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Effects of photoperiod and aging on the adult spermatogenesis of Polygonia c-aureum (Lepidoptera: Nymphalidae), in relation to adult diapause

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Abstract

Adult spermatogenesis of Polygonia c-aureum was compared between non-diapausing and diapausing butterflies before overwintering. This butterfly has seasonal polyphenism, i.e., summer and autumnal forms. Summer form butterflies that emerged in summer reproduce shortly after emergence, while autumnal forms that emerged in autumn mate in spring. Immatures were reared under either a long photoperiod, which produced the summer form without diapause or under a short photoperiod, which produced the autumnal form with diapause. We found almost no differences in adult spermatogenesis between the two seasonal forms, indicating that adult spermatogenesis is not related to adult diapause. Although adult diapause in the autumnal form is maintained under short photoperiods and terminated under long photoperiods, such a photoperiod did not affect the spermatogenesis of the autumnal form. Our earlier studies indicate that relatively few eupyrene and apyrene sperm are produced after overwintering. Although apyrene spermatogenesis occurred in young adults, eupyrene spermatogenesis did in a small scale before overwintering. These results suggest strongly that male autumnal form butterflies prepare the sperm until overwintering, which had been formed during the larval, pupal and young adult stages.

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Abbreviations

ALD:

Autumnal form under a long day length

ASD:

Autumnal form under a short day length

ANOVA:

Analysis of variance

FWL:

Forewing length

GLM:

General linear model

HSD:

Honestly significant difference

LD:

Long day length

SD:

Short day length

SD:

Standard deviation

SLD:

Summer form under a long day length

T:

Treatment

References

  • Cloutier EJ, Beck SD (1963) Spermatogenesis and diapause in the European corn borer, Ostrinia nubilalis. Ann Entomol Soc Am 56:253–255

    Google Scholar 

  • Cook PA, Gage MJG (1995) Effects of risks of sperm competition on the numbers of eupyrene and apyrene sperm ejaculated by the moth Plodia interpunctella (Lepidoptera: Pyralidae). Behav Ecol Sociobiol 36(4):261–268

    Google Scholar 

  • Cook PA, Wedell N (1996) Ejaculate dynamics in butterflies: a strategy for maximizing fertilization success? Proc R Soc B 263:1047–1051

    Google Scholar 

  • Danks HV (2001) The nature of dormancy responses in insects. Acta Soc Zool Bohem 65:169–179

    Google Scholar 

  • Dobson AJ (1990) An introduction to generalized linear models. Chapman and Hall, London, p 174

    Google Scholar 

  • Endo K (1970) Relation between ovarian maturation and activity of the corpora all in seasonal forms of the butterfly, Polygonia c-aureum L. Dev Growth Differ 11:297–304

    CAS  PubMed  Google Scholar 

  • Endo K (1972) Activation of the corpora allata in relation to ovarian maturation in the seasonal forms of the butterfly, Polygonia c-aureum L. Dev Growth Differ 14:263–274

    Google Scholar 

  • Endo K (1973) Hormonal regulation of mating in the butterfly, Polygonia c-aureum L. Dev Growth Differ 15:1–10

    Google Scholar 

  • Fernandez FC, Cruz-Landim C (2005) Apyrene spermatozoa in Achroia grisella (Lepidoptera: Piralidae): a honeybee waxmoth. Braz J Biol 65:739–741

    CAS  PubMed  Google Scholar 

  • Friedländer M (1982) Juvenile hormone and regulation of dichotomous spermatogenesis during the larval diapause of the codling moth. J Insect Physiol 28:1009–1012

    Google Scholar 

  • Friedländer M (1997) Control of the eupyrene-apyrene sperm dimorphism in Lepidoptera. J Insect Physiol 43:1085–1092

    PubMed  Google Scholar 

  • Friedländer M, Benz G (1981a) The eupyrene-apyrene dichotomous spermatogenesis of Lepidoptera. Organ culture study on the timing of apyrene commitment of the codling moths. Int J Invert Rep 3:113–120

    Google Scholar 

  • Friedländer M, Benz G (1981b) Precocious reprogramming of eupyrene-apyrene spermatogenesis commitment induced by allatectomy of the penultimate larval instar of the moth Actias selene. J Insect Physiol 27:267–269

    Google Scholar 

  • Friedländer M, Seth RK, Reynolds SE (2005) Eupyrene and apyrene sperm: Dichotomous spermatogenesis in Lepidoptera. Adv Insect Physiol 32:206–308

    Google Scholar 

  • Fujita K, Inoue M, Watanabe M, Taher MA, Islam F, Shahjahan RMK, Endo K, Yamanaka A (2009) Photoperiodic regulation of reproductive activity in summer- and autumn-morph butterflies of Polygonia c-aureum L. Zool Stud 48:291–297

    Google Scholar 

  • Garvey LK, Gutierrez GM, Krider HM (2000) Ultrastructure and morphogenesis of the apyrene and eupyrene spermatozoa in the gypsy moth (Lepidoptera: Lymantriidae). Ann Entomol Soc Am 93:1147–1155

    Google Scholar 

  • Hamon C, Chauvin G (1992) Ultrastructural analysis of spermatozoa of Korscheltellus lupulimus L. (Lepidoptera: Hepialidae) and Micropterix calthella L. (Lepidoptera:Micropterigidae). Int J Insect Morphol Embryol 21:149–160

    Google Scholar 

  • Heming BS (2003) Insect development and evolution. Cornell University Press, New York

    Google Scholar 

  • Hidaka T, Aida S (1963) Day length as the main factor of seasonal form determination in Polygonia c-aureum (Lepidoptera: Nymphalidae). Zool Sci 4:167–174 (in Japanese with English summary)

    Google Scholar 

  • Hidaka T, Takahashi H (1967) Temperature conditions and maternal effects as modifying factors in photoperiodic control of the seasonal form in Polygonia c-aureum (Lepidoptera: Nymphalidae). Zool Mag 72:77–83

    Google Scholar 

  • Hiroyoshi S (1997) Effects of photoperiod and age on the initiation of sperm movement in male Polygonia c-aureum Linnaeus (Lepidoptera: Nymphalidae). Appl Entomol Zool 32:19–25

    Google Scholar 

  • Hiroyoshi S (1999) Eupyrene and apyrene spermatogenesis in the Asian comma butterfly, Polygonia c-aureum (Lepidoptera: Nymphalidae). Entomol Sci 2:297–305

    Google Scholar 

  • Hiroyoshi S (2000) Effects of aging, temperature and photoperiod on testis development of Polygonia c-aureum (Lepidoptera: Nymphalidae). Entomol Sci 3:227–236

    Google Scholar 

  • Hiroyoshi S, Mitsuhashi J (1998) Effects of environmental conditions and aging on eupyrene sperm movement in male adults of Polygonia c-aureum (Lepidoptera: Nymphalidae). Zool Sci 15:561–565

    CAS  PubMed  Google Scholar 

  • Hiroyoshi S, Reddy GVP (2018) Field and laboratory studies on the ecology, reproduction, and adult diapause of the Asian comma butterfly, Polygonia c-aureum L. (Lepidoptera: Nymphalidae). Insects 9:169. https://doi.org/10.3390/insects9040169

    Article  PubMed Central  Google Scholar 

  • Hiroyoshi S, Reddy GVP, Mitsuhashi J (2017a) Effects of juvenile hormone analogue (methoprene) and 20-hydroxyecdysone on reproduction in Polygonia c-aureum (Lepidoptera: Nymphalidae) in relation to adult diapause. J Comp Physiol A 203:635–647

    CAS  Google Scholar 

  • Hiroyoshi S, Reddy GVP, Mitsuhashi J (2018) Effects of photoperiod, temperature and aging on adult diapause termination and post-diapause development in female Asian comma butterflies, Polygonia c-aureum Linnaeus (Lepidoptera: Nymphalidae). J Comp Physiol A 204:849–858

    Google Scholar 

  • Hiroyoshi S, Yoshimura J, Iwabuchi K, Reddy GVP, Mitsuhashi J (2017b) Effects of pre-overwintering conditions on eupyrene and apyrene spermatogenesis after overwintering in Polygonia c-aureum (Lepidoptera: Nymphalidae). J Insect Physiol 100:1–8

    CAS  PubMed  Google Scholar 

  • Iossa G, Maury C, Fletcher RM, Eady PE (2019) Temperature-induced developmental plasticity in Plodia interpunctella: Reproductive behaviour and sperm length. J Evol Biol 32:675–682

    PubMed  Google Scholar 

  • Jamienson BGM, Dallai R, Afzelius BA (1999) Insects: their spermatozoa and phylogeny. Science Publishers Inc., Enfield

    Google Scholar 

  • Jans P, Benz G, Friedländer M (1984) Apyrene spermatogenesis inducing factor is present in the haemolymph of male and female pupae of the codling moth. J Insect Physiol 30:495–497

    CAS  Google Scholar 

  • Kubo-Irie M, Ohta K, Meguro T, Nakazawa T, Mohri H (1999) Morphological evidence that spermatogenic cells undergo apoptosis within testis of diapausing swallowtail pupa (Atrophaneura alcinous). J Exp Zool 283:194–201

    CAS  Google Scholar 

  • Kubo-Irie M, Yamaguchi T, Tanaka Y, Yamazaki I, Irie M, Mohri H, Shimoda M (2011) Identification of the starting point for spermatogenesis resumption in the post-diapause development of the sweet potato hornworm, Agrius convolvuli L. J Insect Physiol 57:784–790

    CAS  PubMed  Google Scholar 

  • Leviatan R, Friedländer M (1979) The eupyrene-apyrene dichotomous spermatogenesis of Lepidoptera. I. The relationship with postembryonic development and the role of the decline in juvenile hormone titer toward pupation. Dev Biol 68:515–524

    CAS  PubMed  Google Scholar 

  • Mari IP, Gigliolli AAS, Nanya S, Portela-Castro ALdB (2018) Histological and electron microscopy observations on the testis and spermatogenesis of the butterfly Dionejuno (Cramer, 1779) and Agraulis vanillae (Linnaeus, 1758) (Lepidoptera: Nymphalidae). Micron 109:11–21

    PubMed  Google Scholar 

  • Nagaoka S, Asagoshi M, Kato K, Takata Y (2017) Success in the acquisition of Bombyx mori sperm motility is influenced by the extracellular production of nitric oxide (NO) in the presence of seminal fluid nitric oxide synthase (NOS). Insect Biochem Mol Biol 84:40–47

    CAS  PubMed  Google Scholar 

  • Numata H, Hidaka T (1980) Development of male sex cells in the swallowtail, Papilio xuthus L. (Lepidoptera: Papilionidae) in relation to pupal diapause. Appl Entomol Zool 15:151–158

    Google Scholar 

  • Pener MP (1992) Environmental cues, endocrine factors, and reproductive diapause in male insects. Chronobiol Int 9:102–113

    CAS  PubMed  Google Scholar 

  • Pereira MC, Santos DC (2015) Testis morphology and dichotomic spermatogenesis in the sugarcane borer Diatraea saccharalis (F.) (Lepidoptera: Crambidae). Neotrop Entomol 44:481–488

    CAS  PubMed  Google Scholar 

  • Shimoda M, Kubo-Irie M, Ohta K, Irie M, Mohri H (2007) Spermatogenesis in the testes of diapause and non-diapause pupae of the sweet potato hornworm, Agrius convolvuli (L.) (Lepidoptera: Sphingidae). Zool Sci 24:1036–1044

    PubMed  Google Scholar 

  • Silberglied RE, Shepherd JG, Dickinson JL (1984) Eunuchs: the role of apyrene sperm in Lepidoptera? Am Nat 123(2):255–265

    Google Scholar 

  • Sonneenschein M, Hauser CL (1990) Presence of only eupyrene spermatozoa in adult males of the genus, Micropterix Hubner and its phylogenetic significance (Lepidoptera: Zeugloptera, Micropterigidae). Int J Insect Morphol Embryol 19:269–276

    Google Scholar 

  • Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects. Oxford University Press, New York

    Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. S. Moriya, Dr. K. Tateishi, and Mr. K. Takashino for their help. We are also grateful to Dr. J Mitsuhashi and Dr. K. Iwabuchi for their advice in the course of this study. Two anonymous reviewers improved the manuscript.

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Author notes

  1. Satoshi Hiroyoshi

    Present address: , Kawagoe, Saitama, 350-1115, Japan

Authors and Affiliations

  1. Laboratory of Applied Entomology, Faculty of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, 183-0054, Japan

    Satoshi Hiroyoshi

  2. USDA-ARS-Southern Insect Pest Management Research Unit, 141 Experiment Station Road, P.O. Box 346, Stoneville, MS, 38776, USA

    Gadi V. P. Reddy

  3. Central Region Agricultural Research Center, National Agriculture and Food Research Organization, 2-1-18 Kannondai, Tsukuba, Ibaraki, 305-8602, Japan

    Takayuki Mitsunaga

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Correspondence to Satoshi Hiroyoshi.

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Hiroyoshi, S., Reddy, G.V.P. & Mitsunaga, T. Effects of photoperiod and aging on the adult spermatogenesis of Polygonia c-aureum (Lepidoptera: Nymphalidae), in relation to adult diapause. J Comp Physiol A 206, 467–475 (2020). https://doi.org/10.1007/s00359-020-01413-x

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