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Is a Gall an Extended Phenotype of The Is a Gall an Extended Phenotype of the Inducing Insect? A Comparative Study of Selected Morphological and Physiological Traits of Leaf and Stem Galls on Machilus thunbergii (Lauraceae) Induced by Five Species of Daphnephila (Diptera: Cecidomyiidae) in Northeastern Taiwan Author(s): Liang-Yu Pan, Wen-Neng Chen, Shau-Ting Chiu, Anantanarayanan Raman, Tung-Chuang Chiang and Man-Miao Yang Source: Zoological Science, 32(3):314-321. Published By: Zoological Society of Japan DOI: http://dx.doi.org/10.2108/zs140244 URL: http://www.bioone.org/doi/full/10.2108/zs140244 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. ZOOLOGICAL SCIENCE 32: 314–321 (2015) © 2015 Zoological Society of Japan Is a Gall an Extended Phenotype of the Inducing Insect? A Comparative Study of Selected Morphological and Physiological Traits of Leaf and Stem Galls on Machilus thunbergii (Lauraceae) Induced by Five Species of Daphnephila (Diptera: Cecidomyiidae) in Northeastern Taiwan Liang-Yu Pan1†, Wen-Neng Chen1†, Shau-Ting Chiu2†, Anantanarayanan Raman3†, Tung-Chuang Chiang1, and Man-Miao Yang1* 1Department of Entomology, National Chung Hsing University, 250, Kuo Kuang Rd., Taichung 402, Taiwan 2Division of Biology, National Museum of Natural Science, 1, Kuan Chien Rd., Taichung 404, Taiwan 3Charles Sturt University & Graham Centre for Agricultural Innovation, PO Box 883, Orange, NSW 2800, Australia Mature galls induced by Daphnephila truncicola, D. taiwanensis, D. sueyenae, D. stenocalia, and D. ornithocephala on Machilus thunbergii in northern Taiwan were examined to verify the dictum that the morphology of galls is an expression of the extended phenotype of the respective gall-inducing insect. Based on their length-width ratio, the materials were grouped into either fleshy (those induced by D. taiwanensis and D. sueyenae) or slim galls (those induced by D. truncicola, D. stenocalia, and D. ornithocephala). Stem galls induced by D. truncicola showed an energy level of 0.0178 kJ/g. Among leaf galls, the greatest energy level was in the one induced by D. stenocalia (0.0193 kJ/g), followed by D. sueyenae (0.0192 kJ/g), D. taiwanensis (0.0189 kJ/g), and D. ornithocephala (0.0160 kJ/g). The numbers of reserve and nutritive cell layers in galls were greater in the stem galls induced by D. truncicola, similar to those in the fleshy leaf galls, than in the slim leaf galls. Based on the fungal taxa isolated from the larval chambers and considering the similarities and diver- gences among gall characteristics, the galls induced by D. truncicola and D. taiwanensis clustered into one, whereas those of D. sueyenae aligned with the ‘D. stenocalia–D. ornithocephala’ cluster. The present study verified that shapes, structure, nutritive tissues, energy levels, and multiple coexisting fungal taxa within galls reinforce that they are extended phenotypes of the respective gall-inducing Daphnephila species and they represent adaptive evolution of Daphnephila on M. thunbergii. Key words: Daphnephila, nutrition sink ability, Machilus thunbergii, gall shape, fungi serve as useful model systems to make such measurements INTRODUCTION in the context of evolution of phytophagy and cecidogeny A majority of gall-inducing insects display a high level of (Price, 2005; Yukawa et al., 2005). Many congeneric specificity to plants (Raman, 1996; Abrahamson et al., 1998, Cecidomyiidae induce galls of varied morphologies either on 2003; Raman et al., 2005) and each gall-inducing insect the same or on closely related species (Skuhravá et al., species generally induces a gall of specific morphology 1984; Yukawa et al., 2005; Raman, 2007; Tokuda et al., (Raman, 2011). Measurements of congruence and depar- 2008). Among the gall-inducing Cecidomyiidae (Gagné, tures from their levels of specificity enable interpretations of 1989; Skuhravá, 2006), the levels of specificity of the evolution of gall-inducing insects (Joy and Crespi, 2007). Daphnephila to species of Lauraceae are striking (Tokuda Biological and biogeographical treatments (Roskam, 1985, and Yukawa, 2007). 1992) indicate that the galls induced by the Cecidomyiidae At least 30 species of Daphnephila (Asphondyliini: Asphondyliina) are suspected to induce galls on the eastern * Corresponding author. Tel. : +886-4-22840361 ext. 551; Palearctic and Oriental species of Machilus and Persea (the Fax : +886-4-22878490; Persea group of Lauraceae, sensu Chanderbali et al., 2001; E-mail: [email protected] Li et al., 2011). Only nine of these have been named: three † These authors contributed equally to this work. from India, one from Japan, and five from Taiwan (Tokuda doi:10.2108/zs140244 and Yukawa, 2007). Available biological information reveals Gall as the phenotype of Daphnephila 315 that the second-stage larvae of the Japanese populations of determined with a digital caliper (CD–6” CSX, Mitutoyo, Japan) and D. machilicola overwinter within galls on Machilus thunbergii, a scientific millimeter ruler, under a stereo-binocular microscope and turn into third-stage larvae in the following spring (MZ125, Leica, Hamburg, Germany; Fig. 1). After removing the (Yukawa, 1974). The species of Daphnephila have adopted inhabitant, the galls were weighed (BL120S, Sartorius, Germany) type-IIA life-history strategy which was defined by Yukawa and the mass of larvae was measured using a microbalance (M2P, Sartorius, Germany). Volumes of galls were calculated by adding (1987) and was suggested to live a longer period than the geometric volume measurements and deduction of that of the larval other type-IIA gall midges (Tokuda et al., 2008). Historically chamber, which was treated as a cylinder. For example, volumes of Daphnephila originated in tropical south Asia and dispersed the galls of D. truncicola and D. taiwanensis parts were considered with Machilus through Taiwan to Japan (Tokuda and as a cone and hemisphere (Fig. 1) and added, minus the larval Yukawa, 2007; Tokuda et al., 2008). All five Taiwanese spe- chamber value treated as a cylinder to obtain the final volume cies induced galls of distinct morphologies on M. thunbergii, value. Gall and larval fresh mass data were analyzed using Genstat which sympatrically distributed in northeastern Taiwan 10 (Payne et al., 2007). Canonical-variate analysis was used to (Tokuda et al., 2008). In addition to inducing galls of char- examine differences among the determined variables, which were acteristic shapes, the Taiwanese species of Daphnephila the identities of the gall-inducing insect taxa (Tokuda et al., 2008) are associated with fungi, a trait common in many of the and compared to obtain within-group variances and co-variances facilitating a data presentation that best described associations Asphondyliini (Gagné, 1994; Roskam, 2005; Rohfritsch, among inducing taxa of insects. Following the tests of significance 2008). Molecular phylogenetic analysis reveal that the stem- of canonical-variate axes, the Mahalanobis–distance measurement gall inducing insect D. truncicola occurred at an ancestral was applied to determine distances among groups, based on position relative to the leaf-gall inducing Ceciodmyiidae, viz., canonical variate scores. D. taiwanensis, D. sueyenae, D. stenocalia, and D. orni- thocephala, whereas the phylogenetic relationships among Light microscopy D. sueyenae, D. stenocalia, and D. ornithocephala were not Mature galls induced by D. truncicola (n = 6) on stems, and D. clear (Tokuda et al., 2008). taiwanensis (n = 6), D. sueyenae (n = 6), D. stenocalia (n = 6), and In the present study, we applied quantitative and quali- D. ornithocephala (n = 6) on leaves were excised and used for light tative measurements to compare ‘mature’ galls seeking microscopy. These were fixed in formal–acetic–alcohol (FAA: 70% ethanol 90 ml, 40% formalin 5 ml, and glacial acetic acid 5 ml) for answers to the following questions: Is the morphology of 72 h. The fixed tissues were then transferred to 70% ethanol and stem and leaf galls on M. thunbergii an expression of stored for 24 h, followed by 80, 90, 95, and 100% ethanol (changed extended phenotype (sensu Dawkins, 1982; Weis et al., every 24 h). The fixed materials were processed through customary 1988) of the respective species of Daphnephila? Do these techniques for embedding in paraffin wax using tertiary–butyl–alcohol morphological and physiological gall characteristics indicate series. Sections (10 μm) were cut on a rotary microtome (Histostat adaptive radiation of Daphnephila on M. thunbergii? To 820, Reichert, NY, USA) and mounted on glass slides in Canada answer these questions, we characterized morphometrics balsam after deparaffinization, clearing, and staining
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