Systematic Entomology (2017), 42, 555–574 DOI: 10.1111/syen.12231 The phylogeny of lance lacewings (Neuroptera: Osmylidae) SHAUN L. WINTERTON1,JINGZHAO2, IVONNE J. GARZÓN-ORDUÑA1, YONGJIE WANG3 andZHIQI LIU2 1California State Collection of Arthropods, California Department of Food & Agriculture, Sacramento, CA, U.S.A., 2Department of Entomology, China Agricultural University, Beijing, China and 3College of Life Sciences, Capital Normal University, Beijing, China Abstract. The first phylogeny of the lacewing family Osmylidae is presented here based on a total evidence analysis of DNA sequences for multiple gene loci and mor- phology for representatives of almost all extant genera. Our phylogeny shows a basal dichotomy in the family, with subfamilies Protosmylinae, Spilosmylinae and Gumilli- nae comprising one lineage, and the other lineage including Osmylinae, Porisminae, Eidoporisminae, Kempyninae and Stenosmylinae. The status of Paryphosmylus Krüger and Lysmus Navás as members of Protosmylinae is affirmed as well as the placement of Gumillinae near Protosmylinae and Spilosmylinae. Our results suggest that Poris- minae, Eidoporisminae and Stenosmylinae evolved from a common ancestor, and their relationships, including likely paraphyly of Stenosmylinae, requires further assessment. Divergence time analysis revealed that the family originated during the Late Permian before the break-up of the supercontinent Pangaea and that present generic distributions are not due to Gondwanan biogeographic events. All major subfamily-level lineages were present by the end of the Triassic, in agreement with the rich Mesozoic-aged fossil record for the family. Introduction recently described from South America and Asia (Wang & Liu, 2009, 2010; Ardila-Camacho & Noriega, 2014; Martins et al., The lance lacewings (Neuroptera: Osmylidae) are a small 2016; Winterton & Wang, 2016). family of charismatic insects distributed today in all major The phylogenetic position of Osmylidae has traditionally biogeographical regions except the Nearctic (New, 1989a). been highly contentious. The family has been allied with They are medium to large lacewings with cryptically patterned various families within Neuroptera, but most recent authors wings and reticulated venation (Figs 1, 2A, B). The highly agree on a close relationship among Osmylidae, Nevrorthidae distinctive larvae (Fig. 2C–E) are generalist predators that have and Sisyridae, with all three placed towards the base of the spectacularly elongated, lance-like jaws, which they use to neuropteran phylogeny (Withycombe, 1925; Haring & Aspöck, impale their prey. Larvae of many species are in riparian habitats 2004; Aspöck & Aspöck, 2008; Winterton et al., 2010; Yang near freshwater streams, although members of some subfamilies et al., 2012; Wang et al., 2016). Based on mounting evidence (i.e. Stenosmylinae, Porisminae) are distinctly terrestrial and are from quantitative analyses of morphology, DNA sequences and typically found under bark in much drier habitats. Presently examples in the fossil record, it is clear that these three families there are at least 225 extant species described in around 26 arose early in lacewing evolution during the Late Permian genera (Kimmins, 1940; New, 1986a,1986b,1986c; Wang & and Early Triassic, although the actual relationships among Liu, 2009; S.L. Winterton, unpublished data), although the them are still unclear (Winterton et al., 2010; Yang et al., 2012; number of species is expected to increase, with new species Wang et al., 2016). Some authors have proposed Nevrorthidae present in collections. For instance, new species have been as the sister family to the rest of the order (e.g. Aspöck et al., 2001; Haring & Aspöck, 2004; Aspöck & Aspöck, 2008), but compelling evidence to the contrary has been forwarded using Correspondence: Shaun L. Winterton, California State Collection total evidence analyses of morphology and DNA sequence of Arthropods, California Department of Food & Agriculture, 3294 Meadowview Rd., Sacramento, California 95832-1148, U.S.A. data. These analyses suggest that the family Coniopterygidae E-mail: [email protected] are instead the sister family to the rest of the order, with © 2017 The Royal Entomological Society 555 556 S. L. Winterton et al. Fig. 1. Examples of living Osmylidae adults. (A) Gryposmylus pennyi Winterton & Wang (Protosmylinae) (Vietnam) (photograph © Stephen D. Gaimari); (B) Isostenosmylus sp. (Stenosmylinae) (Peru) (photograph © Steve Marshall); (C) Phymatosmylus caprorum Adams (Stenosmylinae) (Chile) (photograph © Steve Marshall); (D) Heterosmylus processus Dong, Xu, Wang, Jia & Liu (Protosmylinae) (China) (photograph © Jishen Wang); (E) Osmylus fulvicephalus Stephens (Osmylinae) (Spain) (photograph used under Creative Commons); (F) Oedosmylus latipennis Kimmins (Stenosmylinae) (Australia) (photograph © Shaun L. Winterton); (G) Porismus strigatus Burmister (Porisminae) (Australia) (photograph © Shaun L. Winterton). © 2017 The Royal Entomological Society, Systematic Entomology, 42, 555–574 Lance lacewing phylogeny 557 Fig. 2. Examples of living Osmylidae adults and larvae. (A) Kempynus incisus (McLachlan) (Kempyninae) (New Zealand) (photograph © Gil Wizen); (B) Thyridosmylus paralangi Wang, Winterton et Liu (Spilosmylinae) (China) (photograph © Shaun L. Winterton); (C) Kempynus sp. (larva) (Kempyninae) (Australia) (photograph © Kristi Ellington); (D) Isostenosmylus sp. (larva) (Stenosmylinae) (Brazil) (photograph © Enio Branco); (E) unidentified larvae (Stenosmylinae) (Australia) (photograph © Kristi Ellington). © 2017 The Royal Entomological Society, Systematic Entomology, 42, 555–574 558 S. L. Winterton et al. Nevrorthidae placed in a subsequent clade near the base of the Plethosmylus Krüger, Porismus McLachlan, Spilosmylus Kolbe, lacewing tree (Winterton et al., 2010; Yang et al., 2012; Wang Stenolysmus Kimmins, Stenosmylus McLachlan, Thaumatosmy- et al., 2016). lus Krüger and Thyridosmylus Krüger. Specimens suitable for Osmylidae is divided into nine subfamilies – Eidoporisminae, DNA sequencing were unavailable for Gumilla Navás, Eido- Gumillinae, Kempyninae, Mesosmylininae, Osmylinae, Poris- porismus Esben-Petersen, Sinosmylus Yang, Paryphosmylus minae, Protosmylinae, Spilosmylinae and Stenosmylinae Krüger, Clydosmylus New, Euporismus Tillyard and Euosmy- (Krüger, 1912–1915; New, 1989a) – although Mesosmylininae lus Krüger, although they were scored for morphology based are only known from fossils. Mesosmylininae comprise at least on pinned specimens and included in some analyses. The genus seven genera known from the Late Triassic to Mid-Cretaceous Lahulus Navás is known only from the original description and (e.g. Jepson et al., 2009, 2012; Khramov, 2014a,2014b). The was not included here. Little is discernible about this genus from extinct subfamily Epiosmylinae is considered a junior synonym the description by Navás (1930), although he did state a clear of Gumillinae (Lambkin, 1988; Wang et al., 2009a,2009b; similarity with the genus Hyposmylus Krüger, a genus subse- Khramov, 2014a,2014b). The putative sister family to Osmyl- quently found to be a synonym of Osmylus Latreille. The other idae is Archeosmylidae (Late Permian to Early Triassic) and genera known from India are Spilosmylus Kolbe, Thyridosmy- is differentiated based on several wing venation features, such lus Krüger, Lysmus Navás and Osmylus. We cannot immediately as a nonpectinately branched forewing CuP (Khramov, 2014a). deduce that Lahulus as a synonym of Osmylus as the male gen- Saucrosmylidae Ren & Yin (2003) was originally included italic drawing by Navás (1930) is unlike any other found in the as a subfamily in Osmylidae, but recently was elevated to family and it will require further examination to determine its family rank by Fang et al. (2015) as a possible sister family status as a valid genus. The genus Glenosmylus Krüger is consid- to Osmylidae (cf. Yang et al., 2012). Similarly, the subfam- ered a synonym of Thaumatosmylus Krüger, while Mesosmylus ily Cratosmylinae (comprising only the genus Cratosmylus Krüger and Grandosmylus Makarkin are considered synonyms Myskowiak et al.) was recently described in Osmylidae by of Osmylus and Parosmylus Needham, respectively. Myskowiak et al. (2015), but we consider that this subfamily Outgroups were selected based on recent phylogenetic esti- is more suitably placed in Nymphidae based on the same wing mates of the Neuroptera using morphology and DNA sequence venation characters presented by the authors. data (Winterton et al., 2010; Yang et al., 2012), including Few synoptic works on world Osmylidae have been published mitochondrial genomes and gene arrangement (Wang et al., since the important series of papers on the family by Krüger 2016); we selected representatives from the closely related (1912–1915), and those few treatments have focused only families Nevrorthidae (Austroneurorthus Nakahara, Nevrorthus on provincial faunas (e.g. Tjeder, 1957; New, 1983a,1983b, Costa), Sisyridae (Climacia McLachlan, Sisyra Burmeister) 1986a,1986b,1986c, 1988, 1991; Wang, 2010; Martins et al., and Coniopterygidae (Conwentzia Enderlein, Cryptoscenea 2016) or particular subfamilies and genera (Kimmins, 1940, Enderlein). 1942; Adams, 1969; Wang & Liu, 2009; Wang et al., 2011a; Ardila-Camacho & Noriega, 2014; Winterton & Wang, 2016). The proliferation of genera based on spurious characters by Morphology and terminology Krüger (1912–1915) and the rarity of specimens in collections mean that there are few publications