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Phylogeny and Historical Biogeography of Silky Lacewings (Neuroptera: Psychopsidae)

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Phylogeny and Historical Biogeography of Silky Lacewings (Neuroptera: Psychopsidae) Systematic Entomology (2018), 43, 43–55 DOI: 10.1111/syen.12247 Phylogeny and historical biogeography of silky lacewings (Neuroptera: Psychopsidae) DEON K. BAKKES* , MERVYN W. MANSELLand CATHERINE L. SOLE Department of Zoology and Entomology, University of Pretoria, Hatfield, South Africa Abstract. Psychopsidae (silky winged lacewings) are a small family of Neuroptera characterized by broad hirsute wings that impart a physical resemblance to moths. The fossil record includes many psychopsid-like taxa from the Late Triassic to Early Oligocene from all major continents. Extant species have a disjunct, tripartite distribution comprising Afrotropical, Southeast Asian and Australian regions that is significant to historical biogeography. Two subfamilies are currently recognized: Zygophlebiinae in the Afrotropics, and Psychopsinae in Australia and Southeast Asia. This study explores phylogeny and historical biogeography of Psychopsidae, using data from biogeography, comparative morphology and molecular sequences (16S, 18S, CAD, COI). Our results show that: (i) the morphological phylogeny is incongruent with molecular data; (ii) Afrotropical Silveira Navás represent a separate lineage that warrants placement in its own subfamily; (iii) the family originated in Pangea; and (iv) the present genus level distribution resulted from two vicariance events associated with Gondwanan fragmentation. Introduction species are known to live under the bark of myrtaceous trees, preying on Microlepidoptera (Tillyard, 1919b; Tjeder, 1960). Psychopsidae Handlirsch (Neuroptera) are a small family of Adult females have a specialized oviposition strategy that lacewings, comprising about 26 extant species in five genera involves grinding a substrate of sand or plant material with the worldwide (Oswald, 1993). Members are characterized by toothed side of the gonocoxite stylus. The substrate is then trans- broad moth-like wings with a parallel triplet-vein formation ferred to the abdominal chamber and used to coat eggs, probably comprising the subcostal, radial and radial sector veins col- for camouflage and minimizing desiccation. Eggs are laid singly lectively known as the vena triplica (Tillyard, 1922a). Extant during flight (Tjeder, 1960; New, 1988; Oswald, 1993). species manifest a disjunct, tripartite distribution between the Fossil Psychopsidae manifest considerable disparity across a Afrotropical, Australian and Southeast Asian regions. The rich fossil record (Ren & Engel, 2008). The Kalligrammatidae Afrotropical fauna (Fig. 1A–D, G, H) comprises three gen- Handlirsch, Aetheogrammatidae Ren & Engel and Osmylopsy- era – Cabralis Navás, Silveira Navás and Zygophlebius Navás chopidae Martynova (syn. Brongniartiellidae Martynova; see in Zygophlebiinae Navás – while Australian and Southeast Peng et al., 2016) are extinct families that share the closest rela- Asian fauna have only one genus each – Psychopsis New- tionship with extant Psychopsidae (Fig. 2 and Andersen, 2001). man in Australia (Fig. 1E, F) and Balmes Navás in Southeast Makarkin (2010) placed these within Psychopsoidea Handlirsch Asia – both in Psychopsinae Handlirsch. Larvae have been which, in turn, is sister to Myrmeleontiformia (Withycombe, found in leaf debris surrounding trees, and two Australian 1925; Mansell, 1992; Haring & Aspöck, 2004; Grimaldi & Correspondence: Deon K. Bakkes and Catherine L. Sole, Department Engel, 2005; Beutel & Pohl, 2006; Badano et al., 2016). Psy- of Zoology and Entomology, University of Pretoria, Private Bag X chopsidae (s.s.) comprise fossil Triassopsychopsinae Tillyard 20, 0028, Hatfield, South Africa. E-mail: [email protected]; along with extant taxa, and are considered a distinct lineage of [email protected] Psychopsoidea united by a broad costal space (Makarkin, 1997; *Present address: Gertrud Theiler Tick Museum, Epidemiology, Andersen, 2001; Lambkin, 2014). Within Psychopsidae (s.s.), Parasites & Vectors, Agricultural Research Council – Onderstepoort extant lineages have an abruptly closing vena triplica distally, Veterinary Research, Pretoria 0110, South Africa. while extinct Baisopsychops Makarkin and Triassopsychops © 2017 The Royal Entomological Society 43 44 D. K. Bakkes et al. Fig. 1. Diversity of Psychopsidae. (A) Silveira marshalli (McLachlan, 1902) (photo: Wynand Uys). (B) Cabralis cns (photo: Hennie de Klerk). (C) Silveira occultus Tjeder, 1960 (photo: Peter Duelli). (D) Zygophlebius leoninus Navás, 1910 (photo: Wynand Uys). (E) Psychopsis sp. Larva (photo: Shaun Winterton). (F) Psychopsis insolens (photo: Shaun Winterton). (G) Cabralis cns larva (photo: Peter Duelli). (H) Silveira rufus (photo: Penni Warncke). [Colour figure can be viewed at wileyonlinelibrary.com]. © 2017 The Royal Entomological Society, Systematic Entomology, 43, 43–55 Silky lacewing evolution 45 Tillyard (Triassopsychopsinae) have this termination gradually Material and methods tapering (Fig. 2). This supports division between all extant subfamilies, and extinct Triassopsychopsinae (Tillyard, 1922b; Sampling and taxon selection Makarkin, 1997; Andersen, 2001). Fossil Propsychopsis Krüger are an exception, with a tapering vena triplica similar to Taxa used in this study are listed alongside voucher and Gen- Triassopsychops, but with similar adult characters to extant Bank accession numbers in Table S1. Twenty-three Psychopsi- dae specimens were collected either by hand-netting or at mer- Balmes (MacLeod, 1970), and similar larval characters to cury vapour light traps, preserved in absolute ethanol and placed extant Psychopsis (Tillyard, 1919a; MacLeod, 1970). These into −20∘C storage. Sequences for Psychopsis margarita Till- similarities place Propsychopsis near Balmes in Psychopsinae yard were obtained from GenBank. The sample set represents all (Andersen, 2001). extant genera and all major biogeographic regions of Psychop- Psychopsidae have previously been considered closely related sidae. Afrotropical species were sampled extensively, although to, or the sister family of, Nemopteridae Burmeister based fresh material of Zygophlebius zebra (Brauer) was not collected. on assessments of adult and larval morphology (Withycombe, Australian and Southeast Asian faunas were represented by two 1925; Aspöck et al., 2001; Aspöck & Aspöck, 2008). Recent species from each genus. Nine outgroup taxa were selected studies, however, which focused holistically on Neuropterida based on the phylogeny of Winterton et al. (2010) according to using molecular and morphological characters, have shown that sister clade sampling (Hillis, 1998). The final dataset comprised Psychopsidae are closer to Nymphidae Rambur, placing Psy- 33 individuals representing 13 Psychopsidae species. Specimens chopsidae as sister to all other Myrmeleontiformia (Winterton collected by the authors are housed in the South African National et al., 2010; Wang et al., 2016). Extant species are divided into Collection of Insects, Pretoria (SANC), with accession num- Zygophlebiinae and Psychopsinae based on a cladistic analy- bers from the Palpares Relational Database (Mansell & Kenyon, sis of 60 morphological characters (Oswald, 1993). Psychopsi- 2002) as voucher numbers (Table S1). nae comprise Australian and Southeast Asian genera that appear closely related despite geographic distance (New, 1988; Oswald, 1993). Zygophlebiinae comprise all Afrotropical genera, with Morphological characters Cabralis and Zygophlebius closely related, and Silveira more pleisiomorphic and distinct (Oswald, 1993). Ninety-eight morphological characters describing adult mor- The historical biogeography of extant Psychopsidae was phology of males and females were scored for phylogenetic investigated by Oswald (1993) in an area cladogram test (Nel- analyses (Table S2). These characters include Oswald’s (1993) son & Platnick, 1981; Humphries & Parenti, 1986) that was dataset, although several were refined to improve states specific formulated to account for Balmes in Southeast Asia. This test to Afrotropical taxa. New characters specific to Afrotropical found most support for an Australian dispersal route based on species were added. All morphological characters were treated the close relationship between Balmes and Psychopsis,and as unordered, with gap or unknown characters coded as ‘−’or indicated that Balmes underwent northwestern dispersal from ‘?’ respectively. Australia along the Malay Archipelago to mainland Asia. The second-most supported hypothesis was Indian drift, postulating that Balmes arrived in Southeast Asia via tectonic move- DNA extraction, sequencing and alignment ment of India towards Asia after Gondwanaland fragmented Four genes were selected for sequencing to represent a (Ali & Aitchison, 2008). Oswald (1993) also considered range of mutational rate changes over time, maximizing phy- hypotheses for Balmes as a Laurasian relic and an African logenetically informative data, and testing whether gene trees disperser, but these were rejected due to the close relationship reflect the species tree by congruence (Doyle, 1992; Maddi- between Balmes and Psychopsis (Oswald, 1993). This delimited son, 1997; Nichols, 2001). These comprised two ribosomal Psychopsidae historical biogeography under two competing genes (16S rDNA and 18S rDNA) and two protein-encoding hypotheses. Uncertainty remains, however, due to the limita- genes [mitochondrial cytochrome oxidase I (COI) and nuclear tion of not including timing data in the area-cladogram test CPSase region of carbamoyl-phosphate synthetase-aspartate (Oswald, 1993).
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