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Origin and Transformation of the In-Flight Wing-Coupling Structure in Psocodea (Insecta: Paraneoptera)

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Origin and Transformation of the In-Flight Wing-Coupling Structure in Psocodea (Insecta: Paraneoptera) Title Origin and transformation of the in-flight wing-coupling structure in Psocodea (Insecta: Paraneoptera) Author(s) Ogawa, Naoki; Yoshizawa, Kazunori Journal of Morphology, 279(4), 517-530 Citation https://doi.org/10.1002/jmor.20785 Issue Date 2018-04 Doc URL http://hdl.handle.net/2115/75534 This is the peer reviewed version of the following article: "Origin and transformation of the in-flight wing-coupling structure in Psocodea (Insecta: Paraneoptera)."Journal of Morphology; 279(4) pp517-530 Apr 2018, which has been Rights published in final form at DOI:10.1002/jmor.20785. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions. Type article (author version) File Information 2018JMOR.pdf Instructions for use Hokkaido University Collection of Scholarly and Academic Papers : HUSCAP Page 1 of 45 Journal of Morphology 1 1 OGAWA 2 3 4 5 Origin and transformation of the in-flight wing-coupling structure in 6 7 8 Psocodea (Insecta: Paraneoptera) 9 10 11 12 Naoki OGAWA*, Kazunori YOSHIZAWA 13 14 15 Systematic Entomology, School of Agriculture, Hokkaido University, 16 17 Sapporo 060-8589, Japan 18 19 TEL: +81-11-706-2486 20 21 22 Fax: +81-11-706-2424 23 24 [email protected] 25 26 27 28 Short title: Wing coupling structure in ‘Psocoptera’ 29 30 31 32 33 34 35 ABSTRACT 36 37 38 Many four-winged insects have mechanisms that unite the fore- and 39 40 hindwings in a single plane. Such an in-flight wing coupling apparatus may 41 42 improve flight performance in four-winged insects, but its structure is 43 44 45 variable among different insect groups. The wings of bark lice (Insecta: 46 47 Psocodea: ‘Psocoptera’) also have an in-flight wing coupling apparatus, but 48 49 to date, its morphology has not been studied in detail. In this study, we 50 51 52 examined the wing-coupling structure in representative species of the three 53 54 suborders of bark lice (Trogiomorpha, Troctomorpha and Psocomorpha) and 55 56 inferred its origin and transformation. We conclude that the main 57 58 59 60 John Wiley & Sons Journal of Morphology Page 2 of 45 2 1 OGAWA 2 3 4 5 component of the psocodean wing coupling apparatus evolved once in the 6 7 common ancestor via modification of cuticular structures at the apex of the 8 9 10 forewing CuP vein. Morphological differences in components of the coupling 11 12 structures are phylogenetically informative at the intraorder level and 13 14 include an autapomorphy that characterizes Troctomorpha and a 15 16 17 synapomorphy that supports a sister relationship between Troctomorpha 18 19 and Psocomorpha. 20 21 22 23 24 INTRODUCTION 25 26 The evolution of insect wings and powered flight are cited as epochal events 27 28 in their history (Brodsky, 1994), and insect flight mechanisms have 29 30 31 attracted significant interest from functional and comparative biologists 32 33 (Wootton, 1992; Brodsky, 1994; Grodnitsky, 1995, 1999). Winged insects 34 35 usually have two pairs of (i.e., four) wings. Some four-winged insects, such 36 37 38 as dragonflies (Odonata) and locusts (Orthoptera), flap the fore- and 39 40 hindwings independently (Chapman, 2013), but this condition is rather 41 42 exceptional among insects, possibly because this mode is less efficient and 43 44 45 less stable (Pope, 1994). Loss of the thrust-generating function in either the 46 47 fore- or hindwing pair (i.e., dipterous flight) is more frequent; this occurs, for 48 49 example, in Diptera (true flies) and Strepsiptera (the twisted wing 50 51 52 parasites). The forewings of Coleoptera (beetles), the elytra, function to 53 54 protect the wings from external damage (Linz et al., 2016). The elytra are 55 56 sclerotized and held away from the body during flight, and they do not 57 58 59 60 John Wiley & Sons Page 3 of 45 Journal of Morphology 3 1 OGAWA 2 3 4 5 generate thrust. Complete loss of the capacity to generate thrust in either 6 7 the fore- or hindwing pair occurs in mayflies (Ephemeroptera), earwigs 8 9 10 (Dermaptera), crickets (Orthoptera), stick insects (Phasmida), scale insects 11 12 (Hemiptera), wasps (Hymenoptera), lacewings (Neuroptera), and moths 13 14 (Lepidoptera) (Grodnitsky, 1995). 15 16 17 The predominant flight mode in four-winged insects is functionally 18 19 two-winged flight (Grodnitsky, 1999). In such insects, the fore- and 20 21 hindwings are connected by an in-flight coupling apparatus. Grodnitsky 22 23 24 (1999) defined two coupling modes in the functionally two-winged insects: 25 26 wings that are coupled during the downstroke only (part-time coupling) and 27 28 wings that are mechanically connected and fully synchronized during flight 29 30 31 (full-time coupling). The wing coupling apparatus of “full-time” coupled 32 33 flyers has been reported in Paraneoptera [bark lice (Psocodea: Weber, 1936), 34 35 thrips (Thysanoptera: Pesson, 1951a; Moritz, 1997), aphids, cicadas and 36 37 38 true bugs (Hemiptera: Pesson, 1951b; Bohne and Schneider, 1979; D’Urso 39 40 and Ippolito, 1994; Ni et al., 2002)] and Holometabola [wasps 41 42 (Hymenoptera: Basibuyuk and Quicke, 1997), moths and butterflies 43 44 45 (Lepidoptera: Tillyard, 1918; Braun, 1924), and caddisflies (Trichoptera: 46 47 Tillyard, 1918; Stocks, 2010a)]. Such full-time wing coupling apparatuses 48 49 are one of two primary types: 1) setae of one wing that interact with setae or 50 51 52 other structures on the other wing, such as in Thysanoptera (Pesson, 1951a; 53 54 Moritz, 1997), Hymenoptera (Basibuyuk and Quicke, 1997), and Trichoptera 55 56 (Tillyard, 1918; Stocks, 2008, 2010a,b); 2) non-setal cuticular structures, 57 58 59 60 John Wiley & Sons Journal of Morphology Page 4 of 45 4 1 OGAWA 2 3 4 5 often in the form of grooves, such as in various Hemiptera (Pesson, 1951b; 6 7 D’Urso and Ippolito, 1994) and the jugum in Lepidoptera and Trichoptera 8 9 10 (Tillyard, 1918; Stocks, 2010ab). 11 12 The in-flight wing coupling apparatus of the free-living Psocodea, or 13 14 “Psocoptera”, is located on the distal end of the CuP vein (Fig. 2A, “fli”) and 15 16 17 clasps the hindwing at all times during wing flapping. The psocopterans 18 19 also have a repose-coupling apparatus located on the R or Sc vein that 20 21 engages the costa of the hindwing at rest (New, 1974; Mockford, 1967) (Fig. 22 23 24 2A, “rep”), but this structure is not further examined here. The psocopteran 25 26 in-flight wing coupling structure is formed from non-setal cuticles and 27 28 consists of a “hook” that engages the anterior margin of the hindwing 29 30 31 (Weber, 1936; Günther, 1974). Although there are some SEM studies on the 32 33 psocopteran in-flight coupling structures (New, 1974; Lawson and Chu, 34 35 1974), the structures have not been studied comprehensively. Therefore, 36 37 38 their evolutionary pattern and phylogenetic value are as yet unclear. 39 40 Furthermore, there is also uncertainty about the homology of the structures 41 42 with those of other paraneopteran orders (i.e., Thysanoptera and 43 44 45 Hemiptera: Lawson and Chu, 1974) 46 47 Currently, three suborders of ‘Psocoptera’ are recognized: 48 49 Trogiomorpha, Troctomorpha (including the parasitic lice) and Psocomorpha 50 51 52 (Yoshizawa et al., 2006). Mockford (1967) and Yoshizawa (2002, 2005) 53 54 recognized that in-flight wing coupling structures in psocids are 55 56 phylogenetically informative characters, having a ‘hook’ composed of 57 58 59 60 John Wiley & Sons Page 5 of 45 Journal of Morphology 5 1 OGAWA 2 3 4 5 truncated ‘spines’ fused at their bases as either a synapomorphy supporting 6 7 the clade Troctomorpha + Psocomorpha (Mockford, 1967) or an 8 9 10 autapomorphy of Psocomorpha (Yoshizawa, 2002; 2005). Molecular 11 12 phylogenetic approaches support Troctomorpha and Psocomorpha as sister 13 14 taxa (Yoshizawa et al., 2006; Yoshizawa and Johnson, 2014), but few 15 16 17 morphological characters that might support this relationship are known. 18 19 We expanded on the previous wing characters surveys that were mostly 20 21 based on light microscopy by including additional taxa and using SEM to 22 23 24 examine structures at higher magnification and resolution. We evaluated 25 26 wing coupling characters based on the phylogenetic hypotheses presented by 27 28 Yoshizawa & Johnson (2010, 2014), Friedemann et al. (2014) and Yoshizawa 29 30 31 & Lienhard (2016). We examined the homology and character state 32 33 transformations of the wing coupling apparatus. 34 35 36 37 38 MATERIALS & METHODS 39 40 Taxon selection (Table 1) 41 42 The taxa examined were as follows: Trogiomorpha, 5 species 43 44 45 representing 4 families; Troctomorpha, 7 species representing 9 families; 46 47 and 16 species representing the 23 families of Psocomorpha. We included a 48 49 species of Psocomorpha: Calopsocidae, recently synonymized with 50 51 52 Pseudocaeciliidae (Yoshizawa and Johnson, 2014), because of the highly 53 54 modified, elytra-like wings. Aeolothrips kurosawai (Thysanoptera: 55 56 Aeolothripidae) and Cinara sp. (Hemiptera: Aphididae) were selected as 57 58 59 60 John Wiley & Sons Journal of Morphology Page 6 of 45 6 1 OGAWA 2 3 4 5 outgroups. 6 7 8 9 10 Treatment of Specimens 11 12 Specimens examined were stored in 80% or 99% ethanol. Forewings 13 14 were removed and dehydrated in 100% ethanol for 1 hour. Wing cuticle was 15 16 17 hardened by soaking with 1,1,1,3,3,3-hexamethyldisilazane for 1 hour and 18 19 air drying prior to mounting on 10mm aluminum stubs.
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