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Phylogeny of Pleasing Lacewings (Neuroptera: Dilaridae) with a Revised Generic Classification and Description of a New Subfamily

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Phylogeny of Pleasing Lacewings (Neuroptera: Dilaridae) with a Revised Generic Classification and Description of a New Subfamily Systematic Entomology (2017), 42, 448–471 DOI: 10.1111/syen.12225 Phylogeny of pleasing lacewings (Neuroptera: Dilaridae) with a revised generic classification and description of a new subfamily XINGYUE LIU1, HORST ASPÖCK2, SHAUN L. WINTERTON3, WEIWEI ZHANG4 andULRIKE ASPÖCK5,6 1Department of Entomology, China Agricultural University, Beijing, China, 2Institute of Specific Prophylaxis and Tropical Medicine, Medical Parasitology, Medical University (MUW), Vienna, Austria, 3California State Collection of Arthropods, Sacramento, CA, U.S.A., 4Three Gorges Entomological Museum, Chongqing, China, 5Naturhistorisches Museum Wien, Zweite Zoologische Abteilung, Vienna, Austria and 6Department of Integrative Zoology, University of Vienna, Vienna, Austria Abstract. The phylogeny of pleasing lacewings (Neuroptera: Dilaridae) is recon- structed for the first time based on morphological data using all fossil and extant genera. Accordingly, a revised generic classification of Dilaridae is proposed, with a new subfamily (i.e. Berothellinae subfam.n.) erected based on its remarkably differ- ent morphological features from the other dilarid subfamilies. A revision of all dilarid genera is presented, including descriptions of some little-known species from Asia and Mid-Cretaceous Burmese amber. New genera and species herein described include Berothella holzschuhi U. Aspöck, Liu & H. Aspöck, sp.n., Cretodilar burmanus Liu & Zhang, gen. et sp.n., Dilar cretaceus Liu & Zhang, sp.n., Neonallachius orientalis Liu, U. Aspöck & H. Aspöck, sp.n. and Neonallachius thailandicus Liu & Winterton, sp.n. Two new combinations, i.e. Neonallachius krooni (Minter, 1986), comb.n. and Neonallachius ponomarenkoi (Zakharenko, 1991), comb.n., are proposed. Evolution- ary patterns of some important characters and the historical biogeography of Dilaridae are also discussed. This published work has been registered in ZooBank, http://zoobank.org/urn:lsid: zoobank.org:pub:68836312-FBDC-4F9F-8516-2365F44596BF. Introduction 2010a,2010b; Randolf et al., 2014). However, recent molecular phylogenetic studies suggest that Dilaridae are instead the sis- Dilaridae, commonly called pleasing lacewings, are a small ter group of the clade including all lacewing families except family of distinctive neuropterans characterized by sexually for Coniopterygidae, Nevrorthidae, Sisyridae and Osmylidae dimorphic antennae (generally unipectinate in the male and (Winterton et al., 2010; Wang et al., 2016). Currently, Dilaridae filiform in the female), the presence of three setose tuber- comprise one extinct and four extant genera with 94 species, cles on the head and a narrowly elongate female ovipositor subdivided into two subfamilies, i.e. Dilarinae and Nallachi- (Fig. 1). The family is distributed in most zoogeographic regions inae (Oswald, 1998; Engel, 1999; Zhang et al., 2016). In the but is surprisingly lacking in the Australian region (Oswald, classification given by Oswald (1998), only Nallachius Navás 1998). The family was originally considered to form a mono- belongs to Nallachiinae, while the remaining extant genera, i.e. phylum together with Berothidae, Rhachiberothidae and Man- Berothella Banks, Dilar Newman and Neonallachius Nakahara, tispidae as ‘the dilarid clade’ based on morphological evidence are placed in Dilarinae, which also include the extinct genus (Aspöck et al., 2001; Aspöck & Aspöck, 2008; Beutel et al., Cascadilar Engel from Eocene Baltic amber. The biology of Dilaridae is poorly documented. The larvae are known for only seven species (Gurney, 1947; MacLeod Correspondence: Xingyue Liu, Department of Entomology, China Agricultural University, Beijing 100193, China. E-mail: & Spiegler, 1961; Ghilarov, 1962; Monserrat, 1988a, 2014; [email protected] Minter, 1992). Nallachius larvae (Fig. 1D) are considered to 448 © 2016 The Royal Entomological Society Phylogeny of the family Dilaridae 449 Fig. 1. Living pleasing lacewings (Dilaridae). (A) Dilar nobilis Zhang, Liu, Aspöck & Aspöck, male (photograph by Jiangyun Wang); (B) Dilar sp., female (photograph by Weiwei Zhang); (C) Nallachius americanus (McLachlan), male (photograph by Matt Bertone); (D) Nallachius americanus (McLachlan), larva (photograph by Matt Bertone). be predaceous and are subcorticolous on dead trees (Gurney, genera, the intergeneric phylogeny of Dilaridae has never been 1947; MacLeod & Spiegler, 1961), while the larvae of Dilar are studied. reported from soil samples (Ghilarov, 1962; Monserrat, 2014). It In this paper, we provide a revision of all dilarid genera, is of interest that the adult of Berothella holzschuhi sp.n. herein with descriptions of some little known species from Asia. We described emerged from a piece of wood. Typically nocturnal, erect a new subfamily of Dilaridae (Berothellinae subfam.n.) adult dilarids can be collected at lights, while some species are that displays remarkably different morphological characters also active in the daytime (Monserrat, 2014). compared with the other dilarid subfamilies. We also clarify The taxonomy of Dilaridae has been intensively studied the taxonomic status of Neonallachius and some Nallachius since the early 1900s, with a monograph of the family by species previously described from the Old World. Based on Navás [1909a] (1908-1909), although the descriptions and the morphological characters, a phylogeny among all extant illustrations contained therein are of little value for identifi- and fossil genera of Dilaridae is reconstructed. Accordingly, a cation. After the 1950s, a series of works on Dilaridae were revised classification system of Dilaridae and biogeographical published, including a review of Nallachius (Adams, 1970), implications are also presented. revisions of Asian and European Dilar (Aspöck & Aspöck, 1967, 1968; Aspöck et al., 1980; Monserrat, 1988a,1988b; Materials and methods Oswald & Schiff, 2001), and a world catalogue of the family (Oswald, 1998). Very recently, the knowledge of Dilaridae Exemplar sampling has increased significantly through the works of Machado & Rafael (2010), Zhang et al. (2014a,2014b,2014c, 2015, Specimens of extant dilarids are deposited in the Entomo- 2016), Monserrat (2014) and Aspöck et al. (2015). How- logical Museum, China Agricultural University, Beijing, China ever, genera of Dilaridae (e.g. Berothella and Neonallachius) (CAU); the Natural History Museum, London, U.K. (BMNH); remain poorly known. Moreover, despite the small number of the Museum für Naturkunde, Berlin, Germany (MFN); the © 2016 The Royal Entomological Society, Systematic Entomology, 42, 448–471 450 X. Liu et al. Table 1. Character matrix. 000000000111111111 1 22222 2222233 123456789012345678 9 01234 5678901 Nipponeurorthus damingshanicus 000–00000100000010 0 00000 10000–0 Sisyra terminalis 000–00100100000010 0 –001– –0000–0 Gumilla adspersus 000–00000000000010 0 000? ? 00000–0 Cyrenoberotha penai 000–00100100010010 0 000? ? 00000–0 Berothella holzschuhi 110–1100011012110– – 0011– –00010? Berothella phantoma 110–1100011012110– – 1001– –00010? Berothella pretiosa 110–1100011012110– – 0011– –00010? Cascadilar eocenicus 1210111201110?1–0– – ? ??? ? ? ?????? Cretodilar burmanus 120001010211??1–0– – ? ??? ? ? ?????? Dilar harmandi 120011020111011–0– – 1001– –000111 Dilar nevadensis 120011020111011–0– – 1001– –000111 Nallachius americanus 221111000100010112 0 00001 00000–1 Nallachius pulchellus 221111000100010112 0 00001 00000–1 Neonallachius krooni 221011101200010110 1 01000 11110–1 Neonallachius orientalis 221011001201010110 1 01000 11110–1 Neonallachius ponomarenkoi 221011001200010111 1 0101– 01110–1 Neonallachius thailandicus 221011001200010111 1 0001– 01100–1 Museum of Comparative Zoology, Harvard University, Cam- Phylogenetic analysis bridge, MA, U.S.A. (MCZ); the Zoological Institute, Russian Academy of Sciences, St.Petersberg, Russia (ZIN); the Califor- The present phylogenetic analysis aims to reconstruct the rela- nia State Collection of Arthropods, California Department of tionships among genera of Dilaridae. We included species of all Food and Agriculture, Sacramento, CA, U.S.A. (CDFA); the extant and fossil genera of the family. For genera with a small Essig Museum of Entomology, University of California, Berke- number of species, we included all species except for the type ley, CA, U.S.A (EMEC); and the Collection of Hubert and species of Neonallachius (i.e. Neonallachius annandalei Naka- Renate Rausch, Scheibbs, Austria (CHRR). hara), which was not available for study. For Dilar, containing The Burmese amber with inclusions of dilarids investigated a relatively large number of species, we selected two represen- here originated from the Hukawang Valley in Tanai Town- tative species for the analysis [i.e. Dilar harmandi (Navás) and ship, Myitkyina District of Kachin State, Myanmar. The age Dilar nevadensis Rambur], while all the Old World species of Nallachius of this deposit has been dated at 98.8 ± 0.6 million years old previously described were included together with two Neotropical Nallachius species [i.e. Nallachius americanus (ma) (Albian-Cenomanian) using Uranium-lead (U-Pb) dating (McLachlan) and Nallachius pulchellus (Banks)]. In total, we of zircons from the volcaniclastic matrix of the amber (Shi included 13 ingroup taxa. For outgroups, we included Nip- et al., 2012). Type specimens of new Burmese amber dilar- poneurorthus damingshanicus Liu, Aspöck & Aspöck (Nevror- ids are currently housed in the Entomological Museum, China thidae), Sisyra terminalis Curtis (Sisyridae), Gumilla adsper- Agricultural University
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