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Historical Perspective

  • Mamoru Watanabe
Chapter
Part of the Ecological Research Monographs book series (ECOLOGICAL)

Abstract

Male butterflies move over a large area in search of receptive females, infrequently returning to the same area, or patrol within a small area, frequently returning to the same locality. Factors affecting mate-locating behaviour have been mentioned traditionally in the abiotic environment, such as ambient temperature, as well as the biotic environment, such as body temperatures, lek assembly, and territorial perching. Visual cues can be used in the detection and discrimination of conspecific individuals by both sexes, because of their diurnal activities, although some species detect females by scent alone. Various courtship displays have been described in ethology. After adequate courtship behaviour by males, virgin females of most species will accept copulation. Until 30 years ago, it was believed that females in the majority of species mate only once, but that males have the capacity to mate more than once. A plug secreted by males of some species during copulation seemed to prevent further mating of females, supporting such female monogamy. Mate refusal postures of mated females when encountered by males also suggested maintaining female monogamy. Consequently, virgin females are receptive, showing little choice to mate, and mated females are faithful. However, counting the number of spermatophores in the bursa copulatrix of females has indicated that females of most species regularly mate more than once, because a single spermatophore is transferred from the male during a single copulation. Further matings occur after sperm reserves or nutrients are depleted, suggesting that females are not continuously available to mate. Although the sex ratio is unity, for most of the time there are more males than receptive females, and in such circumstances males are in competition to gain access to scarce receptive females. Therefore, female mate choice, particularly in mated females, would be favoured.

Keywords

Accessory glands Aedeagus Territory Age Bursa copulatrix Copula duration Ductus ejaculatorius Eupyrene sperm bundle Hill-topping Patrolling Spermatophore 

References

  1. Alcock J (2010) The hilltopping mating system of the duskywing skipper Erynnis tristis (Lepidoptera: Hesperiidae). J Res Lepid 43:1–5Google Scholar
  2. Ando S, Watanabe M (1992) Egg load and multiple matings of a cabbage butterfly, Pieris canidia indica (Evans), in the wild. Jpn J Appl Entomol Zool 36:200–201 (in Japanese with English summary)CrossRefGoogle Scholar
  3. Ando S, Watanabe M (1993) Mating frequency and egg load in the white butterfly, Pieris melete Menetries, in a wild environment. Jpn J Ecol 43:111–114 (in Japanese)Google Scholar
  4. Bergman M, Wiklund C (2009) Visual mate detection and mate flight pursuit in relation to sunspot size in a woodland territorial butterfly. Anim Behav 78:14–23Google Scholar
  5. Birch MC, Lucas D, White PR (1989) The courtship behavior of the cabbage moth, Mamestra brassicae (Lepidoptera: Noctidae), and the role of male hair-pencils. J Insect Behav 2:227–239CrossRefGoogle Scholar
  6. Bissoondath CJ, Wiklund C (1995) Protein content of spermatophores in relation to monandry/polyandry in butterflies. Bahav Ecol Sociobiol 37:365–371CrossRefGoogle Scholar
  7. Bissoondath CJ, Wiklund C (1997) Effect of male body size on sperm precedence in the polyandrous butterfly Pieris napi L. (Lepidoptera: Pieridae). Behav Ecol 8:518–523CrossRefGoogle Scholar
  8. Boggs CL, Gilbert LE (1979) Male contribution to egg production in butterflies: evidence for transfer of nutrients at mating. Science 206:83–84CrossRefPubMedGoogle Scholar
  9. Boggs CL, Nieminen M (2004) Checkerspot reproductive biology. In: Ehrlich PR, Hanski I (eds) On the wings of checkerspots. Oxford University Press, Oxford, pp 92–111Google Scholar
  10. Bulmer MG (1983) Models for the evolution for protandry in insects. Theor Popul Biol 23:314–322CrossRefGoogle Scholar
  11. Burns JM (1968) Mating frequency in natural populations of skippers and butterflies as determined by spermatophore counts. Proc Natl Acad Sci USA 61:852–859Google Scholar
  12. Caballero-Mendieta N, Cordero C (2013) Male mating costs in a butterfly that produces small ejaculates. Physiol Entomol 38:318–325CrossRefGoogle Scholar
  13. Crudgington HS, Siva-Jothy MT (2000) Genital damage, kicking and early death. Nature (Lond) 407:855–856CrossRefGoogle Scholar
  14. Deinert EI, Lobgino JT, Gilbert LE (1994) Mate competition in butterflies. Nature (Lond) 370:23–24CrossRefGoogle Scholar
  15. Ehrlich PR (1965) The population biology of the butterfly Euphydryas editha. II. The structure of the Jasper Ridge colony. Evolution 19:327–336CrossRefGoogle Scholar
  16. Ehrlich PR, Gilbert LE (1973) Population structure and dynamics of the tropical butterfly Heliconius ethilla. Biotropica 5:69–82CrossRefGoogle Scholar
  17. Estrada C, Gilbert LE (2010) Host plants and immatures as mate-searching cues in Heliconius butterflies. Anim Behav 80:231–239CrossRefGoogle Scholar
  18. Fagerstrom T, Wiklund C (1982) Why do males emerge before females? Protandry as a mating strategy in male and female butterflies. Oecologia (Berl) 52:164–166CrossRefGoogle Scholar
  19. Fincke OM (1982) Lifetime mating success in a natural population of the damselfly, Enallagma hageni (Walsh) (Odonata: Coenagrionidae). Bahav Ecol Sociobiol 10:293–302CrossRefGoogle Scholar
  20. Fiske P, Rintamäki PT, Karvonen E (1998) Mating success in lekking males: a meta-analysis. Behav Ecol 9:328–338CrossRefGoogle Scholar
  21. Forsberg J, Wiklund C (1988) Protandry in the green-veined white butterfly, Pieris napi L. (Lepidoptera; Pieridae). Funct Ecol 2:81–88CrossRefGoogle Scholar
  22. Fosberg J, Wiklund C (1989) Mating in the afternoon: time-saving in courtship and remating by females of the polyandrous butterfly Pieris napi L. Behav Ecol Sociobiol 25:349–356CrossRefGoogle Scholar
  23. Grula JW, McChesney JD, Taylor OR Jr (1980) Aphrodisiac pheromones of the sulfur butterflies Colias eurytheme and C. philodice (Lepidoptera, Pieridae). J Chem Ecol 6:241–256CrossRefGoogle Scholar
  24. Hasegawa M, Watanabe M (2008) Changes in mate preference of male Colias erate poliographus in relation to copulation experience of females. Jpn J Entomol 11:105–114 (in Japanese with English summary)Google Scholar
  25. Irie S, Watanabe M (2009) Courtship behavior of the male sulfur butterfly Colias erate toward experienced females that were inhibited from showing mate refusal behavior by experimental manipulation. Jpn J Biol Educ 49:68–75 (in Japanese with English summary)Google Scholar
  26. Iwasa Y, Odendaal FJ, Murphy DD, Ehrlich PR, Launer AE (1983) Emergence patterns in male butterflies: a hypothesis and a test. Theor Popul Biol 23:363–379CrossRefGoogle Scholar
  27. Kaitala A, Wiklund C (1995) Female mate choice and mating costs in the polyandrous butterfly Pieris napi (Lepidoptera: Pieridae). J Insect Behav 8:355–363CrossRefGoogle Scholar
  28. Karlsson B (1996) Male reproductive reserves in relation to mating system in butterflies: a comparative study. Proc R Soc Lond B 263:187–192CrossRefGoogle Scholar
  29. Kemp DJ, Wiklund C (2001) Fighting without weaponry: a review of male–male contest competition in butterflies. Behav Ecol Sociobiol 49:419–442CrossRefGoogle Scholar
  30. Kemp DJ, Macedonia JM, Ball TS, Rutowski RL (2008) Potential direct fitness consequences of ornament-based mate choice in a butterfly. Behav Ecol Sociobiol 62:1017–1026CrossRefGoogle Scholar
  31. Kiritani K, Nozato K, Miyai S, Ban Y (1984) Studies on ecology and behavior of Japanese black swallowtail butterflies. I. Ecological characteristics of male populations in Papilio helenus nicconicolens Butler and P. protenor demetrius Cramer (Lepidoptera: Papilionidae). Appl Entomol Zool 19:509–517Google Scholar
  32. Klein AL, de Araujo AM (2010) Courtship behavior of Heliconius erato phyllis (Lepidoptera, Nymphalidae) towards virgin and mated females: conflict between attraction and repulsion signals? J Ethol 28:409–420CrossRefGoogle Scholar
  33. Konagaya T, Watanabe M (2015) Adaptive significance of the mating of autumn-morph females with non-overwintering summer-morph males in the Japanese common grass yellow, Eurema mandarina (Lepidoptera: Pieridae). Appl Entomol Zool 50:41–47CrossRefGoogle Scholar
  34. Konagaya T, Mutoh N, Suzuki M, Rutowski RL, Watanabe M (2015) Estimates of female lifetime fecundity and changes in the number and types of sperm stored with age and time since mating in the monandrous swallowtail butterfly, Battus philenor (Lepidoptera: Papilionidae) in the Arizona desert. Appl Entomol Zool 50:311–316CrossRefGoogle Scholar
  35. Labine PA (1968) The population biology of the butterfly, Euphydryas editha. VIII. Oviposition and its relation to patterns of oviposition in other butterflies. Evolution 22:799–805CrossRefGoogle Scholar
  36. LaMunyon CW, Eisner T (1994) Spermatophore size as determinant of paternity in an arctiid moth (Utetheisa ornatrix). Proc Natl Acad Sci USA 91:7081–7084Google Scholar
  37. Lederhouse RC (1981) The effect of female mating frequency on egg fertility in the black swallowtail, Papilio polyxenes asterius (Papilionidae). J Lepid Soc 35:266–277Google Scholar
  38. Leopold RA (1976) The role of male accessory glands in insect reproduction. Annu Rev Entomol 21:199–221CrossRefGoogle Scholar
  39. Marshall LD (1985) Protein and lipid composition of Colias philodice and C. eurytheme spermatophores and their changes over time. J Res Lepid 24:21–30Google Scholar
  40. Nakanishi Y, Watanabe M, Ito T (1996) Differences in lifetime reproductive output and mating frequency of two female morphs of the sulfur butterfly, Colias erate (Lepidoptera: Pieridae). J Res Lepid 35:1–8CrossRefGoogle Scholar
  41. Nozato K, Kiritani K, Miyai S, Ban Y (1985) Studies on ecology and behavior of Japanese black swallowtail butterflies. IV. Estimation of life span of male Papilio helenus nicconicolens Butler and P. protenor demetrius Cramer (Lepidoptera: Papilionidae). Appl Entomol Zool 20:494–496Google Scholar
  42. Osanai M, Aigaki T, Kasuga H (1987) Energy metabolism in the spermatophore of the silkmoth, Bombyx mori, associated with accumulation of alanine derived from arginine. Insect Biochem 17:71–75CrossRefGoogle Scholar
  43. Parker GA (1970) Sperm competition and its evolutionary consequences in insects. Biol Rev 45:525–567CrossRefGoogle Scholar
  44. Parker GA (1982) Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J Theor Biol 96:281–294CrossRefPubMedGoogle Scholar
  45. Rajyaguru P, Pegram KV, Kingston AC, Rutowski RL (2013) Male wing color properties predict the size of nuptial gifts given during mating in the pipevine swallowtail butterfly (Battus philenor). Naturwissenschaften 100:507–513CrossRefPubMedGoogle Scholar
  46. Rosenberg RH, Enquist M (1991) Contest behaviour in Weidemeyer’s admiral butterfly Limenitis weidemeyerii (Nymphalidae): the effect of size and residency. Anim Behav 42:805–811CrossRefGoogle Scholar
  47. Rutowski RL (1978) The courtship behavior of the small sulphur butterfly, Eurema lisa (Lepidoptera: Pieridae). Anim Behav 26:892–903CrossRefGoogle Scholar
  48. Rutowski RL (1984) Sexual selection and the evolution of butterfly mating behavior. J Res Lepid 23:125–142Google Scholar
  49. Rutowski RL (1991) The evolution of male mate-locating behavior in butterflies. Am Nat 138:1121–1139CrossRefGoogle Scholar
  50. Rutowski RL, Gilchrist GW (1986) Copulation in Colias eurytheme (Lepidoptera: Pieridae): patterns and frequency. J Zool Lond A 209:115–124CrossRefGoogle Scholar
  51. Rutowski RL, Rajayaguru P (2013) Male-specific iridescent coloration in the pipevine swallowtail (Battus philenor): used in mate choice but not sexual discrimination by males. J Insect Behav 26:200–211CrossRefGoogle Scholar
  52. Rutowski RL, Newton M, Schaefer J (1983) Interspecific variation in the size of the nutrient investment made by male butterflies during copulation. Evolution 37:708–713CrossRefGoogle Scholar
  53. Rutowski RL, Alcock J, Carey M (1989) Hiltopping in the pipevine swallowtail butterfly (Battus philenor). Ethology 82:244–254CrossRefGoogle Scholar
  54. Rutowski RL, Nahm AC, Macedonia JM (2010) Iridescent hindwing patches in the pipevine swallowtail: differences in dorsal and ventral surface relate to signal function and context. Funct Ecol 24:767–775CrossRefGoogle Scholar
  55. Sasaki N, Konagaya T, Watanabe M, Rutowski RL (2015) Indicators of recent mating success in the pipevine swallowtail butterfly (Battus philenor) and their relationship to male phenotype. J Insect Physiol 83:30–36CrossRefPubMedGoogle Scholar
  56. Scott JA (1972) Mating of butterflies. J Res Lepid 11:99–127Google Scholar
  57. Scott JA (1975) Variability of courtship of the buckeye butterfly, Precis coenia (Nymphalidae). J Res Lepid 14:142–147Google Scholar
  58. Scriber JM, Lederhouse RC (1988) Hand-pairing of Papilio glaucus glaucus and Papilio pilumnus (Papilionidae) and hybrid survival on various food plants. J Res Lepid 27:96–103Google Scholar
  59. Shreeve TG (1987) The mate location behaviour of the male speckled wood butterfly, Pararge aegeria, and the effect of phenotypic differences in hind-wing spotting. Anim Behav 35:682–690CrossRefGoogle Scholar
  60. Silberglied RE, Taylor OR Jr (1978) Ultraviolet reflection and its behavioral role in the courtship of sulfur butterflies Colias eurytheme and C. philodice (Lepidoptera, Pieridae). Behav Ecol Sociobiol 3:203–243CrossRefGoogle Scholar
  61. Singer MC (1982) Sexual selection for small size in male butterflies. Am Nat 119:440–443CrossRefGoogle Scholar
  62. Stern VM, Smith RF (1960) Factors affecting egg production and oviposition in populations of Colias philodice eurytheme Boisduval (Lepidoptera: Pieridae). Hilgardia 29:411–454CrossRefGoogle Scholar
  63. Sugawara T (1979) Stretch reception in the bursa copulatrix of the butterfly, Pieris rapae crucivora, and its role in behaviour. J Comp Physiol 130:191–199CrossRefGoogle Scholar
  64. Svärd L, Wiklund C (1988) Prolonged mating in the monarch butterfly Danaus plexippus and nightfall as a cue for sperm transfer. Oikos 52:351–354CrossRefGoogle Scholar
  65. Svärd L, Wiklund C (1989) Mass and production rate of ejaculates in relation to monandry/polyandry in butterflies. Behav Ecol Sociobiol 24:395–402CrossRefGoogle Scholar
  66. Takanashi T, Hiroki M, Obara Y (2001) Evidence for male and female sex pheromones in the sulfur butterfly, Eurema hecabe. Entomol Exp Appl 101:89–92CrossRefGoogle Scholar
  67. Tatar M (1991) Clutch size in the swallowtail butterfly, Battus philenor: the role of host quality and egg load within and among seasonal flights in California. Behav Ecol Sociobiol 28:337–344CrossRefGoogle Scholar
  68. Thibout E (1979) Stimulation of reproductive activity of females of Acrolepiosis assectella (Lepidoptera: Hyponomeutoidea) by the presence of eupyrene spermatozoa in the spermatheca. Entomol Exp Appl 26:279–290CrossRefGoogle Scholar
  69. Tschudi-Rein K, Benz G (1990) Mechanisms of sperm transfer in female Pieris brassicae (Lepidoptera: Pieridae). Ann Entomol Soc Am 83:1158–1164CrossRefGoogle Scholar
  70. Välimäki P, Kaitala A (2010) Properties of male ejaculates do not generate geographical variation in female mating tactics in a butterfly Pieris napi. Anim Behav 79:1173–1179CrossRefGoogle Scholar
  71. Vande Velde L, Damiens D, Van Dyck H (2011) Spermatophore and sperm allocation in males of the monandrous butterfly Pararge aegeria: the female’s perspective. Ethology 117:645–654CrossRefGoogle Scholar
  72. Vane-Wright D (2003) Butterflies. The Natural History Museum, LondonGoogle Scholar
  73. Watanabe M (1978) Adult movements and resident ratios of the black-veined white, Aporia crataegi, in a hilly region. Jpn J Ecol 28:101–109Google Scholar
  74. Watanabe M (1979a) Natural mortalities of the swallowtail butterfly, Papilio xuthus L., at patchy habitats along the flyways in a hilly region. Jpn J Ecol 29:85–93Google Scholar
  75. Watanabe M (1979b) Population sizes and resident ratios of the swallowtail butterfly, Papilio polytes L., at a secondary bush community in Dharan, Nepal. Kontyu 47:291–297Google Scholar
  76. Watanabe M (1988) Multiple matings increase the fecundity of the yellow swallowtail butterfly, Papilio xuthus L., in summer generations. J Insect Behav 1:17–29CrossRefGoogle Scholar
  77. Watanabe M, Ando S (1993) Influence of mating frequency of lifetime fecundity in wild females of the small white Pieris rapae (Lepidoptera, Pieridae). Jpn J Entomol 61:691–696Google Scholar
  78. Watanabe M, Hirota M (1999) Effects of sucrose intake on spermatophore mass produced by male swallowtail butterfly Papilio xuthus L. Zool Sci 16:55–61CrossRefGoogle Scholar
  79. Watanabe M, Imoto T (2003) Thermoregulation and flying habits of the Japanese sulfur butterfly Colias erate (Lepidoptera: Pieridae) in an open habitat. Entomol Sci 6:111–118CrossRefGoogle Scholar
  80. Watanabe M, Irie S (2011) Female abdomen position signals receptivity during courtship in the Japanese sulphur butterfly, Colias erate (Pieridae). J Lepid Soc 65:259–263Google Scholar
  81. Watanabe M, Nishimura M (2001) Reproductive output and egg maturation in relation to mate-avoidance in monandrous females of the small copper, Lycaena phlaeas (Lycaenidae). J Lepid Soc 54:83–87Google Scholar
  82. Watanabe M, Nozato K (1986) Fecundity of the yellow swallowtail butterflies, Papilio xuthus and P. machaon hippocrates, in a wild environment. Zool Sci 3:509–516Google Scholar
  83. Watanabe M, Sasaki N (2010) Pattern of sperm storage and migration in the reproductive tract of the swallowtail butterfly Papilio xuthus: cryptic female choice after second mating. Physiol Entomol 35:328–333CrossRefGoogle Scholar
  84. Watanabe M, Sato K (1993) A spermatophore structured in the bursa copulatrix of the small white Pieris rapae (Lepidoptera, Pieridae) during copulation and its sugar content. J Res Lepid 32:26–36Google Scholar
  85. Watanabe M, Nozato K, Kiritani K (1986) Studies on ecology and behavior of Japanese black swallowtail butterflies (Lepidoptera: Papilionidae). 5. Fecundity in summer generations. Appl Entomol Zool 21:448–453Google Scholar
  86. Watanabe M, Nakanishi Y, Bon’no M (1997) Prolonged copulation and spermatophore size ejaculated in the sulfur butterfly, Colias erate (Lepidoptera: Pieridae) under selective harassments of mated pairs by conspecific lone males. J Ethol 15:45–54CrossRefGoogle Scholar
  87. Watanabe M, Wiklund C, Bon’no M (1998a) Ejaculation timing of eupyrene and apyrene sperm in the cabbage white butterfly Pieris rapae (Lepidoptera, Pieridae) during copulation. Entomol Sci 1:15–19Google Scholar
  88. Watanabe M, Wiklund C, Bon’no M (1998b) The effect of repeated matings on sperm numbers in successive ejaculates of the cabbage white butterfly Pieris rapae (Lepidoptera: Pieridae). J Insect Behav 11:559–570CrossRefGoogle Scholar
  89. Watanabe M, Bon’no M, Hachisuka A (2000) Eupyrene sperm migrates to spermatheca after apyrene sperm in the swallowtail butterfly, Papilio xuthus L. (Lepidoptera: Papilionidae). J Ethol 18:91–99CrossRefGoogle Scholar
  90. West DA (1983) Hand-pairing of Battus philenor (Papilionidae). J Lepid Soc 37:90Google Scholar
  91. Wickman P-O (1985) Male determined mating duration in butterflies? J Lepid Soc 39:341–342Google Scholar
  92. Wickman P-O (1986) Courtship solicitation by females of the small heath butterfly, Coenonympha pamphilus (L.) (Lepidoptera: Satyridae) and their behaviour in relation to male territories before and after copulation. Anim Behav 34:153–157CrossRefGoogle Scholar
  93. Wickman P-O, Wiklund C (1983) Territorial defence and its seasonal decline in the speckled wood butterfly (Pararge aegeria). Anim Behav 31:1206–1216CrossRefGoogle Scholar
  94. Wiklund C (1977) Courtship behavior in relation to female monogamy in Leptidea sinapis (Lepidoptera). Oikos 29:275–283CrossRefGoogle Scholar
  95. Wiklund C (1982) Behavioral shift from courtship solicitation to mate avoidance in female ringlet butterflies (Aphantopus hyperanthus) after copulation. Anim Behav 30:790–793CrossRefGoogle Scholar
  96. Wiklund C (2003) Sexual selection and the evolution of butterfly mating systems. In: Boggs CL, Watt WB, Ehrlich PR (eds) Butterflies: ecology and evolution taking a flight. University of Chicago Press, Chicago, pp 67–90Google Scholar
  97. Wiklund C, Fagerstrom T (1977) Why do males emerge before females? a hypothesis to explain the incidence of protandry in butterflies. Oecologia (Berl) 31:153–158CrossRefGoogle Scholar
  98. Wiklund C, Forsberg J (1991) Sexual size dimorphism in relation to female polygamy and protandry on butterflies: a comparative study of Swedish Pieridae and Satyridae. Oikos 60:373–381CrossRefGoogle Scholar
  99. Wiklund C, Gotthard K, Nylin S (2003) Mating system and the evolution of sex-specific mortality rates in two nymphalid butterflies. Proc R Soc Lond B 270:1823–1828Google Scholar
  100. Zonneveld C (1992) Polyandry and protandry in butterflies. Bull Math Biol 54:957–9765CrossRefGoogle Scholar

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© Springer Japan 2016

Authors and Affiliations

  • Mamoru Watanabe
    • 1
  1. 1.Graduate School of Life and Environmental SciencesUniversity of TsukubaTsukubaJapan

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