J. gracila should be considered as a junior syn- cicadomorph superfamilies in the Triassic (Shcherbakov onym of J. crebra. and Popov 2002;Szwedo2018). These sinoalid genera and species mentioned above share Cercopoidea, known as froghoppers (adults) or spittlebugs the following wing topology: tegmen with RA and RP with (nymphs), is a worldwide distributed insect superfamily com- only one independent terminal branch, M two-branched, and prising approximately 3000 species and occurring in most hindwing with M single-branched. However, Fu and Huang terrestrial habitats (Cryan and Svenson 2010;Chenetal. (2018) reported a remarkable genus and species, 2015a, b; Paladini et al. 2018). This superfamily, with numer- Stictocercopis wuhuaensis, from the Daohugou locality with ous primitive characters, is closer to their stem group (i.e., a relatively complex wing venation: tegmen with RA with Hylicelloidea) than the other two superfamilies, Cicadoidea three or four independent terminal branches, RP two- and Membracoidea (Shcherbakov 1992;Wangetal.2012). branched, M with five terminal branches, and hingwing with The known Mesozoic froghoppers are now assigned to three M two-branched. The monospecific genus Chengdecercopis extinct families: Procercopidae widely distributed in the from the Jiulongshan Formation, originally ascribed to Jurassic and Lower Cretaceous of Eurasia and accepted as Procercopidae (Hong 1983), is venationally similar to the one of the stem lineages of cercopoids and ancestral group genus Stictocercopis, and so should be transferred to of modern ones, Cercopionidae exclusively recorded in the Sinoalidae. Recently, a new taxon, Fangyuania xiai,was mid-Cretaceous and likely derived from the Procercopidae, erected from mid-Cretaceous burmite, with some novel and the Sinoalidae from the Middle-Upper Jurassic of north- and specialized body structures, such as head produced, eastern China and Upper Cretaceous Burmese amber crown broad, pronotum extremely shortened, and number (Shcherbakov and Popov 2002; Hamilton 1990;Chenetal. of lateral spines on hind tibia reduced, offering novel in- 2018). Sinoalidae, having a mixture of ancestral features sights into the taxonomic diversity and morphological dis- (shared with Hylicelloidea and Jurassic Procercopidae) and parity of Sinoalidae and also greatly extending the duration some specialized traits, likely represents an ancestral form of and geographic distribution of this family (Chen et al. Cercopoidea (Wang et al. 2012;Chenetal.2018). Recently, 2018). We herein report one additional new sinoalid frog- some new sinoalids have been reported from the Middle- hopper from Burmese amber, with some unique body struc- Upper Jurassic Daohugou Beds of Ningcheng, northeastern tures rarely or even never discovered in the entire super- China, and some sinoalids remain pending to be formally family Cercopoidea. described and illustrated from the same horizon; the fossil In the present study, we analyzed the morphological material, with a series of primitive traits, even further fills disparity of Mesozoic Sinoalidae based on the new fossil the morphological gap between Sinoalidae and the stem data and phylogenetic inferences, shedding light on the Clypeata (Fu and Huang 2018; unpublished data). evolutionary development of this family and providing Sinoalidae is the most recently described extinct family of some interesting information on the morphological diversi- Cercopoidea (Wang et al. 2012). This froghopper family can fication of primitive Clypeata. A considerable portion of be easily recognized by its tegmen with the costal area and fossil insect groups are mainly described on the basis of a clavus commonly more sclerotized and punctate than the re- sole fore- or hindwing. However, the vast majority of the maining part, and its hind tibia with two rows of lateral spines. Mesozoic Sinoalidae were erected based on multiple In Wang et al. (2012), three species assigned to two genera whole-bodied specimens (Table 1), providing a case study (Sinoala parallelivena, Jiania crebra, and J. gracila Wang to discuss the significance of body information in and Szwedo, 2012) were erected based on 27 whole-bodied palaeoentomological studies. New fossil data and phylogenetic inferences shed light on the morphological disparity of Mesozoic... 289

Fig. 1 Palaeogeographic distribution of the Sinoalidae. Maps reconstructed for a the Middle Jurassic (164.5 Ma) and b Late Cretaceous (96.6 Ma) after Scotese 2014. 1, Middle-Upper Jurassic of northeastern China; 2, Lowermost Upper Cretaceous of Myanmar. Circles indicate the number of genera

Material and methods (Cruickshank and Ko 2003; Poinar et al. 2008; Kania et al. 2015; Bai et al. 2017): according to Ross (2018), 916 species Fossil material and venational terminology within 713 genera attributed to 510 families in 99 orders (or similar ranks) had been reported up to the end of April 2018. The amber specimen was discovered in the Hukawng Valley Some of these taxa are hemipterans, with most belonging to the of Kachin Province in northern Myanmar. Burmese amber, suborder Heteroptera (true bugs), and only three representatives valued as a medium for jewelry and carvings, has been mined of the suborder Cicadomorpha: the singing cicada Burmacicada for thousands of years (Poinar et al. 2008). Due to the remark- protera Poinar et Kritsky, 2011, the leafhopper Priscacutius able distinction from other types, the amber was named as denticulatus Poinar et Brown, 2017, and the froghopper Burmite by Helm (1893). After a long-term controversy, the Fangyuania xiai Chen, Szwedo et Wang, 2017 (Poinar Jr. and age of Burmese amber is biostratigraphically considered to be Kritsky 2011; Poinar Jr. and Brown 2017;Chenetal.2018). mid-Cretaceous (e.g., Cruickshank and Ko 2003; Grimaldi The yellow and transparent amber containing the fossil et al. 2005;Rossetal.2010) and considered to be earliest sinoalid is deposited in the Nanjing Institute of Geology and Cenomanian (98.79 ± 0.62 Ma) as indicated in a recent U-Pb Palaeontology, Chinese Academy of Sciences (NIGP169679). zircon dating study (Shi et al. 2012). The photograph of the amber piece was taken with a Pentax Amber affords exceptional three-dimensional preservation of K-7 digital camera. The fossil specimen was examined, insects as well as other tiny organisms (Chen et al. 2016a), often photomicrographed, and measured using the VHX 5000 providing more details than imprint fossils (e.g., Perrichot et al. digital microscope platform, with incident and transmitted 2009;Wangetal.2016). As probably the most diverse Mesozoic light used simultaneously. The line drawings and reconstruc- palaeobiota (Shi et al. 2012), the Burmese amber biota now is tions were prepared using image-editing software (CorelDraw recognized as a significant window to the Cretaceous world X7 and Adobe Photoshop CS6).

Table 1 Geographical and stratigraphical distribution of Sinoalidae

Horizon Locality Taxon Preservation Reference

Cenomanian (K2) Hukawng Valley, Kachin, Fangyuania xiai Chen, Szwedo et Wang, 2018 B + T + H Chen et al. 2018 Myanmar Mesodorus orientalis gen. et sp. nov. B + T + H This paper Jiulongshan Formation, Xiaofanzhangzi, Chengde, China Chengdecercopis xiaofanzhangziensis B + T Hong 1983 Callovian-Oxfordian Hong, 1983 (J2-3) Zhouyingzi, Luangping, China Huabeicercopis yangi Hong, 1983 B + T Hong 1983 ?Hebeicercopis triangulata Hong, 1983 H Hong 1983 Luanpingia longa Hong, 1983 T Hong 1983 Daohugou Beds, Daohugou, Ningcheng, China L. daohugouensis Fu, Cai et Huang, 2017 B + T Fu et al. 2017 Callovian-Oxfordian Sinoala parallelivena Wang et Szwedo, 2012 B + T + H Wang et al. 2012 (J2-3) Jiania crebra Wang et Szwedo, 2012 B + T Wang et al. 2012 J. gracila Wang et Szwedo, 2012 B + T + H Wang et al. 2012 Shufania hani Chen, Zheng, Wei et Wang, 2017 T Chen et al. 2017 Stictocercopis wuhuaensis Fu et Huang, 2018 B + T + H Fu and Huang 2018

B body, T tegmen, H hindwing, J2-3 Middle to Upper Jurassic, K2 Upper Cretaceous 290 Chen J. et al.

The venational terminology used herein mainly follows Phylogenetic analyses Nel et al. (2012). In this study, a new interpretation of the wing venation pattern for all Paraneoptera was proposed, assuming Phylogenetic inferences were performed using two methods: that CuA gets fused with the MP+R stem at the wing base and maximum parsimony analysis (MP) in PAUP* (Swofford connected with CuP by a specialized crossvein cua-cup (tra- 2003) and Bayesian inference analysis (BI) in MRBAYES ditionally treated as the independent base of CuA), which is 3.1.2 (Ronquist and Huelsenbeck 2003). For MP analysis, remarkably different from the traditional interpretations. heuristic searches were executed for 1000 replicates with Herein, the first longitudinal vein in the clavus is treated as TBR branch swapping. Non-parametric bootstrap analysis

Pcu rather than A1 and the independent medial vein is treated (BS) with 1000 replicates was performed to assess nodal reli- as MP instead of M as in Bourgoin et al. (2015). abilities. To reduce time spent in swapping on large numbers of suboptimal trees, only five trees were retained per replicate. For BI analysis, the Mkv model, assuming all states have the Taxon sampling and character choice same frequency and all transitions between different states occur at the same rate, was chosen (Lewis 2001;Allman Up to now, 12 species within 10 genera have been ascribed to et al. 2009). Bayesian Markov Chain Monte Carlo chains were the Sinoalidae (Hong 1983; Wang et al. 2012; Chen et al. executed for 10 million generations with sample frequency 2017, 2018;Fuetal.2017; Fu and Huang 2018;thisstudy). setting as per 1000 generation. Twenty-five percent trees were ?Hebeicercopis triangulata was erected based on an isolated discarded as burn-in to ensure that the MCMC analysis had hindwing and its genus- and species-level systematic position stabilized. The Bayesian posterior probabilities (PP) of the is still uncertain, and so this taxon is excluded in our phylo- tree nodes were calculated. genetic analyses. All remaining 11 species within nine genera The 50% majority-rule trees reconstructed in the MP and are included as ingroups. The superfamily Hylicelloidea is BI analyses were used in character mapping. These inferences considered as the ancestral group to all the three modern su- were executed in the morphological analysis software pro- perfamilies (Cicadoidea, Membracoidea, and Cercopoidea) of gram WinClada ver. 1.00.08 (Nixon 2002). the Cicadomorpha (Wang et al. 2012), but most hylicelloids were described on the basis of isolated tegmina or hindwings. A few species, e.g., Vietocylca peregrina Shcherbakov 1988, Results however, contain information on wings and body structures, and so this species is chosen as the ultimate Systematic paleontology outgroup. Procercopidae is widely accepted as one of the stem lineages within Cercopoidea (Shcherbakov Order Hemiptera Linnaeus 1758 and Popov 2002;Wangetal.2012;Chenetal. Suborder Cicadomorpha Evans 1946 2015a, b). Jurocercopis grandis Wang et Zhang, 2009 Superfamily Cercopoidea Leach 1815 represents the primitive form of Procercopidae and so it Family Sinoalidae Wang and Szwedo, 2012 is chosen as another outgroup herein. Mesodorus Chen et Wang, gen. nov. All sinoalid taxa of certain systematic position were erected Type species: Mesodorus orientalis Chen et Wang, sp. nov. based on specimens possessing at least a tegmen. Except Diagnosis: As that of the type and only known species. Luanpingia longa Hong 1983 and Shufania hani Chen, Etymology: The generic name is formed from BMesozoic^ Zheng, Wei and Wang, 2017, all sinoalid species included in and the Greek Bdory^ (indicating its long and spear-like head); our phylogenetic analyses contain information on body struc- gender masculine. tures. The sinoalid hindwing is conservative and with little Mesodorus orientalis Chen et Wang, sp. nov. (Figs. 2, 3, 4, variation in related taxa. Although the hindwing is largely or 5, 6, 7, 8, 9d, 10c) even completely missing for many sinoalids, it is very likely Holotype: NIGP169679, a complete adult insect with over- that missing hindwing data have little impact on the results of lapped wings on top of the body, gender unknown. our cladistic reconstruction. Characters of body structures, Locality and age: Hukawng Valley, Kachin Province, tegmen, and hindwing are employed in our phylogenetic anal- Myanmar; lowermost Cenomanian, Upper Cretaceous. yses. The morphological matrix comprises 34 characters: Etymology: The specific epithet refers the locality of the characters 1–10 are based on body structures, 11–30 on teg- fossiliferous amber being oriental (Myanmar in Southeast mina, and 31–34 on hindwings (Table 2). Of these, 24 char- Asia). acters are coded as binary and 10 as multistate. All the char- Diagnosis: Body dorsoventrally flattened. Head extremely acters are unordered and of equal weight. Missing data are produced with anteriorly directed process and anterior margin coded with question marks and inapplicable data are coded acutely angled in middle; antenna long, with flagellum fili- with dashes. The data matrix is in Table 3. form and only four segments visible. Pronotum with length/ New fossil data and phylogenetic inferences shed light on the morphological disparity of Mesozoic... 291

Table 2 Definition of morphological characters and states

No. Morphological characters and states

Body structure 1 Crown: 0, short, not extended; 1, anteriorly slightly extended; 2, distinctly extended. 2 Anteriorly margin of Crown: 0, rounded; 1, angled in the middle. 3 Head without compound eyes: 0, with length nearly equal to or even shorter than width; 1, with length distinctly longer than width. 4 Postclypeus: 0, narrow and distinctly inflated; 1, wide at base and relatively flat. 5 Antenna: 0, short, with flagellum aristiform; 1, long, with flagellum filiform. 6 Pronotum: 0, well-developed, largely concealing mesonotum; 1, reduced, as long as or even shorter than mesonotum. 7 Longitudinal carinae on pronotum: 0, absent; 1, present, five in number. 8 Hind margin of pronotum: 0, straight or slightly curved; 1, W-shaped. 9 Position of lateral spine on hind tibiae: 0, one row; 1, two rows. 10 Ovipositor: 0, not exceeding tips of tegmen; 1, slightly exceeding tips of tegmen; 2, distinctly exceeding tips of tegmen. Tegmen 11 Level of sclerosis: 0, strongly all over; 1, wing tip more sclerotized than other parts; 2, costal area and clavus commonly more sclerotized than other parts. 12 Elliptical spots on veins: 0, absent; 1, present and numerous. 13 Pc+CP: 0, ending far away from wing tip; 1, very long, parallel to costal margin and almost ending at wing tip. 14 Common stalk of ScP+R+MP: 0, absent; 1, present, but very short; 2, relatively long. 15 Length of stem ScP+RA: 0, at most 3 times as long as ScP+R; 1, extremely longer than ScP+R, at least 4.5 times as long as the latter 16 RA: 0, multi-branched (with at least two independent terminal branches); 1, just with one independent terminal branch. 17 RA2 connecting crossvein ir when RA just with one independent terminal branch: 0, far away from bifurcation of ScP+RA; 1, very close to bifurcation of ScP+RA. 18 Common stalk of MP+CuA: 0, long; 1, present, but extremely short; 2, absent. 19 MP: 0, multi-branched (at least four in number); 1, reduced, two-branched. 20 Bifurcation of MP: 0, apparently basad of apex of clavus; 1, at the same level of apex of clavus; 2, distad of apex of clavus. 21 Bifurcation of CuA: 0, distad or almost at the same level of costal area; 1, apparently basad of apices of costal area. 22 Crossvein cua-cup connecting to: 0, MP+CuA at its bifurcation; 1, MP+CuA not at its bifurcation; 2, stem ScP+R+MP+CuA at its forking. 23 Crossvein imp: 0, present; 1, absent. 24 Crossvein mp-cua: 0, present; 1, absent. 25 Crossvein mp-cua connecting to MP: 0, at stem MP; 1, at MP3+4.

26 Crossvein mp-cua connecting to CuA: 0, at CuA1; 1, at or extremely near to bifurcation of CuA; 2, at CuA. 27 Apex of costal area: 0, basad of apex of clavus; 1, almost at the same level of apex of clavus; 2, distinctly distad of apex of clavus. 28 Cell between Pc+CP and CA: 0, short, not exceeding the middle of wing length; 1, long, near to wing tip but extremely narrow; 2, long, near to wing tip and relatively broad. 29 Length of the first apical cell: 0, apparently shorter than radial cell (C1); 1, almost as long as C1. 30 Apical cell between branches of CuA: 0, elongate; 1, shortened and nearly triangular. Hindwing 31 Peripheric membrane: 0, absent or extremely narrow; 1, present at wing apex. 32 Stem ScP+R: 0, apparently shorter than stem ScP+RA; 1, as long as, or even longer than stem ScP+RA. 33 MP: 0, multi-branched (at least three in number); 1, two-branched; 2, single-branched. 34 Crossvein mp-cua when MP not single-branched: 0, connecting MP3+4; 1, connecting stem MP.

width ratio about 0.5:1, widest at its lateral angle; five longi- basal cell nearly 1/4th of wing length; Pc+CP extremely long, tudinal carinae present. Mesonotum with mesoscutal sulcus almost parallel to costal margin; common stalk MP+CuA rel- broadly U-shaped and scutellum apparently sunken. Hind tib- atively long, connecting with crossvein cua-cup just beyond iae extremely slender with two rows of lateral piliferous its separation from ScP+R+MP+CuA; MP two-branched. spines, one and two in number for each row. Tegmen with Hindwing with outer margin smoothly curved, without pe- costal area long with apex at about basal 0.85 of wing length; ripheral membrane; stem ScP+R long; MP not branched. 292 Chen J. et al. – – – – 1111 ????

Fig. 2 Overall view of the entire amber piece containing the holotype of Mesodorus orientalis gen. et sp. nov.

Description: Body dorsoventrally flatten, size small, length including tegmen in repose about 6.5 mm, wings tent-like over abdomen. Head: Head with compound eyes length 1.1 mm, width 1.0 mm, apparently narrower than pronotum, with a median

denote that the state is unknown o r inapplicable, respectively carina. Crown with tiny granules, extremely produced into ante- ^ 200020000 10010?10 001001000 0000??11 000?00000 ?0000000 – riorly directed process; anterior margin acutely angled in middle. B Three ocelli visible on disc of crown, at about its 2/3rds length. and ^

? Compound eyes large, somewhat semicircular in dorsal view B and circular in ventral view. Postclypeus broad, with distinct transverse grooves. Antenna long, with scape apparently thicker than pedicel, flagellum filiform with only four segments visible. Thorax: Pronotum about 0.7 mm long and 1.4 mm wide, with length/width ratio about 0.5:1, widest at its lateral angle; 010010210020002 1111 ???? 010110110020000 1100012 012010210020002 1100 ???? 012010210020002 1100012 011010212021011 1100 ???? 010011010000000 2200112 010011010010000 2200012 ???? 000???200?2000{01}?0?1 010110210020002 1100 ???? 0100102101201 –– 10000 – 00000 – 00000 – disc granulate; five longitudinal carinae present, with median

phylogenetic study. The one relatively weak; anterior margin thickened, nearly straight; anterolateral margins almost as long as anterior margin; lateral angles obtuse; posterolateral margins strongly curved at junction with lateral carinae; posterior margin nearly as long as anterior margin, smoothly curved. Mesonotum about 1.0 mm long and 0.9 mm wide, with length/width ratio

racters included in the about 1.1:1, distinctly narrower than pronotum; disc with piliferous granules; mesoscutal sulcus broadly U-shaped; scutellum small and apparently sunken. Forelegs with coxae about 0.3 mm, trochanters about 0.2 mm, femora about 0.8 mm, tibiae about 1.4 mm, and tarsi about 0.4 mm in 1001110011 2 1001110011 2 210111001? 2 1001110011 2 1001110012 2 ?????????? 2 211111111? 2 000??100?? ? 100?1100?? ? ?????????? ? 000111001? 1 0000000000 0 ?????????? 0 length; femora distinctly thicker than tibiae; tibiae slender, densely covered with setae; basi- and midtarsomere of similar length and apical tarsomere distinctly longer; two well- developed tarsal claws. Middle legs with coxae about 0.2 mm, trochanters about 0.3 mm, femora about 0.9 mm, tibiae about 1.2 mm, and tarsi about 0.4 mm in length; femora strong and ridged; tibiae slender, densely covered with setae; basitarsomere about half as long as apical tarsomere, Morphological character state matrix of 34 cha midtarsomere extremely short; tarsal claws well-developed. Hind legs with coxae about 0.5 mm, trochanters about Sinoala parallelivena Jiania gracila Fangyuania xiai Luanpingia daohugouensis Jiania crebra Shufania hani Mesodorus orientalis Chengdecercopis xiaofanzhangziensis Huabeicercopis yangi Luanpingia longa Stictocercopis wuhuaensis Jurocercopis grandis ao/hrce 12345678910111213141516171819202122232425262728293031323334 Taxon/character Vietocylca peregrina Table 3 0.2 mm, femora about 0.9 mm, tibiae about 1.5 mm, and tarsi New fossil data and phylogenetic inferences shed light on the morphological disparity of Mesozoic... 293

Fig. 3 Line drawing of wings of holotype of Mesodorus orientalis gen. et sp. nov.: a tegmen; b hindwing

about 0.7 mm in length; femora long, apparently slenderer basitarsomere about as long as apical tarsomere, midtarsomere than fore- and middle femora; tibiae extremely slender, inflat- obviously shorter, basi- and midtarsomere with one row of ed at apex, with two rows of well-developed setae on surface apical teeth with long setae at apex; tarsal claws distinct. (one row obviously stronger than the other), two rows of lat- Abdomen: Abdomen flat, widest near middle. Pygofer eral piliferous spines (one and two in number for each row), largely covered by hind tarsi and nearly invisible. Genitalia and two rows of apical teeth (teeth of apical row with long completely invisible and gender unknown. Anal tube? with a setae at apex and teeth of basal row without setae); long apical process densely covered with long hairs.

Fig. 4 Photographs of holotype of Mesodorus orientalis gen. et sp. nov.: a dorsal view; b ventral view. Scale bar = 1 mm 294 Chen J. et al.

Fig. 5 Head of Mesodorus orientalis gen. et sp. nov.: a dorsal view; b anteclypeus; sca., scape; ped., pedicel; fla., flagellum. Joints between ventral view; c left antenna; d right antenna. Symbols: ant., antenna; cro., segments of antennae are indicated by isosceles triangles. Scale bars = crown; ce., compound eye; oce., ocellus; pc., postclypeus; ac., 0.5 mm

Tegmen: Tegmen punctate, distinctly longer than abdomen, 6.4:1, apex at about basal 0.85 of wing length. Clavus arched, with length about 4.9 mm, width about 1.8 mm. Costal area broad, apex at about basal 0.7 of wing length. Cell between and clavus densely covered with piliferous granules, more costal margin and Pc+CP relatively broad. Basal cell long, sclerotized than other parts. Longitudinal veins covered with nearly 1/4th of wing length. Apical cells six. Pc+CP thickened piliferous granules. Wing margin with tiny spines. Costal mar- and extremely long, almost parallel to costal margin. ScP with gin smoothly arched. Apical margin rounded. Posterior mar- independent basal part very short, running to R+MP+CuA, gin arched at about basal 0.2 of wing length and then nearly fusing with the latter just at middle of basal cell. ScP+R+ straight. Costal area broad, very long, length/width ratio about MP+CuA smoothly curved, bifurcating into ScP+R and

Fig. 6 Thorax of Mesodorus orientalis gen. et sp. nov.: a pronotum; b sulcus; scu., scutellum; cox., coxa; tro., trochanter; fem., femur; tib., tibia; mesonotum; c left foreleg; d right middle leg (mirrored); e left hind leg tar., tarsus. Scale bars = 0.5 mm (mirrored). Symbols: pro., pronotum; mes., mesonotum; ms., mesoscutal New fossil data and phylogenetic inferences shed light on the morphological disparity of Mesozoic... 295

Fig. 7 Abdomen of Mesodorus orientalis gen. et sp. nov.: a dorsal view; b ventral view; c enlargement of apical process of anal tube. Scale bars = 0.5 mm (a, b)or=0.1mm(c)

Fig. 8 Details of wings of Mesodorus orientalis gen. et sp. nov.: a puncta tegmen; d spines on outer margin of tegmen and hindwing; e spines on and piliferous granules on costal area of tegmen; b puncta and piliferous costal margin of hindwing; f puncta on hindwing. Scale bars = 0.1 mm granules on clavus of tegmen; c puncta and piliferous granules on C1 of 296 Chen J. et al.

Fig. 9 Reconstruction of head and thorax of representatives within Sinoalidae: a Stictocercopis wuhuaensis Fu et Huang, 2018; b Sinoala parallelivena Wang et Szwedo, 2012; c Fangyuania xiai Chen, Szwedo et Wang, 2018; d Mesodorus orientalis gen. et sp. nov.

MP+CuA at about basal 0.25 of wing length. ScP+R almost MP+CuA. Stem MP longer than stem ScP+R, nearly straight, straight, bifurcating into ScP+RA and RP at basal 0.4 of wing branched into MP1+2 and MP3+4 at middle of wing; MP1+ length. ScP+RA nearly straight, branching into ScP+RA1 and 2 and MP3+4 long and unbranched, connected by RA2 at about basal 0.8 of wing length. RA1 short; RA2 crossvein imp;MP3+4 connected to CuA1 by crossvein connecting crossvein ir just beyond its division from ScP+ mp-cua. Stem CuA strongly curved at base, and then

RA. RP long and slightly curved at junction with crossveins nearly straight, branching into CuA1 and CuA2 at about ir and rp-mp.Positionofcrossveinrp-mp variable, apparently basal 0.75 of wing length, slightly basad of end of CuP. basad of crossvein ir in left tegmen but distad in right one. CuP long and nearly straight beyond crossvein cua-cup.

Common stalk MP+CuA relatively long, connecting with Pcu nearly straight and sub-parallel to CuP. A1 long and crossvein cua-cup just beyond its separation from ScP+R+ sub-parallel to Pcu.

Fig. 10 Reconstruction of hind tibia of representatives within Sinoalidae: a Jiania crebra Wang et Szwedo, 2012; b Fangyuania xiai Chen, Szwedo et Wang, 2018; c Mesodorus orientalis gen. et sp. nov. New fossil data and phylogenetic inferences shed light on the morphological disparity of Mesozoic... 297

Hindwing: Wing membrane punctate and wing margin monophyletic group with low BS support (Clade II; 49%), with tiny spines. Outer margin smoothly curved, without pe- and the Cretaceous ones (Fangyuania xiai and Mesodorus ripheral membrane. Stem ScP+R long, branching into ScP+ orientalis gen. et sp. nov.) constituted the other monophyletic

RA and RP near wing incision of anterior margin; ScP+RA1 clade with significant support (Clade III; 94%; 2: 0 > 1, 27: very short, separating from ScP+RA just apicad of wing inci- 1 > 2). Within Clade II, the phylogenetic relationships among sion; RA2 and RP unbranched and slightly curved; RP con- different genera and species were not well resolved (BS values nected to MP by crossvein rp-mp. MP not branched, slightly 41% at most), and the two non-monospecific genera Jiania curved at junction with crossveins rp-mp and mp-cua. Stem and Luanpingia were resolved as monophyletic lineages, with

CuA long, bifurcating into CuA1 and CuA2 apicad of bifurca- BS supports as 50 and 81%, respectively. Shufania hani was tion of ScP+RA; CuA1 slightly longer than CuA2. recovered as a very specialized taxon, with a series of synapomorphic and homoplasious traits on tegmen (20: 0 > Phylogenetic assessments 2, 23: 0 > 1, 25: 0 > 1, 26: 2 > 1). Within the well-supported Clade III, the validity of the systematic position of the new Maximum parsimony analysis yielded 103 most parsimonious genus and species Mesodorus orientalis was supported, with trees, with the following characteristics: tree length = 50, con- three synapomorphies of body structure (3: 0 > 1, 7: 0 > 1, 8: sistency index (CI) = 0.900, and retention index (RI) = 0.857. 0 > 1), which is remarkably distinguishing is from sibling tax- The 50% majority-rule consensus tree (plus other groups com- on Fangyuania xiai from same original horizon and locality. patible with this tree) is shown in Fig. 11 with bootstrap sup- Bayesian inference analysis converged before 10 million port values (BS) labeled near tree nodes. The monophyly of generations, and the average standard deviation of split fre- the Sinoalidae was recovered with BS value as 70%. The quencies was well below 0.01 at the end and so stasis was Middle to Late Jurassic Stictocercopis wuhuaensis and considered to be reached. The 50% majority-rule consensus Chengdecercopis xiaofanzhangziensis constituted a mono- tree from Bayesian analysis is shown in Fig. 12,withPP phyletic clade (Clade I; BS 68%; character number and state labeled near tree nodes. The topology of the BI tree was the change 30: 0 > 1) and occupied the basal position of the same as that of 50% majority-rule consensus MP tree at nodes Sinoalidae, with sister relationship to all remaining sinoalids, with high support values; however, in spite of relatively low which constituted a monophyletic clade (76%; 13: 0 > 1, 16: support, more dichotomic nodes were resolved in MP tree, but 0 > 1, 19: 0 > 1, 33: 1 > 2). In this clade, all remaining Middle many clades recovered in the MP tree were not resolved in the to Late Jurassic taxa (Huabeicercopis yangi, Luanpingia BI tree, since some nodes were polychotomous. The mono- longa, L. daohugouensis, Sinoala parallelivena, Jiania phyly of the Sinoalidae was recovered and well supported (PP crebra, J. gracila, and Shufania hani) were recovered as a 0.97; character number and state change: 18: 0 > 2, 22: 0 > 2).

Fig. 11 Fifty percent majority-rule consensus tree of Sinoalidae inferred characters, and the black circles indicate non-homoplasious characters. from maximum parsimony analysis based on 34 morphological I, II, and III indicate three clades of Sinoalidae discussed in the text. characters. Numbers above the nodes indicate bootstrap support values. Polygons behind taxa indicate their locality and age: the Middle to Late Numbers above branches indicate character numbers, and below Jurassic of northeastern China (squares) and the Late Cretaceous of branches indicate state changes. White circles indicate homoplasious Myanmar (triangles) 298 Chen J. et al.

Fig. 12 Fifty percent majority-rule consensus tree of Sinoalidae inferred indicate character numbers, and below branches indicate state changes. from Bayesian inference analysis based on 34 morphological characters, White circles indicate homoplasious characters, and the black circles with representatives of fore- and hind wings illustrated. Numbers above indicate non-homoplasious characters. I, II, and III indicate three clades the nodes indicate posterior probabilities. Numbers above branches of Sinoalidae recovered in MP three and discussed in the text

Stictocercopis wuhuaensis and Chengdecercopis Huang 2018). The new taxon Mesodorus orientalis gen. et sp. xiaofanzhangziensis occupied the basal position of the nov. in Cretaceous amber undoubtedly belongs to Sinoalidae Sinoalidae, but the two taxa were not resolved as a monophy- on the following characteristics: three ocelli on crown; disc of letic lineage. The remaining sinoalids constituted a monophy- crown and pronotum with granules; antennal flagellum fili- letic clade with a high PP value and a series of synapomorphic form, with few elongate segments; postclypeus very wide; features in body structure, tegmen, and hindwing (0.98; 1: 0 > hind tibia with two rows of lateral spines; tegmen with costal 1, 13: 0 > 1, 16: 0 > 1, 19: 0 > 1, 28: 0 > 1, 33: 1 > 2). Clade II area and clavus more sclerotized and remaining parts mem- constituted the Middle to Late Jurassic sinoalids but was not branous, appendix absent, vein MP with two terminals and recovered and phylogenetic relationships in this clade were crossvein imp present; hindwing without submarginal vein also unresolved; however, the two non-monospecific genera and appendix, with stem ScP+R long and M not branched. Jiania and Luanpingia were resolved as monophyletic line- The new genus and species, however, is distinctly different ages as in the MP tree, with PP support values as 0.59 and from all reported sinoalids in bearing the following three re- 0.73, respectively. Clade III constituted the Cretaceous markable characteristics of the body structure: (1) crown ex- Fangyuania xiai and Mesodorus orientalis gen. et sp. nov. tremely extended, produced into a long anteriorly directed was significantly supported with a high PP value and a series process and so making head distinctly longer than wide (ex- of synapomorphic and homoplasious features in body struc- cluding compound eyes); (2) five longitudinal carinae present ture and tegmen (0.98; 1: 1 > 2, 2: 0 > 1, 17: 0 > 1, 18: 2 > 0, on pronotum, with the medial one relatively weak; (3) hind 27: 1 > 2, 28: 1 > 2). Within the clade, Fangyuania xiai and margin of pronotum W-shaped. Mesodorus orientalis gen. et sp. nov. were separated from Modern froghoppers commonly have a compact and round each other by displaying one synapomorphy (31: 0 > 1) and crown with a distinct tylus; nevertheless, an elongate head has three synapomorphies (3: 0 > 1, 7: 0 > 1, 8: 0 > 1), evolved several times in independent genera of the modern frog- respectively. hopper families Machaerotidae, Aphrophoridae, and Clastopterinae, such as in Dianmachaerota, Grypomachaerota, Sigmasoma,andPhilagra Stål, 1863, and Grellaphia (Hayashi Discussion 1985; Nie and Liang 2009; Hamilton 2015;Wangetal.2015). The long head process of these extant cercopoids, however, is Validity of the new taxon obviously different from that of the new taxon in having a very narrow and/or strongly upcurved shape. All recorded fossil frog- The family Sinoalidae possesses some plesiomorphic traits hoppers have a short and rounded crown just like most living similar to ancient Clypeata (i.e., Hylicelloidea), shares some ones. Therefore, the flat and spear-like head of the new taxon is morphological features with con-superfamilial Procercopidae, unique within the Cercopoidea. In addition, the pronotum with and also bears some derived remarkable characters (Wang five longitudinal carinae in Mesodorus orientalis gen. et sp. nov. et al. 2012;Chenetal.2017, 2018;Fuetal.2017;Fuand is likely another specialized trait for the Cercopoidea to our New fossil data and phylogenetic inferences shed light on the morphological disparity of Mesozoic... 299 knowledge. A mesonotum with several longitudinal carinae is form from the Jurassic Clade I to the Cretaceous Clade III. The common for certain groups of the Fulgoromorpha and is also two distinct Jurassic clades clearly show that Sinoalidae was recorded in the extinct cicadomorph family Palaeontinidae highly diverse in the latest Middle Jurassic, suggesting that (Wang et al. 2008;Chenetal.2016b). Nevertheless, few groups this family should have originated much earlier than the fossil within the two related hemipteran orders have a pronotum with record indicates (Wang et al. 2012). As a primitive cercopoid obvious lateral longitudinal carinae. The pronotum with hind lineage, Sinoalidae shares some plesiomorphic characters with margin W-shaped is one of the common characters for modern ancient Clypeata (Hylicelloidea), discernable from its sibling froghoppers, except for certain cercopids (Evans 1966). lineage Procercopidae (Wang et al. 2012;Chenetal.2018). Considering that Mesodorus orientalis gen. et sp. nov. apparent- Considering that Procercopidae has been well recorded in the ly nested within the Sinoalidae in our phylogenetic analyses, the Lower Jurassic in Eurasia and was even reported in the low- pronotum with hind margin W-shaped shared by the new taxon ermost Jurassic Dzhil Formation of Kyrgyzstan (formerly and modern froghoppers should be the result of parallel reported as the Upper Triassic) (Becker-Migdisova evolution. 1962; Shcherbakov and Popov 2002), these two primitive Besides the three remarkable body characteristics men- lineages of Cercopoidea likely split in the Late Triassic. tioned above, Mesodorus gen. nov. can be distinguished from Although as one of the most abundant groups of other sinoalid genera by a series of wing features. The new Cercopoidea reported in the Mesozoic, Sinoalidae has an ap- genus differs from Stictocercopis and Chengdecercopis in parently fragmentary fossil record in temporal and spatial di- possessing a tegmen with Pc+CP extremely long, almost par- mensions up to now. Considering its abundance and remark- allel to the costal margin, RA with just one independent ter- able morphological disparity in the Middle to Late Jurassic minal branch, MP two-branched, and a hindwing with MP and putative origin in the Late Triassic, the family was likely unbranched; from Huabeicercopis, Luanpingia, Sinoala, more widespread in the Jurassic and Cretaceous than the fossil

Jiania,andShufania in possessing a tegmen with RA2 record indicated. However, the fragmentary fossil record connecting crossvein ir just beyond its division from ScP+ limits us to further infer its distribution and radiation in the RA, common stalk MP+CuA relatively long, and apex of Jurassic and Early Cretaceous. Fangyuania and Mesodorus costal area distinctly distad of claval apex, cell between Pc+ gen. nov. in Burmese amber possess some remarkably novel CP and CA broad; from Fangyuania in possessing a tegmen morphological traits, indicating that the Sinoalidae was highly with MP+CuA connecting crossvein cua-cup just beyond its diversified in the mid-Cretaceous. The sinoalids likely fed on division from ScP+R+MP+CuA, and a hindwing with periph- some gymnosperms, being xylem-feeders as the other early eral membrane absent. Clypeata (Chen et al. 2018). True hoppers including Cicadomorpha are generally monophagous or narrowly oli- Diversity, distribution, and evolution of Sinoalidae gophagous (Bartlett et al. 2018). Crown angiosperms rose in the Aptian and onwards in the Cretaceous Terrestrial With 10 genera described, Sinoalidae is now the most diverse Revolution as indicated by fossil flowers, isolated floral or- among the three Mesozoic families within the Cercopoidea at gans, and leaves (Zherikhin 2002; Lloyd et al. 2008; generic level (Hong 1983;Wangetal.2012;Chenetal.2017, Herendeen et al. 2017; Katz 2017). Therefore, sinoalids likely 2018;Fuetal.2017;FuandHuang2018; this study). became extinct in the late Mesozoic owing to a food crisis Furthermore, some new sinoalid genera and species remain (i.e., the displacement of the host-plants during the angiosper- to be described from the Middle to Upper Jurassic mous floristic revolution), together with other extinct Daohugou Beds (Callovian-Oxfordian) and their coeval strata Cicadomorpha, such as Palaeontinidae, Hylicellidae, in northeastern China, and the Upper Cretaceous Burmese Procercopidae, and Archijassidae (Shcherbakov and Popov amber (Cenomanian) (unpublished data). Nevertheless, the 2002; Shcherbakov 2012;Wangetal.2012;Chenetal. known sinoalids are exclusively recorded from these two 2016b). lagerstätten to date (Chen et al. 2018). Sinoalidae from the Callovian-Oxfordian of northeastern Morphological disparity of Sinoalidae China divided into two distinct clades in our phylogenetic reconstruction (Figs. 11 and 12). Clade I, consisted of the Three lineages were recovered within the known sinoalids in genera Stictocercopis and Chengdecercopis,lackofderived our cladistic analyses (Figs. 11 and 12). The Jurassic Clade I morphological characteristics, apparently represents a primi- from the Callovian-Oxfordian of northeastern China, sharing tive lineage of the Sinoalidae. The Clade II, consisting of the many primitive characters with Hylicelloidea and remaining genera (Huabeicercopis, Luanpingia, Sinoala, Procercopidae (represented by two outgroups Vietocylca Jiania, and Shufania), shares a series of apomorphies with peregrina and Jurocercopis grandis, respectively), is likely the two genera Fangyuania and Mesodorus gen. nov. (Clade the most ancient representative of the Sinoalidae. Compared III) from Cretaceous burmite, likely representing a transitional to Clade I, Clade II from the same stratum evolved a series of 300 Chen J. et al. novel and unique wing characteristics: Pc+CP long, parallel to determinants of systematic palaeoentomology. The informa- costal margin and almost ending at wing tip, RA reduced, with tion from body structures are vital to understanding the diver- only one independent terminal branch, MP reduced, with only sification as well as the evolutionary process of extinct insects, two terminal branches, cell between Pc+Cp long but narrow and so should not be dismissed lightly. On the contrary, body on tegmen, and MP reduced, with only one terminal branch on structures need to be described and illustrated in detail and hindwing (Fig. 12). The body structures of Clade I and Clade also should be analyzed appropriately in palaeoentomological II, however, do not change as drastically as wings (Figs. 9a, b studies. and 10a). The Cretaceous Clade III from burmite possesses wing traits similar to Clade II, but its characteristics are appar- Acknowledgements The authors sincerely thank Limei Lin and Yameng ently derived: crown distinctly extended with anterior margin Li for their constructive comments on an earlier version of the manuscript. We also express our heartfelt thanks to Qian Long who helped take the angled in the middle, and hind tibia cylindrical and slender, photograph of the entire amber piece. with lateral spines reduced in number and apical teeth ar- ranged in double rows (Figs. 9c, d and 10b, c). Although with Funding information This research was supported by the National a similar wing topology, the two Cretaceous genera bear some Natural Science Foundation of China (41502007; 41702012; 41572010; very specialized body features: pronotum extremely shortened 41622201; 41688103), the Natural Scientific Foundation of Shandong Province (ZR2016DB24; ZR2016DL04), the China Postdoctoral for Fangyuania, which is unique in the Cercopoidea (Chen Science Foundation (2017M621582), the State Key Laboratory of et al. 2018), and head spear-like and five longitudinal carinae Palaeobiology and Stratigraphy (Nanjing Institute of Geology and present on pronotum inr Mesodorus gen. nov. Palaeontology, CAS) (No. 183105), and the Strategic Priority Research Our phylogenetic analyses show that the relative evolution- Program (B) of the Chinese Academy of Sciences (XDB26000000). ary rates of body structures and wings in different geological Publisher’snoteSpringer Nature remains neutral with regard to jurisdic- periods are somewhat discrepant for the Sinoalidae. Besides, tional claims in published maps and institutional affiliations. possibly due to the simplified topology and reduced branches of longitudinal veins, the hindwings of Cicadomorpha commonly bear fewer diagnostic traits than forewing (Wang et al. 2009;Chenetal.2017). Traditionally, the taxonomy and high- References level classification of the extinct ‘Homoptera’ including Cicadomorpha are mainly on the basis of isolated wings (see Allman, E. S., Holder, M. T., & Rhodes, J. A. (2009). Estimating trees from filtered data: identifiability of models for morphological phy- Carpenter 1992). The genus Jiania was established by Wang logenetics. Journal of Theoretical Biology, 263,108–119. et al. (2012) based on 12 well-preserved and whole-bodied Bai, M., Nie, R., Zhang, W., Ren, D., Shih, C., & Yang, X. (2017). The fossil specimens from the Daohugou beds, Inner Mongolia, first fossil Athyreini beetle (Coleoptera: Geotrupidae). Organisms – China, with two species Jiania crebra and Jiania gracila orig- Diversity & Evolution, 17,157 162. inally attributed to it. Fu et al. (2017) considered that these two Bartlett, C. R., Deitz, L. L., Dmitriev, D. A., Sanborn, A. F., Soulier- Perkins, A., & Wallace, M. S. (2018). The diversity of the true species should be synonymized since they bear the similar hoppers (Hemiptera: Auchenorrhyncha). Insect Biodiversity: body size and wing features. However, these two species are Science and Society, 2,501–590. apparently distinguishable on body structures: J. crebra pos- Becker-Migdisova, E. E. (1962). Some new Hemiptera and Psocoptera. – sesses an extremely long ovipositor, distinctly exceeding tip of Paleontologicheskii Zhurnal, 1962,89 104. Beutel, R. G., Friedrich, F., Ge, S., & Yang, X. (2014). Insect morphology tegmen, which is remarkably different from that of J. gracila, and phylogeny. A textbook for students of entomology.Berlin- and so the synonymy proposed by Fu et al. (2017)shouldbe Boston: Walter de Gruyter. rejected. Bourgoin, T., Wang, R., Asche, M., Hoch, H., Soulier-Perkins, A., Most reported Mesozoic cicadomorphs were described on Stroinski, A., Yap, S., & Szwedo, J. (2015). From micropterism to the basis of a single incomplete specimen, even just with only hyperpterism: recognition strategy and standardized homology- driven terminology of the forewing venation patterns in one fore- or hindwing preserved; most taxa within Sinoalidae, planthoppers (Hemiptera: Fulgoromorpha). Zoomorphology, 134, however, were erected with multiple whole-bodied speci- 63–77. mens, with some clear details of body structures as well as Carpenter, F. M. (1992). Superclass Hexapoda. In R. L. Kaesler (Ed.), wings (Wang et al. 2012;Chenetal.2017, 2018;Fuetal. Treatise on invertebrate paleontology, Part R, Arthropoda 4 (pp. 1– 655). Boulder, Colorado: Geological Society of America. 2017; Fu and Huang 2018; this study), providing an ideal case Chen, J., Wang, B., Zhang, H., & Wang, X. (2014). A remarkable new study for researching the morphological diversification and genus of Tettigarctidae (Insecta, Hemiptera, Cicadoidea) from the disparity in fossil insect groups erected mainly based on iso- Middle Jurassic of northeastern China. Zootaxa, 3764,581–586. lated wings. The present study shows that the current system- Chen, J., Wang, B., Zhang, H., Wang, X., & Zheng, X. (2015a). New atic framework of extinct ‘Homoptera’ just based on isolated fossil Procercopidae (Hemiptera: Cicadomorpha) from the Middle Jurassic of Daohugou, Inner Mongolia, China. European Journal of wings likely leads to underestimating its paleodiversity and Entomology, 112,373–380. does not help us to clearly outline its evolutionary history. Chen, J., Zhang, H., Wang, B., Zheng, X., & Wang, X. (2015b). High Wing characters alone are apparently not sufficient variability in tegminal venation of primitive cercopoids (Insecta, New fossil data and phylogenetic inferences shed light on the morphological disparity of Mesozoic... 301

Hemiptera), as implied by the new discovery of fossils from the integrative approaches to understanding angiosperm origins and Middle Jurassic of China. Entomological Science, 18,147–152. species richness. Annals of Botany, 121,1–8. Chen, J., Wang, B., & Jarzembowski, E. A. (2016a). Palaeontology: Leach, W. E. (1815). Entomology. In D. Brewster (Ed.), The Edinburgh benefits of trade in amber fossils. Nature, 532,441. Encyclopaedia (pp. 57–172). Edinburgh: Blackwood. Chen, J., Zhang, H., Wang, B., Zheng, X., & Wang, X. (2016b). New Lewis, P. O. (2001). A likelihood approach to estimating phylogeny from Jurassic Sinopalaeocossus and related genera with notes on their discrete morphological character data. Systematic Biology, 50,913– evolutionary implications (Hemiptera, Palaeontinidae). Insect 925. Systematics & Evolution, 47,113–129. Linnaeus, C. (1758). Systema natura per regna tria naturae secundum Chen, J., Zheng, Y., Wei, G., & Wang, X. (2017). New data on Jurassic classes, ordines, genera, species, cum characteribus, differentiis, Sinoalidae from northeastern China (Insecta, Hemiptera). Journal of synonymis, locis (10th ed.). Holmiae: Laurentius Salvius 824 pp. Paleontology, 91,994–1000. Lloyd, G. T., Davis, K. E., Pisani, D., Tarver, J. E., Ruta, M., Sakamoto, Chen, J., Szwedo, J., Wang, B., Zheng, Y.,Wang, Y., Wang, X., & Zhang, M., Hone, D. W. E., Jennings, R., & Benton, M. J. (2008). Dinosaurs H. (2018). The first Mesozoic froghopper in amber from northern and the Cretaceous Terrestrial Revolution. Proceedings of the Royal Myanmar (Hemiptera, Cercopoidea, Sinoalidae). Cretaceous Society B, 275,2483–2490. Research, 85,243–249. Nel, A., Prokop, J., Nel, P., Grandcolas, P., Huang, D., Roques, P., Cruickshank, R. D., & Ko, K. (2003). Geology of an amber locality in the Guilbert, E., Dostal, O., & Szwedo, J. (2012). Traits and evolution Hukawng Valley, northern Myanmar. Journal of Asian Earth of wing venation pattern in paraneopteran insects. Journal of – Sciences, 21,441–455. Morphology, 273,480 506. Cryan, J. R., & Svenson, G. J. (2010). Family-level relationships of the Nel, A., Roques, P., Nel, P., Prokin, A. A., Bourgoin, T., Prokop, J., spittle bugs and froghoppers (Hemiptera: Cicadomorpha: Szwedo, J., Azar, D., Desutter-Grandcolas, L., Wappler, T., Cercopoidea). Systematic Entomology, 35,393–415. Garrouste, R., Coty, D., Huang, D., Engel, M. S., & Kirejtshuk, A. Cryan, J. R., & Urban, J. M. (2012). Higher-level phylogeny of the insect G. (2013). The earliest known holometabolous insects. Nature, 503, – order Hemiptera: is Auchenorrhyncha really paraphyletic? 257 261. Systematic Entomology, 37,7–21. Nie, J., & Liang, A. (2009). Dianmachaerota serratiphalla,anewgenus Evans, J. W. (1946). A natural classification of leaf-hoppers (Homoptera, and species of Machaerotini from China (Hemiptera: Cercopoidea: Machaerotidae). Annals of the Entomological Society of America, Jassoidea). Part 1. External morphology and systematic position. – Transactions of the Royal Entomological Society of London, 96, 102,739 746. 47–60. Nixon, K. C. (2002). WinClada Ver. 1.00.08.NewYork:Ithaca. Paladini, A., Takiya, D. M., Urban, J. M., & Cryan, J. R. (2018). New Evans, J. W. (1966). The leafhoppers and froghoppers of Australia and World spittlebugs (Hemiptera: Cercopidae: Ischnorhininae): dated New Zealand (Homoptera: Cicadelloidea and Cercopoidea). molecular phylogeny, classification, and evolution of aposematic Australian Museum Memoir, 12,1–347. coloration. Molecular Phylogenetics and Evolution, 120,32–334. Forero, D. (2008). The systematics of the Hemiptera. Revista Perrichot, V., Nel, A., & Quicke, D. L. J. (2009). New braconid wasps Colombiana de Entomología, 34,1–21. from French Cretaceous amber (Hymenoptera, Braconidae): Fu, Y., & Huang, D. (2018). New fossil genus and species of Sinoalidae synonymisation with Eoichneumonidae and implications for the (Hemiptera: Cercopoidea) from the Middle to Upper Jurassic de- phylogeny of Ichneumonoidea. Zoologica Scripta, 38,79–88. posits in northeastern China. European Journal of Taxonomy, 115, Poinar, G. O., Buckley, R., & Brown, A. E. (2008). The secrets of burmite 127–133. amber. Mid-America Paleontological Society Digest, 20,21–29. Fu, Y., Cai, C., & Huang, D. (2017). A new fossil sinoalid species from Poinar, G., Jr., & Brown, A. (2017). A new genus of leafhoppers the Middle Jurassic Daohugou beds (Insecta: Hemiptera: – (Hemiptera: Cicadellidae) in mid-Cretaceous Myanmar amber. Cercopoidea). Alcheringa, 42,94 100. Historical Biology,1–4. https://doi.org/10.1080/08912963.2017. Grimaldi, D., Zhang, J., Fraser, N. C., & Rasnistyn, A. (2005). Revision 1384472. of the bizarre Mesozoic scorpionflies in the Poinar, G., Jr., & Kritsky, G. (2011). Morphological conservatism in the Pseudopolycentropodidae (Mecopteroidea). Insect Systematics & foreleg structure of cicada hatchlings, Burmacicada protera n. gen., – Evolution, 36,443 458. n. sp. in Burmese amber, Dominicicada youngi n. gen., n. sp. in Hamilton,K.G.A.(1990).Chapter6.Homoptera.InD.A.Grimaldi Dominican amber and the extant Magicicada septendecim (L.) (Ed.), Insects from the Santana Formation, Lower Cretaceous of (Hemiptera: Cicadidae). Historical Biology, 24,461–466. – Brazil (pp. 82 122). New York: Bulletin of the American Museum Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylo- of Natural History. genetic inference under mixed models. Bioinformatics, 19, 1572– Hamilton, K. G. A. (2015). A new tribe and species of Clastopterinae 1574. (Hemiptera: Cercopoidea: Clastopteridae) from Africa, Asia and Ross, A., Mellish, C., York, P., & Crighton, B. (2010). Chapter 12. – North America. Zootaxa, 3946,151 189. Burmese amber. In D. Penney (Ed.), Biodiversity of fossils in amber Hayashi, M. (1985). A new species of Machaerotidae (Homoptera, from the major world deposits (pp. 208–235). Manchester: Siri Cercopoidea) from Taiwan. Kontyu, 53,366–369. Scientific Press. Helm, O. (1893). Further note on Burmite, a new amber-like fossil resin Ross, A.J. (2018). Burmese (Myanmar) amber taxa, on-line checklist from Upper Burma. Records of the Geological Survey of India (Vol. v.2018.1. http://www.nms.ac.uk/explore/stories/natural-world/ 26, pp. 61–64). burmese-amber/ Herendeen, P. S., Friis, E. M., Pedersen, K. R., & Crane, P. R. (2017). Scotese, C. R., (2014). Atlas of Jurassic paleogeographic maps, Palaeobotanical redux: revisiting the age of the angiosperms. Nature PALEOMAP Atlas for ArcGIS. Evanston, IL: Mollweide Plants, 3, 17015. Projection, PALEOMAP Project. Hong, Y. (1983). Middle Jurassic fossil insects in north China. Beijing: Shcherbakov, D. E. (1988). New cicadas (Cicadina) from the later Geological Publishing House 187 pp. Mesozoic of Transbaikalia. Paleontological Journal, 4,52–63. Kania, I., Wang, B., & Szwedo, J. (2015). Dicranoptycha Osten Sacken, Shcherbakov, D. E. (1992). The earliest leafhoppers (Hemiptera: 1860 (Diptera, Limoniidae) from the earliest Upper Cretaceous Karajassidae n. fam.) from the Jurassic of Karatau. Neues Burmese amber. Cretaceous Research, 52, 522–530.Katz, O. Jahrbuch für Geologie und Paläontologie Monatshefte, 1992,39– (2017). Extending the scope of Darwin’s ‘abominable mystery’: 51. 302 Chen J. et al.

Shcherbakov, D. E. (2012). More on Mesozoic Membracoidea Szwedo, J. (2018). The unity, diversity and conformity of bugs (Homoptera). Russian Entomological Journal, 21,15–22. (Hemiptera) through time. Earth and Environmental Science Shcherbakov, D. E., & Popov, Y. A. (2002). Superorder Cimicidea Transactions of the Royal Society of Edinburgh, 107,109–128. Laicharting, 1781 order Hemiptera Linné, 1758. The bugs, cicadas, Wang, B., Zhang, H., Fang, Y., Wang, D., & Ji, S. (2008). New data on plantlice, scale insects, etc. In A. P. Rasnitsyn & D. L. J. Quicke Cretaceous Palaeontinidae (Insecta: Hemiptera) from China. (Eds.), History of insects (pp. 152–155). Dordrecht: Kluwer Cretaceous Research, 29,551–560. Academic Publisher. Wang, B., Zhang, H., & Szwedo, J. (2009). Jurassic Palaeontinidae from Shi, G., Grimaldi, D. A., Harlow, G. E., Wang, J., Wang, J., Wang, M., Lei, China and the higher systematics of Palaeontinoidea (Insecta: W., Li, Q., & Li, X. (2012). Age constraint on Burmese amber based Hemiptera: Cicadomorpha). Palaeontology, 52,53–64. on U-Pb dating of zircons. Cretaceous Research, 37, 155–163. Wang, B., Szwedo, J., & Zhang, H. (2012). New Jurassic Cercopoidea Song, N., & Liang, A. (2013). A preliminary molecular phylogeny of from China and their evolutionary significance (Insecta: Hemiptera). planthoppers (Hemiptera: Fulgoroidea) based on nuclear and mito- Palaeontology, 55,1223–1243. chondrial DNA sequences. PLoS One, 8, e58400. Wang, B., Xia, F., Engel, M. S., Perrichot, V.,Shi, G., Zhang, H., Chen, J., Song, N., Liang, A., & Bu, C. (2012). A molecular phylogeny of Jarzembowski,E.A.,Wappler,T.,&Rust,J.(2016).Debris- Hemiptera inferred from mitochondrial genome sequences. PLoS carrying camouflage among diverse lineages of cretaceous insects. One, 7, e48778. Science Advances, 2, e1501918. Sorensen, J. T., Campbell, B. C., Gill, R. J., & Steffen-Campbell, J. D. Wang, T., Pan, L., Zhang, Y., & Dai, W. (2015). Morphology of the (1995). Non-monophyly of Auchenorrhyncha (BHomoptera^), based mouthparts of the spittlebug Philagra albinotata Uhler upon 18S rDNA phylogeny: eco-evolutionary and cladistic implica- (Hemiptera: Cercopoidea: Aphrophoridae). Arthropod Structure tions within pre-heteropterodea Hemiptera (s. l.) and a proposal for and Development, 44,121–130. new monophyletic suborders. Pan-Pacific Entomologist, 71,31–60. Zherikhin, V. V. (2002). Ecological history of the terrestrial insects. In A. Swofford, D. L. (2003). PAUP*. Phylogenetic analyses using parsimony P. Rasnitsyn & D. L. J. Quicke (Eds.), History of insects (pp. 331– (* and other methods). Sunderland: Sinauer Associates. 388). Dordrecht: Kluwer Academic Publisher.