New Fossil Lepidoptera (Insecta: Amphiesmenoptera) from the Middle Jurassic Jiulongshan Formation of Northeastern China
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New Fossil Lepidoptera (Insecta: Amphiesmenoptera) from the Middle Jurassic Jiulongshan Formation of Northeastern China Weiting Zhang1,6, Chungkun Shih1, Conrad C. Labandeira1,2,3, Jae-Cheon Sohn2,3,4, Donald R. Davis4, Jorge A. Santiago-Blay2,5, Oliver Flint4, Dong Ren1* 1 College of Life Sciences, Capital Normal University, Beijing, China, 2 Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, Distirict of Columbia, United States of America, 3 Department of Entomology and BEES Program, University of Maryland, College Park, Maryland, United States of America, 4 Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia, United States of America, 5 Department of Crop and Agroenvironmental Sciences, University of Puerto Rico Mayagu¨ez, Puerto Rico, United States of America, 6 Geoscience Museum, Shijiazhuang University of Economics, Shijiazhuang, China Abstract Background: The early history of the Lepidoptera is poorly known, a feature attributable to an inadequate preservational potential and an exceptionally low occurrence of moth fossils in relevant mid-Mesozoic deposits. In this study, we examine a particularly rich assemblage of morphologically basal moths that contribute significantly toward the understanding of early lepidopteran biodiversity. Methodology/Principal Findings: Our documentation of early fossil moths involved light- and scanning electron microscopic examination of specimens, supported by various illumination and specimen contrast techniques. A total of 20 moths were collected from the late Middle Jurassic Jiulongshan Formation in Northeastern China. Our principal results were the recognition and description of seven new genera and seven new species assigned to the Eolepidopterigidae; one new genus with four new species assigned to the Mesokristenseniidae; three new genera with three new species assigned to the Ascololepidopterigidae fam. nov.; and one specimen unassigned to family. Lepidopteran assignment of these taxa is supported by apomorphies of extant lineages, including the M1 vein, after separation from the M2 vein, subtending an angle greater than 60 degrees that is sharply angulate at the junction with the r–m crossvein (variable in Trichoptera); presence of a foretibial epiphysis; the forewing M vein often bearing three branches; and the presence of piliform scales along wing veins. Conclusions/Significance: The diversity of these late Middle Jurassic lepidopterans supports a conclusion that the Lepidoptera–Trichoptera divergence occurred by the Early Jurassic. Citation: Zhang W, Shih C, Labandeira CC, Sohn J-C, Davis DR, et al. (2013) New Fossil Lepidoptera (Insecta: Amphiesmenoptera) from the Middle Jurassic Jiulongshan Formation of Northeastern China. PLoS ONE 8(11): e79500. doi:10.1371/journal.pone.0079500 Editor: David Frayer, University of Kansas, United States of America Received June 6, 2013; Accepted September 17, 2013; Published November 22, 2013 Copyright: ß 2013 Zhang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This research was supported by the National Basic Research Program of China (973 Program) (grant 2012CB821906), National Natural Science Foundation of China (grants 31172143, 31230065, 31272352 and 41272006), Project of Great Wall Scholar and KEY project of Beijing Municipal Commission of Education (grants KZ201310028033), and the China Geological Survey (grant 1212011120115). Support for JCS was provided by the United States National Science Foundation’s Assembling the Tree of Life program, award 0531769, and the Maryland Agricultural Experiment Station. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction of the world’s fauna, following their evolution from the stem- group, the Amphiesmenoptera (Fig. 1A) [5], a major holometa- The Lepidoptera, or butterflies and moths, are one of the most bolan lineage comprising two distinctive insect orders, the speciose lineages of herbivores, currently including about 157,500 Lepidoptera and the Trichoptera. The taxonomic boundary described species encompassing the four suborders of Zeugloptera, between Lepidoptera and Trichoptera is often obscured in their Aglossata, Heterobathmiina, and Glossata [1]. In contrast to the early fossil record [3], attributable to an overall morphological documented paleodiversity of otherdiverse insect lineages [2], the similarity and presence of few apomorphic characters visible in Lepidopteran fossil record is depauperate [3]. Only two extant fossil specimens [5]. suborders, Zeugloptera and Glossata, and an extinct suborder, Because of the rarity of Mesozoic Lepidoptera, only 24 genera, Eolepidopterigina proposed by Rasnitsyn [4], are represented in of which two are extant, have been described from the Mesozoic the fossil record. Speciosity of the basal lepidopteran lineages is (Table 1) [3,6–8]. In addition, undescribed Mesozoic fossils have minimal in the fossil record, as in the extant fauna. This may be a been reported, including unequivocal Lepidoptera larvae [5,9], consequence of the Lepidoptera once constituting a minor group and other evidence such as unequivocal or possible Lepidoptera PLOS ONE | www.plosone.org 1 November 2013 | Volume 8 | Issue 11 | e79500 New Middle Jurassic Lepidoptera Figure 1. A stem-group amphiesmenopteran, lepidopterans, and a trichopteran. (A), A stem-group amphiesmenopteran, Necrotaulius tener, modified after Grimaldi and Engel [5]. (B-F), Lepidopteran forewings. (B), Archaeolepis mane, from Grimaldi and Engel [5]. (C), Forewing of an Early Jurassic Germany lepidopteran, from Grimaldi and Engel [5]. (D), Undopterix sukatshevae, modified after Skalski [10]; the red arrowhead showing Rs3+4 furcation beyond the M1+2 furcation. (E), Netoxena nana, modified after Martins-Neto [24]; red line indicates a single-Y configuration. (F), Mesokristensenia sinica, modified after Huang et al. [25]. (G), A trichopteran, Juraphilopotamus lubricus, modified after Gao et al. [43]. doi:10.1371/journal.pone.0079500.g001 wing scales [10–12] and unequivocal Lepidoptera leaf mines assigned most of these to the Lepidoptera on the basis of the 3- [13,14]. Mesozoic fossil Lepidoptera are principally assigned to branched M vein and the presence of scales on the forewings. two extinct families, the Eolepidopterigidae and the Mesokristen- These fossils overwhelmingly are represented by wings. A seniidae, and an extant family, the Micropterigidae, the latter representative forewing is shown in Fig. 1C, indicating a M with considered the most basal extant lineage of Lepidoptera [15,16]. 3 branches and the M1, separated from the M2 at an angle of In addition, Kozlov erected an extinct family, the Undopterigidae about 70 degrees, and sharply angulate at the junction with to accommodate Undopterix Skalski, 1979 [10], but its phylogenetic crossvein r–m. Additionally, a forewing of Undopterix sukatshevae, placement is uncertain. within the Undopterigidae [23], is shown in Fig. 1D, as is a The earliest unequivocal lepidopteran fossil hitherto established forewing of Netoxena nana in the Eolepidopterigidae [3,24], in is Archaeolepis mane Whalley, 1985 (Fig. 1B) from the Early Jurassic, Fig. 1E. Huang et al. [25] described Mesokristensenia sinica in the about 190 million years ago (Ma), of Dorset, England [5,18,19]. Mesokristenseniidae, the forewing of which is shown in Fig. 1F. The next, more recent, early fossils are eight non-monophyletic For comparison, the forewing of a trichopteran, Juraphilopotamus genera, dated to approximately 180 Ma, from the uppermost Lias lubricus Wang, Zhao & Ren, 2009 [17], is shown in Fig. 1G. of Dobbertin, Germany [5], which were described by Handlirsch Recently, we collected 20 well-preserved, nearly complete fossil as Necrotauliidae. However, Ansorge [21,22] disputed the lepidopterans from the Jiulongshan Formation at Daohugou necrotaulid affiliations of the Handlirsch’s specimens and other Village, Shantou Township, Ningcheng County, Inner Mongolia, well-preserved wings from the Grimmen locality of Germany, and in China. This deposit was radiometrically dated by 40K/40Ar at PLOS ONE | www.plosone.org 2 November 2013 | Volume 8 | Issue 11 | e79500 New Middle Jurassic Lepidoptera Table 1. Known fossil records of Mesozoic Lepidoptera. Suborder Family Genus Species Epoch Country Reference ? Archaeolepidae Archaeolepis Whalley, 1985 A. mane Whalley, 1985 J1 United Kingdom [18] Eolepidopterigina Eolepidopterigidae Eolepidopterix Rasnitsyn, 1983 E. jurassica Rasnitsyn, 1983 J3 Kazakhstan [4] Eolepidopterigina Eolepidopterigidae Palaeolepidopterix Kozlov, 1989 P. aurea Kozlov, 1989 J3 Kazakhstan [40] Eolepidopterigina Eolepidopterigidae Daiopterix Skalski, 1984 D. rasnitsyni Skalski, 1984 K1 Russia [23] Eolepidopterigina Eolepidopterigidae Daiopterix Skalski, 1984 D. olgae Kozlov, 1989 K1 Russia [40] Eolepidopterigina Eolepidopterigidae Netoxena Sohn, 2012 N. nana (Martins-Neto, 1999) K1 Brazil [24,52] Eolepidopterigina Eolepidopterigidae Undopterix Skalski, 1979 U. sukatshevae Skalski, 1979 K1 Russia [10] Eolepidopterigina Eolepidopterigidae Undopterix Skalski, 1979