The earliest fossil record of Panorpidae (Mecoptera) from the Middle Jurassic of China

Abstract The early history of Panorpidae (Mecoptera) is poorly known due to sparse fossil records. Up to date, only nine fossil species have been described, all from the Paleogene, except the Early Cretaceous Solusipanorpa gibbidorsa Lin, 1980. However, we suggest S. gibbidorsa is too incompletely preserved to permit even family classification. A new genus with two new species, Jurassipanorpa impunctata gen. et sp. n. and Jurassipanorpa sticta sp. n., are described based on four well-preserved specimens from the late Middle Jurassic Jiulongshan Formation of Daohugou, Inner Mongolia, China. These two new species are the earliest fossil records of Panorpidae. The new genus is erected based on a combination of forewing characters: both R1 and Rs1 with two branches, 1A reaching posterior margin of wing distad of the forking of Rs from R1, and no crossveins or only one crossvein between veins of 1A and 2A. In all four specimens, long and robust setae ranging from 0.09 to 0.38 mm in length and pointing anteriorly, are present on anal veins of forewings. The function of these setae is enigmatic.


Introduction
Mecoptera is a small order of insects, comprising about 600 extant species assigned to nine families (Cai et al. 2008, Krzemiński andSoszyńska-Maj 2012). The Panorpidae is the largest family in the order, with about 400 extant species in six genera: Panorpa Linnaeus, 1758, Leptopanorpa MacLachlan, 1875, Neopanorpa Weele, 1909, Sinopanorpa Cai, Huang & Hua, 2008, Furcatopanorpa Ma & Hua, 2011and Dicerapanorpa Zhong & Hua, 2013(Byers 1967, Cai et al. 2008, Cai and Hua 2009, Ma and Hua 2011, Zhong and Hua 2013. Fossil records of the Panorpidae are fairly rare. Up to date, only three genera have been described in this family and two of them are fossil-only genera: Solusipanorpa Lin, 1980 with one species from the Early Cretaceous of China (Lin 1980); Baltipanorpa Krzemiński, 2012 with one species from the Eocene Baltic amber (Krzemiński and Soszyńska-Maj 2012); and Panorpa Linnaeus, 1758 with seven species from Baltic amber, Eocene of U.S.A. and Oligocene of Germany (Carpenter 1931, Statz 1936, Carpenter 1954. However, the holotype (and the only known specimen) of Solusipanorpa gibbidorsa is too incompletely preserved and cannot be attributed to any particular family. In addition, Archibald et al. (2013: fig. 23) reported several undescribed specimens of Panorpidae in the Early Eocene Okanagan Highlands, Canada and U.S.A. Therefore, with Solusipanorpa gibbidorsa ignored, the fossil records of Panorpidae are known so far since the Early Eocene.
Recently we collected four well-preserved fossils, which we attribute to Panorpidae, from the Jiulongshan Formation at Daohugou, Ningcheng County, Inner Mongolia, China. The Jiulongshan Formation is dated as the late Middle Jurassic, ca. 165 Ma (Ren et al. 1995, 2002, Shen et al. 2003, Chen et al. 2004, Ji et al. 2006, Gao and Ren 2006, Huang et al. 2006, Wang et al. 2013). Based on a combination of forewing characters: both R 1 and Rs 1 with two branches, 1A reaching posterior margin of wing distad of the forking of Rs from R 1, and no crossveins or only one crossvein between veins 1A and 2A, we erect a new genus Jurassipanorpa with two new species.

Materials and methods
This study is based on four fossil specimens collected from the late Middle Jurassic Jiulongshan Formation at Daohugou Village of Ningcheng County in Inner Mongolia, China. All type specimens are housed in the fossil insect collection of the Key Laboratory of Insect Evolution & Environmental Changes, College of Life Sciences, Capital Normal University, Beijing, China (CNUB; Dong Ren, Curator).
The specimens were examined and photographed using a Leica MZ12.5 dissecting microscope with a Leica DFC 500 digital camera and illustrated with the aid of a drawing tube attachment. The line drawings were drawn by Adobe Photoshop CS5. We use the venational nomenclature of Willmann (1989).
Type species. Jurassipanorpa impunctata Ding, Shih & Ren, sp. n. Other included species. Jurassipanorpa sticta Ding, Shih & Ren sp. n. Diagnosis. In forewing, Sc reaching the anterior margin near or beyond the middle of the wing; both R 1 and Rs 1 with two branches; 1A reaching posterior margin distad of the forking of Rs from R 1 ; 3 anal veins present; one crossvein between Cu 1 and Cu 2 and between 1A and 2A respectively.
Remarks. We assigned this genus to Panorpidae mainly based on the following characters: (1) head capsule with prolonged downward mouthparts; (2) slender wings and forewing slightly larger than hind wing with similar veins; (3) forewing Rs with five branches; (4) forewing M with four branches; (5) forewing Cu 1 not fused with M basally, one crossvein between M 4 and Cu 1 ; and (6) hind wing Rs with five and M with four branches as those of forewing. Etymology. From the Latin impunctata, meaning no spots, referring to the fact that no spots and fasciae on all wings.
Paratype. CNU-MEC-NN-2013012 P/C, sex unknown, with well-preserved legs, but four wings overlapping almost entirely and abdomen partially preserved.
Diagnosis. On both fore-and hind wings, Rs 1+2 shorter than Rs 1a+1b , Rs 1+2 shorter than Rs 3+4 , Rs and M forking at the same level and no spots or fasciae.
Description. Mainly based on Holotype, unless indicated as paratype. A wellpreserved female adult fossil. Body 12 mm long. Forewing and hind wing overlapping almost entirely, but most of veins discernible. Thorax and abdomen preserved, but head poorly preserved. Legs poorly preserved, with only few fragments (Figs 1A, 2A, 2C-F). Thorax: In dorsal view, 2.9 mm long, two setae on pronotum as preserved. Pronotum, mesonotum, metanotum clearly discernible. Meso-and metanotum about the same size; larger than pronotum.
Abdomen: In dorsal view, 9 mm long, tapering apically, with eleven visible segments; segments IX-XI more slender and shorter than segments II-VI. Cerci not preserved. Sterna visible in segments II-VI.
Legs: Densely covered with short setae, two long tibial spurs preserved in a mid leg, one tibial spur preserved in a fore leg and two hind legs in paratype (Figs 1C, 2B).
Wings: Venation similar to venation of Panorpa. Forewing (Figs 1A, 2A, B, C, D, F) 14 mm long with a maximal width of 4 mm, longer than the abdomen; Sc terminating at anterior margin near the middle of the wing; one distally located crossvein between Sc and R 1 ; R 1 long, branching and curving around pterostigma; one crossvein present between R 1 and Rs 1 ; Rs with five branches; Rs 1 forking into Rs 1a and Rs 1b ; Rs 1 and Rs 3+4 forking nearly at the same level; Rs 1+2 forking proximad of Rs 3+4 forking; one crossvein between Rs 3+4 and M 1+2 ; Rs and M forking at the same level; M with four branches; M 3+4 shorter than M 1+2 ; Cu 1 not fusing with M basally; one crossvein present between Cu 1 and Cu 2 ; 1A long, reaching posterior wing margin beyond the forking of Rs from R 1 ; one crossvein between 1A and 2A; 2A and 3A long, one crossvein between 2A and 3A; long and robust setae ranging from 0.09 to 0.17 mm in length, present on veins 1A, 2A and 3A (Figs 1B, D, 2D, F). Hind wing (Figs 1A, 2A, E), 12.3 mm long with a maximal width of 3.9 mm, smaller than forewing distinctly, of similar shape and veins; Sc short, reaching anterior wing margin before one-half wing length; one crossvein present between Sc and R 1 ; R 1 without forking; Rs with five branches; Rs and M forking at almost the same level; one crossvein present between R 1 and Rs 1 ; Rs 1 forking into Rs 1a and Rs 1b ; one crossvein between Rs 1b and Rs 2 ; Rs 2 without forking; one crossvein between Rs 2 and Rs 3 ; Rs 1+2 forking proximad of Rs 3+4 forking; one crossvein between Rs 3 and Rs 4 ; M 1+2 forking proximad of Rs 3+4 forking; one crossvein between Rs 3+4 and M 1+2 and one crossvein between Rs 4 and M 1 ; M with four branches; one crossvein between M 1 and M 2 ; M 3+4 shorter than M 1+2 ; one crossvein between M 2 and M 3 and between M 3 and M 4 respectively; Cu 1 coalesced with M basally; one crossvein between M 4 and Cu 1 ; no crossveins between anal veins. Etymology. From the Greek stiktos, meaning spotted, referring to various spots and fasciae on wings.
Diagnosis. On both fore-and hind wings, Rs 1+2 longer than Rs 1a+1b and Rs 1+2 longer than Rs 3+4 . Rs and M forking at the same level on forewing but Rs forking proximad of M forking on hind wing. All wings with scattered dark spots and fasciae.
Description. Mainly based on Holotype, unless indicated as paratype. A wellpreserved adult fossil, sex unknown. Right forewing and hind wing nearly overlapping entirely, but most veins discernible, left forewing and right wings partially overlapping, left hind wing well preserved (Figs 3A, B, 4A).
Head: Head capsule with prolonged downward mouthparts as modern panorpids. Compound eyes large and oval; ocelli untraceable; antennae filiform, with 25 segments as preserved.
Legs: Densely covered with short setae; one mid leg not preserved; coxae and trochanters of all legs not preserved; femur and tibia long; two long tibial spurs present on a fore leg, one tibial spur present on a hind leg and one of them incomplete on a mid leg.
Abdomen: Indiscernible. Wings: Forewing, 11 mm long with a maximum width of 3.9 mm, with scattered dark spots and fasciae (Figs 3A-C, 4A, C, E) with a different pattern from those of extant Panorpidae. Sc long, reaching anterior wing margin beyond one-half of wing length; one crossvein between Sc and R 1 located nearly of mid-length of Sc; R 1 long with two branches; one crossvein between R 1 and Rs 1 ; Rs with five branches, originating from R 1 nearly basal 1/3 of forewing length; Rs 1 forking into Rs 1a and Rs 1b ; one crossvein between Rs 1b and Rs 2 ; two crossveins between Rs 2 and Rs 3 ; Rs 1+2 forking distad to Rs 3+4 forking; one crossvein between Rs 3 and Rs 4 ; Rs and M forking at almost the same level; one crossvein between Rs 4 and M 1 ; M with four branches; one crossvein between M 1 and M 2 ; M 3+4 shorter than M 1+2 ; one crossvein between M 2 and M 3 ; Cu 1 not fusing with M basally, but joining M 4 by a oblique crossvein; Cu 1 fusing with Cu 2 basally and one crossvein between Cu 1 and Cu 2 ; 1A long, reaching posterior wing margin distad to the origination of Rs from R 1 ; 2A and 3A short; long and robust setae ranging from 0.15 to 0.38 mm in length, present on veins 1A, 2A and 3A of holotype and paratype (Fig. 4E, F). Left hind wing extended, right hind wing covered by the right forewing, incomplete; hind wing 9 mm long with a maximal width of 3.2 mm, smaller than forewing distinctly, of similar shape and veins (Figs 3A, B, 4A, D); but fasciae much reduced. Sc short, reaching anterior wing margin beyond one-half of wing length; one crossvein between Sc and R 1 ; R 1 long without forking; Rs with five branches; Rs 1 forking into Rs 1a and Rs 1b ; one crossvein between Rs 1b and Rs 2 ; Rs 1 shorter than Rs 1+2 ; one crossvein between Rs 2 and Rs 3 ; Rs 1+2 forking distad to Rs 3+4 forking; one crossvein between Rs 3 and Rs 4 ; M furcating distad to the Rs forking; one crossvein between Rs 4 and M 1 ; M with four branches; one crossvein between M 2 and Comparison. J. sticta sp. n. is differentiated from J. impunctata gen. et sp. n. by the following characters: (1) J. sticta with various spots and fasciae (vs. J. impunctata without spots and fasciae); (2) Rs 1+2 longer than Rs 1a+1b (vs. Rs 1+2 shorter than Rs 1a+1b ); (3) Rs 1+2 longer than Rs 3+4 (vs. Rs 1+2 shorter than Rs 3+4 ) (4) Rs and M forking at the same level on forewing, but Rs furcating proximad of M forking on hind wing (vs. Rs and M forking at the same level on both fore-and hind wing).

Discussion
In the vast insect fossil collection at the Capital Normal University (> 250,000 fossil insect specimens), we have collected only four panorpid fossils so far from the Daohugou locality. Informal survey of the Mecoptera collection indicates that specimens of Nannochoristidae are abundant, followed by many specimens of Orthophlebiidae, Bittacidae, and Cimbrophlebiidae, then, low numbers of Choristopsychidae, Mesopsychidae, Aneuretopsychidae, Pseudopolycentropodidae, and Eomeropidae, while very rare for Panorpidae. It is interesting to note that the rarity of Panorpidae during the Middle Jurassic of northeastern China is in contrast to their dominance in the Recent world fauna of Mecoptera (about 66% of all extant species).
Described fossil records of the Panorpidae in Mesozoic are extremely rare. Up to now, only one species, Solusipanorpa gibbidorsa Lin, 1980, has been described. However, we consider the holotype of S. gibbidorsa as not sufficiently preserved to be attributed to Panorpidae nor to any other family, and regard S. gibbidorsa as Mecoptera incertae sedis. Eight species in two genera: Panorpa Linnaeus, 1758, and Baltipanorpa Krzemiński, 2012, have been reported from the Eocene and Oligocene, however Carpenter stated that "Panorpa rigida Scudder, from the Florissant shales, is too incompletely preserved to permit even family classification." and "Panorpa arctiiformis Cockerell, also from the Florissant shales, is undoubtedly a member of the family Panorpidae, but I have not seen the type specimen and there is nothing in the description to indicate its affinities." (Carpenter 1931, Carpenter 1954, Willmann 1989, Krzemiński and Soszyńska-Maj 2012, Archibald et al. 2013. Jurassipanorpa impunctata gen. et sp. n. and J. sticta sp. n. described in this study are the earliest fossil panorpids in the world hitherto. The holotypes of these two new species of Jurassipanorpa gen. n. are well-preserved, including both wings and most of the body. New information from these two new species enhances our understanding of the morphological characters of Panorpidae and diversity of Mecoptera during the late Middle Jurassic.
Based on studies of these two new species and documented species of other representative panorpids, we compare and summarize six key forewing characters in Table 1. A combination of the following characters enables us to distinguish the new genus from all other described genera of Panorpidae: (1) R 1 with two branches in  (Byers 1967, Cai et al. 2008, Ma and Hua 2011, Krzemiński and Soszyńska-Maj 2012, Zhong and Hua 2013. We found that the wing venation of this family is comparatively stable, that is, Sc not forking, Rs 2 , Rs 3 , Rs 4 without forking, and M with 4 branches. However, Rs 1 is rather variable, typically, Rs 1 has two branches, but, some with three branches such as Sinopanorpa, while three Mexican extant species Panorpa dividilacinia, P. mixteca, P. umbricola have only a single Rs 1 (Carpenter 1992, Bicha 2006, Cai et al. 2008. Most panorpids have M 4 bending basally in forewings, that is, M 3 is a straight branch while M 4 is derived from M 3 with a basal bending. However, this character is not obvious for some extant panorpids, such as Panorpa wangwushana Shen, 2004 (Huang et al. 2004). On the other hand, most panorpodids have M 3 bending basally in forewings, that is, M 4 is a straight branch while M 3 is derived from M 4 with a basal bending. However, Panorpodes colei Byers, 2005 is an exception to this typical panorpodid character (Byers 2005). J. impunctata gen. et sp. n. has M 4 bending basally in forewing (Figs 2A, C), but J. sticta sp. n. does not have obvious M 4 bending basally, nor M 3 bending basally (Figs 4A, C). Hence, we propose that M 4 or M 3 basal bending is variable in both Panorpidae and Panorpodidae.
All four specimens of J. impunctata gen. et sp. n. (Figs 1B, D, 2D, F) and J. sticta sp. n. (Figs 3C, E, 4E, F) have remarkable long and robust setae on anal veins of the forewings that are not known for any other described fossil or extant panorpid species. Unlike these of Jurassipanorpa gen. n., setae on veins of extant species of Panorpidae as well as of Mesozoic Orthophlebiidae are usually more dense, shorter and decumbent unidirectionally and look similar to microtrichia on the wing membrane (Tillyard 1933, Webb and Penny 1979, Whalley 1985, Whalley 1986). These setae of the new genus, with lengths ranging from 0.09 to 0.38 mm, are similar in appearance to the piliform scales, ranging from 0.12 to 0.21 mm in lengths, present on the hind wing veins of Akainalepidopteron elachipteron Zhang, Shih, Labandeira & Ren, 2013 of Lepidoptera (Zhang et al. 2013), or to robust bristles ("dinotrichia") on the basal anterior margin of forewings on the Recent Notiothauma reedi and fossil Tsuchingothauma shihi and Jurathauma simplex (Eomeropidae) (Crampton 1930, Ren and Shih 2005, Zhang et al. 2011. The wing scales have been used as a diagnostic character for Lepidoptera, while also found in some forewings of Trichoptera (Kristensen 1984, Grimaldi 1999, Zhang et al. 2013. However, it is unlikely that these setae are homologous to piliform scales because scales have not been reported for Panorpidae. Since these setae are lo-cated only on anal veins of the forewings while all pointing anteriorly, we hypothesized that they might have been used for wing coupling. But, we could not find any associated structures preserved on the anterior part of the hind wings on these specimens. Hence, the function of these setae remains enigmatic.