Polyandry and fecundity in the Lepidoptera: Can methodological and conceptual approaches bias outcomes?

Behavioral Ecology and Sociobiology

Volumn 55, Issue 4, 2004, Pages 315-324

  Torres Vila, Luis M ^a   Rodríguez Molina, M Carmen ^b   Jennions, Michael D ^c  

^a Servicio de Sanidad Vegetal   (Spain)

^b Serv de Invest y Desarrollo Tecn   (Spain)

^c AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Descriptive method; Experimental method; Fecundity; Meta analysis; Polyandry

Indexed keywords

CONCEPTUAL FRAMEWORK; EXPERIMENTAL STUDY; FECUNDITY; POLYANDRY;

LEPIDOPTERA;

EID: 10744233630     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-003-0712-2     Document Type: Review

References (95)

1. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145-164
2. Bartlett AC, Lewis LJ (1985) Pink bollworm (Lepidoptera: Gelechiidae): reproduction and sperm use by wild-type and mutant moths. Ann Entomol Soc Am 78:559-563
3. Benz G (1969) Influence of mating, insemination, and other factors on oogenesis and oviposition in the moth Zeiraphera diniana. J Insect Physiol 15:55-71
4. Bergström J, Wiklund C (2002) Effects of size and nuptial gifts on butterfly reproduction: can females compensate for a smaller size through male-derived nutrients? Behav Ecol Sociobiol 52:296-302
5. Bergström J, Wiklund C, Kaitala A (2002) Natural variation in female mating frequency in a polyandrous butterfly: effects of size and age. Anim Behav 64:49-54
6. Boggs CL (1995) Male nuptial gifts: phenotypic consequences and evolutionary implications. In: Leather SR, Hardie J (eds) Insect reproduction. CRC Press, Boca Ratón, pp 215-242
7. Bragg DE (1970) Insemination and fecundity in the artichoke plume moth, Platyptilia carduidactyla (Lepidoptera: Pterophoridae). Ann Entomol Soc Am 63:334-335
8. Brakefield PM, El Filali E, Van der Laan R, Breuker CJ, Saccheri IJ, Zwaan B (2001) Effective population size, reproductive success and sperm precedence in the butterfly, Bicyclus anynana, in captivity. J Evol Biol 14:148-156
9. Brower JH (1975) Plodia interpunctella: effect of sex ratio on reproductivity. Ann Entomol Soc Am 68:846-851
10. Callahan PS, Chapin JB (1960) Morphology of the reproductive system and mating in two representative members of the family Noctuidae, Pseudaletia unipuncta and Peridroma margaritosa with comparison to Heliothis zea. Ann Entomol Soc Am 53:763-782
11. Choe JC, Crespi BJ (1997) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge
12. Chu YI, Yang SCO (1991) Ovipositional biology of the tobacco cutworm (Spodoptera litura F.). Chin J Entomol 11:188-196
13. Cook PA (1999) Sperms numbers and female fertility in the moth Plodia interpunctella (Hübner) (Lepidoptera; Pyralidae). J Insect Behav 12:767-779
14. Danthanarayana W, Gu H (1991) Multiple mating and its effect on the reproductive success of female Epiphyas postvittana (Lepidoptera: Tortricidae). Ecol Entomol 16:169-175
15. Delisle J, Hardy M (1997) Male larval nutrition influences the reproductive success of both sexes of the spruce budworm Choristoneura fumiferana (Lepidoptera: Tortricidae). Funct Ecol 11:451-463
16. Drummond BA (1984) Multiple mating and sperm competition in the Lepidoptera. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, New York, pp 291-370
17. Eberhard WG (1985) Sexual selection and animal genitalia. Harvard University Press, Cambridge
18. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton
19. Esteban-Durán J (1975) Evaluaciön del potencial reproductor de las parejas de Carpocapsa pomonella L. en la naturaleza. Ann INIA, Ser Prot Veg 5:281-285
20. Fadamiro HY, Baker TC (1999) Reproductive performance and longevity of female European corn borer, Ostrinia nubilalis: effects of multiple mating, delay in mating, and adult feeding. J Insect Physiol 45:385-392
21. Gohari H, Hawlitzky N (1986) Activité reproductrice de la pyrale du maïs, Ostrinia nubilalis Hbn. (Lep. Pyralidae) à basses températures constantes. Agronomie 6:911-917
22. Graham HM, Glick PA, Ouye MT, Martin DF (1965) Mating frequency of female pink bollworms collected from light traps. Ann Entomol Soc Am 58:595-596
23. Hedges LV, Olkin I (1985) Statistical methods for meta-analysis. Academic Press, New York
24. Hendricks DE, Graham HM, Fernández AT (1970) Mating of female tobacco budworms and bollworms collected from light traps. J Econ Entomol 63:1228-1231
25. Henneberry TJ, Clayton TE (1983) Pink bollworm (Lepidoptera: Gelechiidae): comparative mating frequencies of laboratory-reared and native moths. Ann Entomol Soc Am 76:925-928
26. Henneberry TJ, Leal MP (1979) Pink bollworm: effect of temperature, photoperiod and light intensity, moth age, and mating frequency on oviposition and egg viability. J Econ Entomol 72:489-492
27. Hou ML, Sheng CF (1999) Fecundity and longevity of Helicoverpa armigera (Lepidoptera: Noctuidae): effects of multiple mating. J Econ Entomol 92:569-573
28. Hunter FM, Petrie M, Otronen M, Birkhead T, Moller AP (1993) Why do females copulate repeatedly with one male? Trends Ecol Evol 8:21-26
29. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21-64
30. Jensen RL, Newsom LD, Gibbens J (1974) The soybean looper: effects of adult nutrition on oviposition, mating frequency, and longevity. J Econ Entomol 67:467-470
31. Karlsson B (1998) Nuptial gifts, resource budgets, and reproductive output in a polyandrous butterfly. Ecology 79:2931-2940
32. Kawagoe T, Suzuki N, Matsumoto K (2001) Multiple mating reduces longevity of females of the windmill butterfly Atrophaneura alcinous. Ecol Entomol 26:258-262
33. Kehat M, Gordon D (1975) Mating, longevity, fertility and fecundity of the cotton leafworm, Spodoptera littoralis Boisd. (Lepidoptera: Noctuidae). Phytoparasitica 3:87-102
34. Kehat M, Gordon D (1977) Mating ability, longevity and fecundity of the spiny bollworm, Earias insulana (Lepidoptera: Noctuidae). Entomol Exp Appl 22:267-273
35. Keller L, Reeve HK (1995) Why do females mate with multiple males? The sexually selected sperm hypothesis. Adv Study Behav 24:291-315
36. Kondoh M (2001) Co-evolution of nuptial gift and female multiple mating resulting in diverse breeding systems. Evol Ecol Res 3:75-89
37. Labine PA (1966) The population biology of the butterfly, Euphydryas editha. IV. Sperm precedence - a preliminary report. Evolution 20:580-586
38. Lamunyon CW (1997) Increased fecundity, as a function of multiple mating, in an arctiid moth, Utetheisa ornatrix. Ecol Entomol 22:69-73
39. Landolt PJ (1997) Cabbage looper (Lepidoptera: Noctuidae) fecundity maximized by a combination of access to water and food, and remating. Ann Entomol Soc Am 90:783-789
40. Lederhouse RC (1981) The effect of female mating frequency on egg fertility in the black swallowtail, Papilio polyxenes asterius (Papilionidae). J Lepid Soc 35:266-277
41. Lederhouse RC, Scriber JM (1987) Ecological significance of a postmating decline in egg viability in the tiger swallowtail. J Lepid Soc 41:83-93
42. Lehner PN (1996) Handbook of ethological methods, 2nd edn. Cambridge University Press, Cambridge
43. Lukefahr MJ, Griffin JA (1957) Mating and oviposition habits of the pink bollworm moth. J Econ Entomol 50:487-490
44. Marks RJ (1976) Mating behaviour and fecundity of the red bollworm Diparopsis castanea Hmps. (Lepidoptera, Noctuidae). Bull Entomol Res 66:145-158
45. Martin JA, Pashley DP, Mason LJ (1989) Sperm use patterns of individual fall armyworm (Lepidoptera: Noctuidae). Ann Entomol Soc Am 82:177-180
46. Mason LJ, Pashley DP (1991) Sperm competition in the soybean looper (Lepidoptera: Noctuidae). Ann Entomol Soc Am 84:268-271
47. Matsumoto K, Suzuki N (1992) Effectiveness of the mating plug in Atrophaneura alcinous (Lepidoptera: Papilionidae). Behav Ecol Sociobiol 30:157-163
48. Miyahara Y (1978) Effect of the intake of sugar at adult stage on the mating of Leucania separata and Agrotis ipsilon. Proc Assoc Plant Prot Kyushu 24:101-104
49. Møller AP, Jennions MD (2001) Testing and adjusting for publication bias. Trends Ecol Evol 16:580-586
50. Mourikis PA, Vassilaina-Alexopoulou P (1970) The behaviour of adults of Heliothis armigera (Hbn.) (Lep., Noctuidae) under laboratory conditions. Z Angew Entomol 66:36-41
51. Nakanishi Y, Watanabe M, Ito T (2000) Differences in lifetime reproductive output and mating frequency of two female morphs of the sulfur butterfly, Colias erate (Lepidoptera: Pieridae). J Res Lepid 35:1-8
52. Oberhauser KS (1989) Effects of spermatophores on male and female monarch butterfly reproductive success. Behav Ecol Sociobiol 25:237-246
53. Ouye MT, Graham HM, Richmond CA, Martin DF (1964) Mating studies of the pink bollworm. J Econ Entomol 57:222-225
54. Pair SD, Laster ML, Martin DF (1977) Hybrid sterility of the tobacco budworm: effects of alternate sterile and normal matings on fecundity and fertility. Ann Entomol Soc Am 70:952-954
55. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525-568
56. Pease RW (1968) The evolutionary and biological significance of multiple pairing in Lepidoptera. J Lepid Soc 22:197-209
57. Proshold FI, Bernon GL (1994) Multiple mating in laboratory-reared gypsy moths (Lepidoptera: Lymantriidae). J Econ Entomol 87:661-666
58. Raulston JR, Snow JW, Graham HM, Lingren PD (1975) Tobacco budworm: effect of prior mating and sperm content on the mating behavior. Ann Entomol Soc Am 68:701-704
59. Ravi Kumar G, Rajeshwary H, Ojha NG, Thangavelu K (1995) Effect of multiple mating on fecundity and fertility in the tropical tasar silkworm, Antheraea mylitta (Lepidoptera: Saturniidae). Entomon 20:15-17
60. Ridley M (1988) Mating frequency and fecundity in insects. Biol Rev 63:509-549
61. Rogers CE, Marti OG (1994) Reproductive potential of once-mated moths of the fall armyworm (Lepidoptera: Noctuidae). Fla Entomol 77:402-410
62. Rogers CE, Marti OG (1996) Beet armyworm (Lepidoptera: Noctuidae): effects of age at first mating on reproductive potential. Fla Entomol 79:343-352
63. Rosenberg MS, Adams DC, Gurevitch J (2000) MetaWin: statistical software for meta-analysis. Version 2.0. Sinauer, Sunderland, Mass.
64. Scherrer B (1984) Biostatistique. Gaétan Morin, Quebec
65. Shorey HH (1963) The biology of Trichoplusia ni (Lepidoptera: Noctuidae). II. Factors affecting adult fecundity and longevity. Ann Entomol Soc Am 56:476-480
66. Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton
67. Simmons LW, Siva-Jothy MT (1998) Sperm competition in insects: mechanisms and the potential for selection. In: Birkhead TR, Moller AP (eds) Sperm competition and sexual selection. Academic Press, New York, pp 341-434
68. Smith LM (1970) Sexual activity and egg fertility of the peach tree borer. J Econ Entomol 63:1909-1910
69. Snow JW, Young JR, Jones RL (1970) Competitiveness of sperm in female fall armyworms mating with normal and chemosterilized males. J Econ Entomol 63:1799-1802
70. Stockel J (1973) Influence des relations sexuelles et du milieu trophique de l'adulte sur la reproduction de Sitotroga cerealella Oliv. (Lépidoptère, Gelechiidae). Conséquences écologiques. PhD thesis, Université François-Rabelais de Tours, Tours
71. Svärd L, McNeil JN (1994) Female benefit, male risk: polyandry in the true armyworm Pseudaletia unipuncta. Behav Ecol Sociobiol 35:319-326
72. Svärd L, Wiklund C (1988) Fecundity, egg weight and longevity in relation to multiple mating in females of the monarch butterfly. Behav Ecol Sociobiol 23:39-43
73. Swaby JA, Daterman GE, Sower LL (1987) Mating behavior of Douglas-fir tussock moth, Orgya pseudotsugata (Lepidoptera: Lymantriidae), with special reference to effects of female age. Ann Entomol Soc Am 80:47-50
74. Takeuchi S, Miyashita K (1975) The process of spermatophore transfer during the mating of Spodoptera litura F. Jpn J Appl Entomol Zool 19:41-46
75. Tamhankar AJ (1995) Host influence on mating behavior and spermatophore reception correlated with reproductive output and longevity of female Earias insulana (Boisduval) (Lepidoptera: Noctuidae). J Insect Behav 8:499-511
76. Tamhankar AJ, Gothi KK, Rahalkar GW (1993) Host-induced augmented reproduction in spotted bollworm, Earias vittella (Fabricius) (Lepidoptera: Noctuidae). Insect Sci Appl 14:371-375
77. Taylor OR (1967) Relationship of multiple mating to fertility in Atteva punctella (Lepidoptera: Yponomeutidae). Ann Entomol Soc Am 60:583-590
78. Thibout E (1975) Analyse des causes de l'inhibition de la réceptivité sexuelle et de l'influence d'une éventuelle seconde copulation sur la reproduction chez la Teigne du Poireau, Acrolepia assectella (Lepidoptera: Plutellidae). Entomol Exp Appl 18:105-116
79. Thibout E (1978) L'activité sexuelle et le rôle de l'accouplement sur la reproduction d'un lépidoptère à distribution géographique étendue: Acrolepiopsis (Acrolepia) assectella Zell. (Hyponomeutoïdae). PhD thesis, Université François-Rabelais de Tours, Tours
80. Torres-Vila LM, Stockel J, Rodríguez-Molina MC (1997) Physiological factors regulating polyandry in Lobesia botrana (Lepidoptera: Tortricidae). Physiol Entomol 22:387-393
81. Torres-Vila LM, Rodríguez-Molina MC, Gragera J, Bielza-Lino P (2001) Polyandry in Lepidoptera: a heritable trait in Spodoptera exigua Hübner. Heredity 86:177-183
82. Torres-Vila LM, Gragera J, Rodríguez-Molina MC, Stockel J (2002) Heritable variation for female remating in Lobesia botrana, a usually monandrous moth. Anim Behav 64:899-907
83. Unnithan GC, Paye SO (1990) Factors involved in mating, longevity, fecundity and egg fertility in the maize stem borer, Busseola fusca (Fuller) (Lep., Noctuidae). J Appl Entomol 109:295-301
84. Vahed K (1998) The function of nuptial feeding in insects: a review of empirical studies. Biol Rev 73:43-78
85. Van der Kraan C, Van der Straten M (1988) Effects of mating rate and delayed mating on the fecundity of Adoxophyes orana. Entomol Exp Appl 48:15-23
86. Walker WF (1980) Sperm utilization strategies in non social insects. Am Nat 115:780-799
87. Ward KE, Landolt PJ (1995) Influence of multiple matings on fecundity and longevity of female cabbage looper moths (Lepidoptera: Noctuidae). Ann Entomol Soc Am 88:768-772
88. Watanabe M (1988) Multiple matings increase the fecundity of the yellow swallowtail butterfly, Papilio xuthus L., in summer generations. J Insect Behav 1:17-30
89. Watanabe M, Ando S (1993) Influence of mating frequency on lifetime fecundity in wild females of the small white Pieris rapae (Lepidoptera: Pieridae). Jpn J Entomol 61:691-696
90. Watanabe M, Nozato K (1986) Fecundity of yellow swallowtail butterflies, Papilio xuthus and P. machaon Hippocrates, in a wild environment. Zool Sci 3:509-516
91. Wedell N, Wiklund C, Cook PA (2002) Monandry and polyandry as alternative lifestyles in a butterfly. Behav Ecol 13:450-455
92. Wiklund C, Kaitala A, Lindfors V, Abenius J (1993) Polyandry and its effect on female reproduction in the green-veined white butterfly (Pieris napi L.). Behav Ecol Sociobiol 33:25-33
93. Wiklund C, Kaitala A, Wedell N (1998) Decoupling of reproductive rates and parental expenditure in a polyandrous butterfly. Behav Ecol 9:20-25
94. Yasui Y (1998) The "genetic benefits" of female multiple mating reconsidered. Trends Ecol Evol 13:246-250
95. Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61:1051-1063