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A Tale of Winglets: Evolution of Flight Morphology in Stick Insects

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A Tale of Winglets: Evolution of Flight Morphology in Stick Insects bioRxiv preprint doi: https://doi.org/10.1101/774067; this version posted October 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 2 A tale of winglets: evolution of flight morphology in stick insects 3 4 Yu Zeng1,2,†, Conner O’Malley1, Sonal Singhal1,3, Faszly Rahim4,5, 5 Sehoon Park1, Xin Chen6,7, Robert Dudley1,8 6 7 1Department of Integrative Biology, University of California, Berkeley, CA 92870, 8 USA 9 2Schmid College of Science and Technology, Chapman University, Orange, CA 10 92866, USA 11 3 Department of Biology, CSU Dominguez Hills, Carson, CA 90747 USA 12 4Islamic Science Institute, Universiti Sains Islam Malaysia, 71800 Bandar Baru 13 Nilai, Negeri Sembilan, Malaysia 14 5Centre for Insect Systematics, Universiti Kebangsaan Malaysia, 43600 Bangi, 15 Selangor, Malaysia 16 6Department of Biology, The College of Staten Island, The City University of New 17 York, NY 10314, USA 18 7Department of Biology, The Graduate School and University Center, The City 19 University of New York, NY 10016, USA 20 8Smithsonian Tropical Research Institute, Balboa, 21 Republic of Panama 22 23 †Corresponding author: [email protected] 24 25 1 bioRxiv preprint doi: https://doi.org/10.1101/774067; this version posted October 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 26 27 Abstract 28 29 The evolutionary transition between winglessness and a full-winged morphology requires 30 selective advantage for intermediate forms. Conversely, repeated secondary wing 31 reductions among the pterygotes indicates relaxation of such selection. However, 32 evolutionary trajectories of such transitions are not well characterized. The stick insects 33 (Phasmatodea) exhibit diverse wing sizes at both interspecific and intersexual levels, and 34 thus provide a system for examining how selection on flight capability, along with other 35 selective forces, drives the evolution of flight-related morphology. Here, we examine 36 variation in relevant morphology for stick insects using data from 1100+ individuals 37 representing 765 species. Although wing size varies along a continuous spectrum, taxa 38 with either long or miniaturized wings are the most common, whereas those with 39 intermediate-sized wings are relatively rare. In a morphological space defined by wing 40 and body size, the aerodynamically relevant parameter termed wing loading (the average 41 pressure exerted on the air by the wings) varies according to sex-specific scaling laws; 42 volant but also flightless forms are the most common outcomes in both sexes. Using 43 phylogenetically-informed analyses, we show that relative wing size and body size are 44 inversely correlated in long-winged insects regardless of sexual differences in 45 morphology and ecology. These results demonstrate the diversity of flight-related 46 morphology in stick insects, and also provide a general framework for addressing 47 evolutionary coupling between wing and body dimensions. We also find indirect 48 evidence for a ‘fitness valley’ associated with intermediate-sized wings, suggesting 49 relatively rapid evolutionary transitions between wingless and volant forms. 50 51 52 Keywords 53 54 body size, evolution, flight, phasmid, sexual dimorphism, wing size 55 56 57 58 Symbols and abbreviations 59 Aw Wing area 60 pw Wing loading 61 L Body length 62 Lw Wing length 63 m Mass 64 SSD Sexual size dimorphism 65 SWD Sexual wing dimorphism 66 Q Relative wing size 67 ΔL Sexual size dimorphism index 68 ΔQ Sexual wing dimorphism index 69 70 71 2 bioRxiv preprint doi: https://doi.org/10.1101/774067; this version posted October 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 72 1. Introduction 73 74 Flight is fundamental to the ecology and evolutionary diversification of pterygote insects by 75 allowing for three-dimensional mobility and greater access to nutritional resources (Dudley, 76 2000). Nonetheless, approximately 5% of the extant pterygote fauna is flightless (Roff, 1994), 77 and various conditions of reduced wing size (e.g., brachyptery and microptery) are found across 78 the neopteran orders. Given structural costs and high energy expenditure during flight, 79 maintenance of the flight apparatus is not universally favored by selection. Partial reduction or 80 complete loss of wings is associated with various morphological and ecological factors, such as 81 developmental tradeoffs, enhanced female fecundity, and reduced demand for aerial mobility in 82 certain habitats (Roff, 1990; Roff, 1994). In these cases, smaller wings exhibit reduced 83 aerodynamic capability, but may serve secondarily derived non-aerodynamic functions such as 84 use in protection, stridulation, and startle displays (see Dudley, 2000). 85 86 Wing evolution can also be influenced indirectly by selection on overall body 87 size. Generally, reduced body mass enables greater maneuverability in flight (e.g., more rapid 88 translational and rotational accelerations), although numerous factors influence insect size 89 evolution (see Blanckenhorn, 2000; Chown and Gaston, 2010). Furthermore, both flight 90 capacity and body size can be subject to sex-specific selection. As a consequence, sexual size 91 dimorphism (SSD) is typically associated with intersexual niche divergence and with sexual 92 selection (see Shine, 1989; Hedrick and Temeles, 1989). Sexual wing dimorphism (SWD) can in 93 some cases be decoupled from SSD, and may be associated with divergence in aerial niche and 94 wing use (e.g., DeVries et al., 2010). Selection for greater locomotor capacity in males can lead 95 to male-biased SWD, and also to female-biased SSD (see Roff, 1986). It is therefore of interest 96 to consider patterns of sexual dimorphism in both wing and body size within a phylogenetic 97 context. 98 99 The stick insects (Phasmatodea) exhibit great diversity in both wing and body size (Figs. 1, 100 2), but underlying evolutionary patterns are not well characterized. Most winged stick insects 101 possess rudimentary and tegmenized forewings. Phasmid hindwings (designated ‘wings’ 102 hereafter) can be of various sizes and exhibit expanded cubital and anal venation with well- 103 developed flight membranes. Fossil evidence suggest that both wing pairs were full-sized in 104 ancestral stick insects (see Shang et al., 2011; Wang et al., 2014; Yang et al., 2019), whereas 105 numerous extant species exhibit wing reduction. Earlier studies have proposed frequent 106 evolutionary transitions between winged and wingless morphologies, although the directionality 107 and the detailed dynamics of phasmid wing evolution remain contested (see Whiting et. al., 108 2003; Stone and French, 2003; Trueman et al., 2004; Whiting and Whiting, 2004; Goldberg and 109 Igić, 2008). Nevertheless, size-reduced wings must lead to degradation in aerodynamic 110 performance, with possibly concurrent changes in body length and mass. Given the unresolved 111 history of wing size evolution of this group, we use the term ‘reduction’ to describe wings that 112 are developmentally truncated relative to a full-sized morphology, without assessing the 113 directionality of wing size evolution within the phylogeny. 114 115 Here, we examine the evolution of phasmid flight morphology on a macroevolutionary 116 scale. We first describe variation in wing and body size using data from 1100+ individuals across 117 765 species, including intraspecific data from the Asceles tanarata species group with three 3 bioRxiv preprint doi: https://doi.org/10.1101/774067; this version posted October 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 118 subspecies exhibiting altitudinal variation in both wing and body size (see Brock, 1999; Seow- 119 Choen and Brock, 1999; Fig. 2b). This group represents one of the few well-documented cases 120 of features of insect flight morphology being distinctly correlated with a gradient in 121 environmental parameters. Second, using live specimens, we derive a scaling relationship for 122 wing loading with wing and body size. We then use this empirical model to extrapolate variation 123 in flight capability across all sampled species. Third, we use phylogenetic correlational analyses 124 to quantify the relationship between changes in wing size (reflecting flight ability) and body size 125 through evolutionary time. Throughout these analyses, we also assess overall patterns of sexual 126 dimorphism among phasmid species within phylogenetic and allometric contexts. In particular, 127 we examine the correlation between SWD and SSD to address the role of sex-specific ecology in 128 driving the diversity of flight morphology. For example, if selection on male-biased mobility and 129 on female-biased fecundity were coupled, we might expect an inverse correlation between SWD 130 and SSD. 131
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