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EUROPEAN JOURNAL of ENTOMOLOGYENTOMOLOGY ISSN (Online): 1802-8829 Eur EUROPEAN JOURNAL OF ENTOMOLOGYENTOMOLOGY ISSN (online): 1802-8829 Eur. J. Entomol. 116: 123–132, 2019 http://www.eje.cz doi: 10.14411/eje.2019.014 ORIGINAL ARTICLE Quantitative response to photoperiod and weak coupling between seasonal morphs and diapause regulation in the Asian comma butterfl y, Polygonia c-aureum (Lepidoptera: Nymphalidae) SATOSHI HIROYOSHI 1, *, MAKIO TAKEDA2, TAKAYUKI MITSUNAGA3 and GADI V.P. REDDY 4 1 Laboratory of Applied Entomology, Faculty of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183-0054, Japan; e-mail: [email protected] 2 Graduate School of Agricultural Science, Kobe University, 1-1 Rokko-dai, Nada, Kobe 657-8501, Japan; e-mail: [email protected] 3 Central Region Agricultural Research Center, National Agriculture and Food Research Organization, 2-1-18 Kannondai, Tsukuba, Ibaraki 305-8666, Japan; e-mail: [email protected] 4 Montana State University, Western Triangle Agricultural Research Center, 9546 Old Shelby Rd., P.O. Box 656, Conrad, MT 59425, USA; e-mail: [email protected] Key words. Lepidoptera, Nymphalidae, Polygonia c-aureum, diapause induction, photoperiodism, ovary, reproduction, seasonal form Abstract. Reproduction and wing patterns (shape and colouration) in Polygonia c-aureum L. (Lepidoptera: Nymphalidae) are regulated by both photoperiod and temperature experienced during the immature stages, which result in the development of summer or autumn forms. The critical day length for this seasonal change in form was 13.5L : 10.5D at 21°C and 13L : 11D at 25°C. We investigated the connection between seasonal form and female reproduction. Under a 15L : 9D photoperiod at 21°C, reproductively active summer form butterfl ies are produced, whereas under an 8L : 16D photoperiod at 21°C autumn form but- terfl ies with a strong tendency to enter diapause were produced. On the other hand, under the critical day lengths at 21 or 25°C, autumn form butterfl ies developed with a weak tendency to enter diapause. When the adult butterfl ies were transferred from a critical or a short photoperiod to a long photoperiod shortly after emergence, the former were more likely to terminate diapause than the latter. If individuals are reared throughout their entire life cycle under a short photoperiod at 21°C, all the adults have a strong tendency to enter diapause. These results reveal the quantitative effects of photoperiod on diapause in this butterfl y and strongly indicate that the determination of the autumn form and induction and maintenance of diapause are not rigidly coupled, at least under laboratory conditions. INTRODUCTION kasuji & Kimura, 1984; Plaistow et al., 2005). Similarly, the Seasonal polyphenism is recorded in many insects (Tau- connection between pupal seasonal polyphenism and pupal ber et al., 1986). Various patterns exist in the relationship or adult diapause is not rigid or incomplete in the black between seasonal forms or change in body colouration swallowtail butterfl y Papilio polyxenes Fabricius (Hazel and diapause depending on the species. For example, as & West, 1983; Sims, 2007), the comma butterfl y Polygo- the planthopper Stirellus bicolor Van Duzee does not enter nia c-album (L.) (Voigt, 1991), and the leafminer Lyonetia diapause, its polyphenism is not related to diapause (Whit- prunifoliella malinella (Matsumura) (Sekita, 2002). How- comb et al., 1972; Tauber et al., 1986). In the dung beetle, ever, there are species in which there is a close relation- Gymnopleurus humanus Macleay, larvae overwinter and ship and both seasonal form and diapause are expressed adult beetles show a temperature-dependent colour poly- in the same imaginal stage, for example, in the lacewings morphism (Davis et al., 2008). In the rice skipper Parnara Chrysopa carnea (Stephens) (Tauber & Tauber, 1970), C. guttata guttata (Bremer & Grey) and the horned beetle Al- congrua (Walker) (Winterton, 1999), and C. sp. (Canard, lomyrina dichotoma (L.), it is the larvae that enter diapause 2005), as well as the rape bug Eurydema oleracea (L.) (Fa- and larval diapause is not tightly coupled with differences sulati, 1979), stink bug Plautia crossota stali Scott (Kotaki in the imaginal seasonal forms (Ishii & Hidaka, 1979; Na- & Yagi, 1987; Kotaki, 1998a, b), brown stink bug Euschis- * Present address: 202 Corpo Mankyu, 1-23-8 Nodamachi, Kawagoe, Saitama 350-1115, Japan. Final formatted article © Institute of Entomology, Biology Centre, Czech Academy of Sciences, České Budějovice. An Open Access article distributed under the Creative Commons (CC-BY) license (http://creativecommons.org/licenses/by/4.0/). 123 Hiroyoshi et al., Eur. J. Entomol. 116: 123–132, 2019 doi: 10.14411/eje.2019.014 tus servus (Say) (Borges et al., 2001), the two-spotted spi- c-album, a species that is closely related to P. c-aureum, a der mite Tetranychus urticae C.L. Koch (Kawakami et al., small proportion of the autumn form mate before overwin- 2009), and elm leaf beetle Xanthogaleruca luteola (Mül- tering. This indicates it is possible that adult diapause in a ler) (Soudi & Moharramipour, 2011), although seasonal proportion of the autumn form of P. c-aureum is terminated polyphenism occurs within the same population in these in early autumn or not induced. This study examines the species. In the squinting bush butterfl y, Bicychus anynana link between seasonal form and adult diapause in females (Butler), the wet season females lay eggs immediately after of P. c-aureum by investigating the effects of combinations mating, whereas the dry season females delay egg-laying of photoperiod and temperature on the induction, mainte- (Prudic et al., 2011). In addition, there is a strong link be- nance, and termination of adult diapause. tween reproductive maturity, diapause, and wing colour in the red locust Nomadacris septemfasciata Audinet-Serville MATERIALS AND METHODS (Franc & Luong-Skovmand, 2009). Wing form is often Insect source and rearing of a colony in the laboratory strongly linked with diapause, as for example in the linden A laboratory colony of P. c-aureum was established using lar- bug Pyrrhocoris apterus (L.) (Socha & Kodrik, 1999) and vae collected in the city of Tokyo (35°67´N, 139°48´E), Japan, in water strider Aquarius paludum (Fabricius) (Inoue & Hara- April and May of 1987. The offspring of the autumn-form of this da, 1997). In the bean bug Riptortus clavatus (L.), there is butterfl y are likely to develop into the summer-form, regardless a close relationship between diapause and seasonal form, of photoperiod (Hidaka & Takahashi, 1967). To avoid this, newly but the link is not consistent at near critical day lengths hatched larvae were reared under a long day length (15L : 9D photoperiod) at 21 ± 1°C, which induced them to produce only (Kobayashi & Numata, 1993). the summer-form. Many studies report that diapause in insects is determined by photoperiod, temperature, humidity, or food conditions Insect rearing for the experiments (Tauber et al., 1986); for example, termination of diapause Newly emerged larvae from the laboratory colony were reared in the peach twig borer, Anarsia lineatella Zeller, occurs under (1) a short day length (8L : 16D photoperiod) (SD) at either after chilling (Damos & Savopoulou-Soultani, 2010) and 21 ± 1°C or 25 ± 1°C, (2) a critical photoperiod (13.5L : 10.5D both temperature and photoperiod affect the induction photoperiod at 21 ± 1°C, (3) 13L : 11D photoperiod at 25 ± 1°C), or (4) a long day length (LD) at 21 ± 1°C, following the methods and termination of diapause in the rice bug, Leptocorisa described by Hiroyoshi (1992). After emergence, the adult butter- chinensis Dallas (Yamashita et al., 2010). It is suggested fl ies were kept either under the same conditions (1–3) as the im- that a photoperiod close to the critical day length has a mature stages, transferred to SD (1) or LD (4) conditions, or (5) signifi cant infl uence on the intensity of pupal diapause in transferred from 25°C to 21°C. In the last experiment, larvae in the swallowtail butterfl y Sericinus montela Gray (Wang et the fourth day of the fi nal (5th) instar that were previously reared al., 2009), while in many insects and mites, diapause ends under SD at 21 ± 1°C were transferred to LD conditions at 21 ± spontaneously when they are kept under diapause-inducing 1°C (6). After emergence, females were separated from males, conditions, without chilling or any other change in regime and kept in separate cages (17 cm × 16.5 cm × 46 cm). A cotton (Tauber et al., 1986; Veerman, 1992). In the nymphalid wool ball soaked in a sucrose solution (10%) was provided ad libitum as food for adults and renewed weekly. butterfl y Polygonia c-aureum L. there is a close relation- ship between adult diapause and seasonal form (summer Experimental design and autumn). Summer form butterfl ies begin reproduction Exp. #1: Effect of the two photoperiods near to CD soon after emergence, whereas autumn form butterfl ies To assess the effects of critical day length (CD) on diapause enter adult diapause and reproduce in spring. Both the sea- induction (See Hiroyoshi, 1992), summer- and autumn-forms sonal form and adult diapause induction in this butterfl y were reared throughout their lifespan under either a 13.5L : 10.5 D are controlled mainly by the photoperiod and temperature photoperiod at 21°C or a 13L : 11D photoperiod at 25°C. Virgin experienced during the larval stage: long photoperiods and summer- and autumn-form adult females were dissected 10, 20 or 30 days after emergence. high temperatures induce the summer-form, which do not diapause, whereas short photoperiods and relatively low Exp. #2: Change in temperature at CD temperatures induce the autumn-form, which enters dia- To assess the effects of temperature on diapause mainte- pause (Hidaka & Aida, 1963; Hidaka & Takahashi, 1967). nance, summer- and autumn-forms that were reared under CD Diapause in female P.
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