Evolutionary Biology

, Volume 40, Issue 2, pp 169–184

Reproductive Trade-Offs and Direct Costs for Males in Arthropods

Synthesis Paper

Abstract

Until 30 years ago, the emphasis on reproductive costs for males was mainly on costs related to mate searching, courtship and fighting with rival males. However, costs for males are substantial and varied and often resemble the more thoroughly studied female reproductive costs. Costs can be referred to as trade-off costs, where investment in reproductive activity comes at the expense of another important activity or fitness component. Investment in reproduction at the expense of longevity and future reproduction is the ultimate cost, because it affects fitness directly. In contrast, flawed performance (e.g., of the immune system) is perceived as a mechanistic trade-off, because it affects fitness indirectly through a mediator (i.e., parasites). Finally, direct costs refer to direct measurements of the energy expenditure during involvement in reproduction-related activities. Both direct and mechanistic trade-off costs often result in decreased longevity compared to unmated males (an ultimate cost). Males incur costs during different reproductive phases: before copulation, when producing sperm, while searching for, courting and copulating with females, and subsequently when guarding females or taking care of offspring. This synthesis follows previous pioneering reviews addressing specific aspects of male costs, but strives to summarize all known male reproductive cost types more comprehensively, including their classification. We suggest several directions for targeted future research. While costs for males have been fairly well described, it is now necessary to uncover the ecological and evolutionary factors responsible for differences between closely related species and systems and to better link between directly-measured costs, mechanistic trade-off costs and ultimate trade-off costs.

Keywords

Competition Homosexual interactions Metabolic rate Missed-opportunity cost Sexual conflict Sexual selection 

Supplementary material

11692_2012_9213_MOESM1_ESM.doc (398 kb)
Supplementary material 1 (DOC 398 kb)

References

  1. Abrahams, M. V. (1993). The trade-off between foraging and courting in male guppies. Animal Behaviour, 45, 673–681.CrossRefGoogle Scholar
  2. Acharya, L., & McNeil, J. N. (1998). Predation risk and mating behavior: The responses of moths to bat-like ultrasound. Behavioral Ecology, 9, 552–558.CrossRefGoogle Scholar
  3. Adamo, S. A. (2004). How should behavioural ecologists interpret measurements of immunity? Animal Behaviour, 68, 1443–1449.CrossRefGoogle Scholar
  4. Ahtiainen, J. J., Alatalo, R. V., Kortet, R., & Rantala, M. J. (2005). A trade-off between sexual signaling and immune function in a natural population of the drumming wolf spider Hygrolycosa rubrofasciata. Journal of Evolutionary Biology, 18, 985–991.PubMedCrossRefGoogle Scholar
  5. Alcock, J. (1994). Postinsemination associations between males and females in insects: The mate-guarding hypothesis. Annual Review of Entomology, 39, 1–21.CrossRefGoogle Scholar
  6. Alonzo, S. H., & Warner, R. R. (1999). A trade-off generated by sexual conflict: Mediterranean wrasse males refuse present mates to increase future success. Behavioral Ecology, 10, 105–111.CrossRefGoogle Scholar
  7. Andrade, M. C. B. (2003). Risky mate search and male self-sacrifice in redback spiders. Behavioral Ecology, 14, 531–538.CrossRefGoogle Scholar
  8. Bailey, W. J., & Haythornthwaite, S. (1998). Risks of calling by the field cricket Teleogryllus oceanicus; potential predation by Australian long-eared bats. Journal of Zoology, 244, 505–513.CrossRefGoogle Scholar
  9. Bailey, W. J., & Nuhardiyati, M. (2005). Copulation, the dynamics of sperm transfer and female refractoriness in the leafhopper Balclutha incise (Hemiptera: Cicadellidae: Deltocephalinae). Physiological Entomology, 30, 343–352.CrossRefGoogle Scholar
  10. Belovsky, G. E., Slade, J. B., & Chase, J. M. (1996). Mating strategies based on foraging ability: An experiment with grasshoppers. Behavioral Ecology, 7, 438–444.CrossRefGoogle Scholar
  11. Benesh, D. P., Valtonen, E. T., & Jormalainen, V. (2007). Reduced survival associated with precopulatory mate guarding in male Asellus aquaticus (Isopoda). Annales Zoologici Fennici, 44, 425–434.Google Scholar
  12. Blanckenhorn, W. U., Hosken, D. J., Martin, O. Y., Reim, C., Teuschl, Y., & Ward, P. I. (2002). The costs of copulating in the dung fly Sepsis cynipsea. Behavioral Ecology, 13, 353–358.CrossRefGoogle Scholar
  13. Blanckenhorn, W. U., Preziosi, R. F., & Fairbairn, D. J. (1995). Time and energy constraints and the evolution of sexual size dimorphism—To eat or to mate? Evolutionary Ecology, 9, 369–381.CrossRefGoogle Scholar
  14. Blanckenhorn, W. U., & Viele, S. N. T. (1999). Foraging in yellow dung flies: Testing for a small-male time budget advantage. Ecological Entomology, 24, 1–6.CrossRefGoogle Scholar
  15. Bonduriansky, R. (2001). The evolution of male mate choice in insects: A synthesis of ideas and evidence. Biological Reviews, 76, 305–339.PubMedCrossRefGoogle Scholar
  16. Bonduriansky, R., Maklakov, A., Zajitschek, F., & Brooks, R. (2008). Sexual selection, sexual conflict and the evolution of ageing and life span. Functional Ecology, 22, 443–453.CrossRefGoogle Scholar
  17. Brockmann, H. J. (2001). The evolution of alternative strategies and tactics. Advances in the Study of Behavior, 30, 1–51.CrossRefGoogle Scholar
  18. Brown, E. A., Gay, L., Vasudev, R., Tregenza, T., Eady, P. E., & Hosken, D. J. (2009). Negative phenotypic and genetic associations between copulation duration and longevity in male seed beetles. Heredity, 103, 340–345.PubMedCrossRefGoogle Scholar
  19. Brown, J. S., & Kotler, B. P. (2004). Hazardous duty pay and the foraging cost of predation. Ecology Letters, 7, 999–1014.CrossRefGoogle Scholar
  20. Burton-Chellew, M. N., Sykes, E. M., Patterson, S., Shuker, D. M., & West, S. A. (2007). The cost of mating and the relationship between body size and fitness in males of the parasitoid wasp Nasonia vitripennis. Evolutionary Ecology Research, 9, 921–934.Google Scholar
  21. Cardoso, M. Z., Roper, J. J., & Gilbert, L. E. (2009). Prenuptial agreements: Mating frequency predicts gift-giving in Heliconius species. Entomologia Experimentalis et Applicata, 131, 109–114.CrossRefGoogle Scholar
  22. Cerenius, L., Lee, B. L., & Söderhäll, K. (2008). The proPO-system: Pros and cons for its role in invertebrate immunity. Trends in Immunology, 29, 263–271.PubMedCrossRefGoogle Scholar
  23. Chapman, T., Arnqvist, G., Bangham, J., & Rowe, L. (2003). Sexual conflict. Trends in Ecology & Evolution, 18, 41–47.CrossRefGoogle Scholar
  24. Cordero, C. (2000). Trade-off between fitness components in males of the polygynous butterfly Callophrys xami (Lycaenidae): The effect of multiple mating on longevity. Behavioral Ecology and Sociobiology, 48, 458–462.CrossRefGoogle Scholar
  25. Cordts, R., & Partridge, L. (1996). Courtship reduces longevity of male Drosophila melanogaster. Animal Behaviour, 52, 269–278.CrossRefGoogle Scholar
  26. Damiens, D., & Boivin, G. (2005). Male reproductive strategy in Trichogramma evanescens: Sperm production and allocation to females. Physiological Entomology, 30, 241–247.CrossRefGoogle Scholar
  27. Davies, S., Kattel, R., Bhatia, B., Petherwick, A., & Chapman, T. (2005). The effect of diet, sex and mating status on longevity in Mediterranean fruit flies (Ceratitis capitata), Diptera: Tephritidae. Experimental Gerontology, 40, 784–792.PubMedCrossRefGoogle Scholar
  28. Dawkins, R. (1976). The selfish gene. Oxford, UK: Oxford University Press.Google Scholar
  29. Desouhant, E., Driessen, G., & Bernstein, A. C. (2005). Host and food searching in a parasitic wasp Venturia canescens: A trade-off between current and future reproduction. Animal Behaviour, 70, 145–152.CrossRefGoogle Scholar
  30. Dickinson, J. L. (1995). Trade-offs between postcopulatory riding and mate location in the blue milkweed beetle. Behavioral Ecology, 6, 280–286.CrossRefGoogle Scholar
  31. Dodson, G., & Marshall, L. (1984). Mating patterns in an ambush bug Phymata fasciata (Phymatidae). American Midland Naturalist, 112, 50–57.CrossRefGoogle Scholar
  32. Dowling, D. K., & Simmons, L. W. (2012). Ejaculate economics: Testing the effects of male sexual history on the trade-off between sperm and immune function in Australian crickets. PLoS ONE, 7, e30172.PubMedCrossRefGoogle Scholar
  33. Dunn, A. M., Dick, J. T. A., & Hatcher, M. J. (2008). The less amorous Gammarus: Predation risk affects mating decisions in Gammarus duebeni (Amphipoda). Animal Behaviour, 76, 1289–1295.CrossRefGoogle Scholar
  34. Engqvist, L., & Sauer, K. P. (2002). A life-history perspective on strategic mating effort in male scorpionflies. Behavioral Ecology, 13, 632–636.CrossRefGoogle Scholar
  35. Engqvist, L., & Sauer, K. P. (2003). Influence of Nutrition on courtship and mating in the scorpionfly Panorpa cognata (Mecoptera, Insecta). Ethology, 109, 911–928.CrossRefGoogle Scholar
  36. Eshel, I., Volovik, I., & Sansone, E. (2000). On Fisher-Zahavi’s handicapped sexy son. Evolutionary Ecology Research, 2, 509–523.Google Scholar
  37. Fedorka, K. M., Zuk, M., & Mousseau, T. A. (2004). Immune suppression and the cost of reproduction in the ground cricket, Allonemobius socius. Evolution, 58, 2478–2485.PubMedGoogle Scholar
  38. Ferkau, C., & Fischer, K. (2006). Costs of reproduction in male Bicyclus anynana and Pieris napi butterflies: Effects of mating history and food limitation. Ethology, 112, 1117–1127.CrossRefGoogle Scholar
  39. Fowler-Finn, K. D., & Hebets, E. A. (2011). More ornamented males exhibit increased predation risk and antipredatory escapes, but not greater mortality. Ethology, 117, 102–114.CrossRefGoogle Scholar
  40. Gaskett, A. C., Herberstein, M. E., Downes, B. J., & Elgar, M. A. (2004). Changes in male mate choice in a sexually cannibalistic orb-web spider (Araneae: Araneidae). Behaviour, 141, 1197–1210.CrossRefGoogle Scholar
  41. Gaskin, T., Futerman, P., & Chapman, T. (2002). Increased density and male–male interactions reduce male longevity in the medfly, Ceratitis capitata. Animal Behaviour, 63, 121–129.CrossRefGoogle Scholar
  42. Gershman, S. N. (2008). Sex-specific differences in immunological costs of multiple mating in Gryllus vocalis field crickets. Behavioral Ecology, 19, 810–815.CrossRefGoogle Scholar
  43. Gershman, S. N., Barnett, C. A., Pettinger, A. M., Weddle, C. B., Hunt, J., & Sakaluk, S. K. (2010). Give ‘til it hurts: Trade-offs between immunity and male reproductive effort in the decorated cricket, Gryllodes sigillatus. Journal of Evolutionary Biology, 23, 829–839.PubMedCrossRefGoogle Scholar
  44. Grazer, V., & Martin, O. Y. (2012). Elevated temperature changes female costs and benefits of reproduction. Evolutionary Ecology, 26, 625–637.CrossRefGoogle Scholar
  45. Griffiths, S. W. (1996). Sex differences in the trade-off between feeding and mating in the guppy. Journal of Fish Biology, 48, 891–898.CrossRefGoogle Scholar
  46. Gwynne, D. T. (1987). Sex-biased predation and the risky mate-locating behaviour of male tick-tock cicadas (Homoptera: Cicadidae). Animal Behaviour, 35, 571–576.CrossRefGoogle Scholar
  47. Gwynne, D. T. (1989). Does copulation increase the risk of predation? Trends in Ecology & Evolution, 4, 54–56.CrossRefGoogle Scholar
  48. Gwynne, D. T. (2008). Sexual conflict over nuptial gifts in insects. Annual Review of Entomology, 53, 83–101.PubMedCrossRefGoogle Scholar
  49. Hack, M. A. (1997). The energetic costs of fighting in the house cricket, Acheta domesticus L. Behavioral Ecology, 8, 28–36.CrossRefGoogle Scholar
  50. Hellriegel, B., & Blanckenhorn, W. U. (2002). Environmental influences on the gametic investment of yellow dung fly males. Evolutionary Ecology, 16, 505–522.CrossRefGoogle Scholar
  51. Herberstein, M. E., Gaskett, A. C., Schneider, J. M., Vella, N. G. F., & Elgar, M. A. (2005). Limits to male copulation frequency: Sexual cannibalism and sterility in St Andrew’s cross spiders (Araneae, Araneidae). Ethology, 111, 1050–1061.CrossRefGoogle Scholar
  52. Himuro, C., & Fujisaki, K. (2010). Mating experience weakens starvation tolerance in the seed bug Togo hemipterus (Heteroptera: Lygaeidae). Physiological Entomology, 35, 128–133.CrossRefGoogle Scholar
  53. Hoback, W. W., & Wagner, W. E., Jr. (1997). The energetic cost of calling in the variable field cricket, Gryllus lineaticeps. Physiological Entomology, 22, 286–290.CrossRefGoogle Scholar
  54. Hoefler, C. D. (2008). The costs of male courtship and potential benefits of male choice for large mates in Phidippus clarus (Araneae, Salticidae). Journal of Arachnology, 36, 210–212.CrossRefGoogle Scholar
  55. Hughes, L., Chang, B. S. W., Wagner, D., & Pierce, N. E. (2000). Effects of mating history on ejaculate size, fecundity, longevity, and copulation duration in the ant-tended lycaenid butterfly, Jalmenus evagoras. Behavioral Ecology and Sociobiology, 47, 119–128.CrossRefGoogle Scholar
  56. Hunt, J., Brooks, R., Jennions, M. D., Smith, M. J., Bentsen, C. L., & Bussiere, L. F. (2004). High-quality male field crickets invest heavily in sexual display but die young. Nature, 432, 1024–1027.PubMedCrossRefGoogle Scholar
  57. Ingleby, F. C., Lewis, Z., & Wedell, N. (2010). Level of sperm competition promotes evolution of male ejaculate allocation patterns in a moth. Animal Behaviour, 80, 37–43.CrossRefGoogle Scholar
  58. Jennions, M. D., Moller, A. P., & Petrie, M. (2001). Sexually selected traits and adult survival: A meta-analysis. Quarterly Review of Biology, 76, 3–36.PubMedCrossRefGoogle Scholar
  59. Kaitala, A. (1991). Phenotypic plasticity in reproductive behavior of waterstriders: Trade-offs between reproduction and longevity during food stress. Functional Ecology, 5, 12–18.CrossRefGoogle Scholar
  60. Kaitala, A., & Axen, A. H. (2000). Egg load and mating status of the golden egg bug affect predation risk. Ecology, 81, 876–880.CrossRefGoogle Scholar
  61. Kaitala, A., Gamberale-Stille, G., & Swartling, S. (2003). Egg carrying attracts enemies in a cryptic coreid bug (Phyllomorpha laciniata). Journal of Insect Behavior, 16, 319–328.CrossRefGoogle Scholar
  62. Katvala, M., Rönn, J. L., & Arnqvist, G. (2008). Correlated evolution between male ejaculate allocation and female remating behaviour in seed beetles (Bruchidae). Journal of Evolutionary Biology, 21, 471–479.PubMedCrossRefGoogle Scholar
  63. Kawecki, T. J., Lenski, R. E., Ebert, D., Hollis, B., Olivieri, I., & Whitlock, M. C. (2012). Experimental evolution. Trends in Ecology & Evolution, 27, 547–560.CrossRefGoogle Scholar
  64. Kelly, C. D., & Jennions, M. D. (2011). Sexual selection and sperm quantity: Meta-analyses of strategic ejaculation. Biological Reviews, 86, 863–884.PubMedCrossRefGoogle Scholar
  65. Kemp, D. J., & Wiklund, C. (2001). Fighting without weaponry: A review of male–male contest competition in butterflies. Behavioral Ecology and Sociobiology, 49, 429–442.CrossRefGoogle Scholar
  66. Kerr, A. M., Gershman, S. N., & Sakaluk, S. K. (2010). Experimentally induced spermatophore production and immune responses reveal a trade-off in crickets. Behavioral Ecology, 21, 647–654.CrossRefGoogle Scholar
  67. Kight, S. L., Sprague, J., Kruse, K. C., & Johnson, L. (1995). Are egg-bearing male water bugs, Belostoma flumineum Say (Hemiptera: Belostomatidae) impaired swimmers? Journal of the Kansas Entomological Society, 68, 468–470.Google Scholar
  68. Kim, T. W., Sakamoto, K., Henmi, Y., & Choe, J. C. (2008). To court or not to court: Reproductive decisions by male fiddler crabs in response to fluctuating food availability. Behavioral Ecology and Sociobiology, 62, 1139–1147.CrossRefGoogle Scholar
  69. Knell, R. J., & Webberley, K. M. (2004). Sexually transmitted diseases of insects: Distribution, evolution, ecology and host behaviour. Biological Reviews, 79, 557–581.PubMedCrossRefGoogle Scholar
  70. Koga, T., Backwell, P. R. Y., Christy, J. H., Murai, M., & Kasuya, E. (2001). Male-biased predation of a fiddler crab. Animal Behaviour, 62, 201–207.CrossRefGoogle Scholar
  71. Koga, T., Backwell, P. R. Y., Jennions, M. D., & Christy, J. H. (1998). Elevated predation risk changes mating behaviour and courtship in a fiddler crab. Proceedings of the Royal Society B, 265, 1385–1390.CrossRefGoogle Scholar
  72. Kotiaho, J. S. (2001). Costs of sexual traits: a mismatch between theoretical considerations and empirical evidence. Biological Reviews, 76, 365–376.PubMedCrossRefGoogle Scholar
  73. Kotiaho, J., Alatalo, R. V., Mappes, J., Parri, S., & Rivero, A. (1998). Male mating success and risk of predation in a wolf spider: A balance between sexual and natural selection? Journal of Animal Ecology, 67, 287–291.CrossRefGoogle Scholar
  74. Kuriwada, T., & Kasuya, E. (2009). Longer copulation duration increases the risk of injury during copulation in the male bell cricket Meloimorpha japonica. Entomological Science, 12, 141–146.CrossRefGoogle Scholar
  75. Lawniczak, M. K. N., Barnes, A. I., Linklater, J. R., Boone, J. M., Wigby, S., & Chapman, T. (2007). Mating and immunity in invertebrates. Trends in Ecology & Evolution, 22, 48–55.CrossRefGoogle Scholar
  76. Leman, J. C., Weddle, C. B., Gershman, S. N., Kerr, A. M., Ower, G. D., St John, J. M., et al. (2009). Lovesick: Immunological costs of mating to male sagebrush crickets. Journal of Evolutionary Biology, 22, 163–171.PubMedCrossRefGoogle Scholar
  77. Levan, K. E., Fedina, T. Y., & Lewis, S. M. (2009). Testing multiple hypotheses for the maintenance of male homosexual behaviour in flour beetles. Journal of Evolutionary Biology, 22, 60–70.PubMedCrossRefGoogle Scholar
  78. Lewis, Z., Sasaki, H., & Miyatake, T. (2011). Sex starved: do resource-limited males ensure fertilization success at the expense of precopulatory mating success? Animal Behaviour, 81, 579–583.CrossRefGoogle Scholar
  79. Lindström, L., Ahtiainen, J. J., Mappes, J., Kotiaho, J. S., Lyytinen, A., & Alatalo, R. V. (2006). Negatively condition dependent predation cost of a positively condition dependent sexual signalling. Journal of Evolutionary Biology, 19, 649–656.PubMedCrossRefGoogle Scholar
  80. MacNally, R., & Young, D. (1981). Some energetics of the bladder cicada, Cystosoma saundersii. Journal of Experimental Biology, 90, 185–196.Google Scholar
  81. Magnhagen, C. (1991). Predation risk as a cost of reproduction. Trends in Ecology & Evolution, 6, 183–186.CrossRefGoogle Scholar
  82. Magrath, M. J. L., & Komdeur, J. (2003). Is male care compromised by additional mating opportunity? Trends in Ecology & Evolution, 18, 424–430.CrossRefGoogle Scholar
  83. Maklakov, A. A., & Bonduriansky, R. (2009). Sex differences in survival costs of homosexual and heterosexual interactions: Evidence from a fly and a beetle. Animal Behaviour, 77, 1375–1379.CrossRefGoogle Scholar
  84. Mappes, J., Alatalo, R. V., Kotiaho, J., & Parri, S. (1996). Viability costs of condition-dependent sexual male display in a drumming wolf spider. Proceedings of the Royal Society B, 263, 785–789.CrossRefGoogle Scholar
  85. Marcotte, M., Delisle, J., & McNeil, J. N. (2005). Impact of male mating history on the temporal sperm dynamics of Choristoneura rosaceana and C. fumiferana females. Journal of Insect Physiology, 51, 537–544.PubMedCrossRefGoogle Scholar
  86. Martin, O. Y., & Hosken, D. J. (2003). Costs and benefits of evolving under experimentally enforced polyandry or monogamy. Evolution, 57, 2765–2772.PubMedGoogle Scholar
  87. Martin, O. Y., & Hosken, D. J. (2004). Copulation reduces male but not female longevity in Saltella sphondylli (Diptera: Sepsidae). Journal of Evolutionary Biology, 17, 357–362.PubMedCrossRefGoogle Scholar
  88. Martín, J., López, P., & Cooper, W. E. (2003). Loss of mating opportunities influences refuge use in the Iberian rock lizard Lacerta monticola. Behavioral Ecology and Sociobiology, 54, 505–510.CrossRefGoogle Scholar
  89. Maxwell, M. R. (1999). The risk of cannibalism and male mating behavior in the Mediterranean praying mantid, Iris oratoria. Behaviour, 136, 205–219.CrossRefGoogle Scholar
  90. McKean, K. A., & Nunney, L. (2001). Increased sexual activity reduces male immune function in Drosophila melanogaster. Proceedings of the Royal Society B, 98, 7904–7909.Google Scholar
  91. McKean, K. A., Yourth, C. P., Lazzaro, B. P., & Clark, A. G. (2008). The evolutionary costs of immunological maintenance and deployment. BMC Evolutionary Biology, 8, 76.PubMedCrossRefGoogle Scholar
  92. McNamara, K. B., Elgar, M. A., & Jones, T. M. (2008). A longevity cost of re-mating but no benefits of polyandry in the almond moth, Cadra cautella. Behavioral Ecology and Sociobiology, 62, 1433–1440.CrossRefGoogle Scholar
  93. Michalczyk, L., Millard, A. L., Martin, O. Y., Lumley, A. J., Emerson, B. C., & Gage, M. J. G. (2011). Experimental evolution exposes female and male responses to sexual selection and conflict in Tribolium castaneum. Evolution, 65, 713–724.PubMedCrossRefGoogle Scholar
  94. Miettinen, M., Kaitala, A., Smith, R. L., & Ordonez, R. M. (2006). Do egg carrying and protracted copulation affect mobility in the golden egg bug? Journal of Insect Behavior, 19, 171–178.CrossRefGoogle Scholar
  95. Monaghan, P., Charmantier, A., Nussey, D. H., & Ricklefs, R. E. (2008). The evolutionary ecology of senescence. Functional Ecology, 22, 371–378.CrossRefGoogle Scholar
  96. Morrell, L. J. (2004). Are behavioural trade-offs all they seem? Counter-intuitive resolution of the conflict between two behaviours. Behavioral Ecology and Sociobiology, 56, 539–545.CrossRefGoogle Scholar
  97. Nakayama, S., & Miyatake, T. (2010). Genetic trade-off between abilities to avoid attack and to mate: A cost of tonic immobility. Biology Letters, 6, 18–20.PubMedCrossRefGoogle Scholar
  98. Oku, K. (2009). Effects of density experience on mate guarding behavior by adult male Kanzawa spider mites. Journal of Ethology, 27, 279–283.CrossRefGoogle Scholar
  99. Oliver, C., & Cordero, C. (2009). Multiple mating reduces male survivorship but not ejaculate size in the polygamous insect Stenomacra marginella (Heteroptera: Largidae). Evolutionary Ecology, 23, 417–424.CrossRefGoogle Scholar
  100. Omkar, & Mishra, G. (2005). Mating in aphidophagous ladybirds: Costs and benefits. Journal of Applied Entomology, 129, 432–436.Google Scholar
  101. Papadopoulos, N. T., Liedo, P., Müller, H. G., Wang, J. L., Molleman, F., & Carey, J. R. (2010). Cost of preproduction in male medflies: The primacy of sexual courting in extreme longevity reduction. Journal of Insect Physiology, 56, 283–287.PubMedCrossRefGoogle Scholar
  102. Parker, G. A. (2006). Sexual conflict over mating and fertilization: An overview. Philosophical Transactions of the Royal Society B, 361, 235–259.CrossRefGoogle Scholar
  103. Parker, G. A., & Partridge, L. (1998). Sexual conflict and speciation. Philosophical Transactions of the Royal Society B, 353, 261–274.CrossRefGoogle Scholar
  104. Parker, G. A., & Pizzari, T. (2010). Sperm competition and ejaculate economics. Biological Reviews, 85, 897–934.PubMedGoogle Scholar
  105. Parker, D. J., & Vahed, K. (2010). The intensity of pre- and post-copulatory mate guarding in relation to spermatophore transfer in the cricket Gryllus bimaculatus. Journal of Ethology, 28, 245–249.CrossRefGoogle Scholar
  106. Partridge, L., & Farquhar, M. (1981). Sexual activity reduces lifespan of male fruitflies. Nature, 294, 580–582.CrossRefGoogle Scholar
  107. Paukku, S., & Kotiaho, J. S. (2005). Cost of reproduction in Callosobruchus maculatus: Effects of mating on male longevity and the effect of male mating status on female longevity. Journal of Insect Physiology, 51, 1220–1226.PubMedCrossRefGoogle Scholar
  108. Pereira, R., Sivinski, J., Teal, P., & Brockmann, J. (2010). Enhancing male sexual success in a lekking fly (Anastrepha suspensa Diptera: Tephritidae) through a juvenile hormone analog has no effect on adult mortality. Journal of Insect Physiology, 56, 1552–1557.PubMedCrossRefGoogle Scholar
  109. Perez-Staples, D., & Aluja, M. (2006). Sperm allocation and cost of mating in a tropical tephritid fruit fly. Journal of Insect Physiology, 52, 839–845.PubMedCrossRefGoogle Scholar
  110. Pizzari, T., & Parker, G. A. (2009). Sperm competition and sperm phenotype. In T. R. Birkhead, D. J. Hosken, & S. Pitnick (Eds.), Sperm biology: An evolutionary perspective (pp. 207–245). Burlington, USA: Academic Press.CrossRefGoogle Scholar
  111. Polis, G. A., Barnes, J. D., Seely, M. K., Henschel, J. R., & Enders, M. M. (1998). Predation as a major cost of reproduction in Namib desert Tenebrionid beetles. Ecology, 79, 2560–2566.CrossRefGoogle Scholar
  112. Rantala, M. J., & Kortet, R. (2003). Courtship song and immune function in the field cricket Gryllus bimaculatus. Biological Journal of the Linnean Society, 79, 503–510.CrossRefGoogle Scholar
  113. Rantala, M. J., Koskimäki, J., Taskinen, J., Tynkkynen, K., & Suhonen, J. (2000). Immunocompetence, developmental stability and wingspot size in the damselfly Calopteryx splendens L. Proceedings of the Royal Society B, 267, 2453–2457.PubMedCrossRefGoogle Scholar
  114. Reaney, L. T. (2007). Foraging and mating opportunities influence refuge use in the fiddler crab, Uca mjoebergi. Animal Behaviour, 73, 711–716.CrossRefGoogle Scholar
  115. Reinhardt, K. (2007). Ejaculate size varies with remating interval in the grasshopper Chorthippus parallelus erythropus (Caelifera: Acrididae). European Journal of Entomology, 104, 725–729.Google Scholar
  116. Reinhold, K., Greenfield, M. D., Jang, Y. W., & Broce, A. (1998). Energetic cost of sexual attractiveness: Ultrasonic advertisement in wax moths. Animal Behaviour, 55, 905–913.PubMedCrossRefGoogle Scholar
  117. Reznick, D., Nunney, L., & Tessier, A. (2000). Big houses, big cars, superfleas and the costs of reproduction. Trends in Ecology & Evolution, 15, 421–425.CrossRefGoogle Scholar
  118. Robinson, B. W., & Doyle, R. W. (1985). Trade-off between male reproduction (Amplexus) and growth in the amphipod Gammarus lawrencianus. Biological Bulletin, 168, 482–488.CrossRefGoogle Scholar
  119. Rolff, J., & Siva-Jothy, M. T. (2002). Copulation corrupts immunity: A mechanism for a cost of mating in insects. Proceedings of the National Academy of Sciences USA, 99, 9916–9918.CrossRefGoogle Scholar
  120. Rondeau, A., & Sainte-Marie, B. (2001). Variable mate-guarding time and sperm allocation by male snow crabs (Chionoecetes opilio) in response to sexual competition, and their impact on the mating success of females. Biological Bulletin, 201, 204–217.PubMedCrossRefGoogle Scholar
  121. Rönn, J. L., Katvala, M., & Arnqvist, G. (2008). Interspecific variation in ejaculate allocation and associated effects on female fitness in seed beetles. Journal of Evolutionary Biology, 21, 461–470.PubMedCrossRefGoogle Scholar
  122. Rose, M., & Charlesworth, B. (1980). A test of evolutionary theories of senescence. Nature, 287, 141–142.PubMedCrossRefGoogle Scholar
  123. Rowe, L. (1994). The costs of mating and mate choice in water striders. Animal Behaviour, 48, 1049–1056.CrossRefGoogle Scholar
  124. Ryne, C. (2009). Homosexual interactions in bed bugs: Alarm pheromones as male recognition signals. Animal Behaviour, 78, 1471–1475.CrossRefGoogle Scholar
  125. Saeki, Y., Kruse, K. C., & Switzer, P. V. (2005). Physiological costs of mate guarding in the Japanese beetle (Popillia japonica Newman). Ethology, 111, 863–877.CrossRefGoogle Scholar
  126. Santangelo, N., Itzkowitz, M., Richter, M., & Haley, M. P. (2002). Resource attractiveness of the male beaugregory damselfish and his decision to court or defend. Behavioral Ecology, 13, 676–681.CrossRefGoogle Scholar
  127. Sbilordo, S. H., Grazer, V. M., Demont, M., & Martin, O. Y. (2011). Impacts of starvation on male reproductive success in Tribolium castaneum. Evolutionary Ecology Research, 13, 347–359.Google Scholar
  128. Scharf, I., Lubin, Y., & Ovadia, O. (2011). Foraging decisions and behavioural flexibility in trap-building predators: A review. Biological Reviews, 86, 626–639.PubMedCrossRefGoogle Scholar
  129. Schneider, J. M., & Lubin, Y. (1998). Intersexual conflict in spiders. Oikos, 83, 496–506.CrossRefGoogle Scholar
  130. Segers, F. H. I. D., & Taborsky, B. (2011). Egg size and food abundance interactively affect juvenile growth and behaviour. Functional Ecology, 25, 166–176.CrossRefGoogle Scholar
  131. Service, P. M. (1989). The effect of mating status on lifespan, egg laying, and starvation resistance in Drosophila melanogaster in relation to selection on longevity. Journal of Insect Physiology, 35, 447–452.CrossRefGoogle Scholar
  132. Sih, A., Krupa, J., & Travers, S. (1990). An experimental study on the effects of predation risk and feeding regime on the mating behavior of the water strider. American Naturalist, 135, 284–290.CrossRefGoogle Scholar
  133. Simmons, L. W., & Kvarnemo, C. (2006). Costs of breeding and their effects on the direction of sexual selection. Proceedings of the Royal Society B, 273, 465–470.PubMedCrossRefGoogle Scholar
  134. Simmons, L. W., Zuk, M., & Rotenberry, J. T. (2005). Immune function reflected in calling song characteristics in a natural population of the cricket Teleogryllus commodus. Animal Behaviour, 69, 1235–1241.CrossRefGoogle Scholar
  135. Siva-Jothy, M. T. (2000). A mechanistic link between parasite resistance and expression of a sexually selected trait in a damselfly. Proceedings of the Royal Society B, 267, 2523–2527.PubMedCrossRefGoogle Scholar
  136. Siva-Jothy, M. T., Tsubaki, Y., & Hooper, R. E. (1998). Decreased immune response as a proximate cost of copulation and oviposition in a damselfly. Physiological Entomology, 23, 274–277.CrossRefGoogle Scholar
  137. Solensky, M. J., & Oberhauser, K. S. (2009). Male monarch butterflies, Danaus plexippus, adjust ejaculates in response to intensity of sperm competition. Animal Behaviour, 77, 465–472.CrossRefGoogle Scholar
  138. South, S. H., Steiner, D., & Arnqvist, G. (2009). Male mating costs in a polygynous mosquito with ornaments expressed in both sexes. Proceedings of the Royal Society B, 276, 3671–3678.PubMedCrossRefGoogle Scholar
  139. Sparkes, T. C., Keogh, D. P., & Pary, R. A. (1996). Energetic costs of mate guarding behavior in male stream-dwelling isopods. Oecologia, 106, 166–171.CrossRefGoogle Scholar
  140. Spratt, E. C. (1980). Male homosexual behaviour and other factors influencing adult longevity in Tribolium castaneum (Herbst) and T. confusum Duval. Journal of Stored Products Research, 16, 109–114.CrossRefGoogle Scholar
  141. Stearns, S. C. (1992). The evolution of life histories. Oxford: Oxford University Press.Google Scholar
  142. Steiger, S., Franz, R., Eggert, A. K., & Müller, J. K. (2008). The Coolidge effect, individual recognition and selection for distinctive cuticular signatures in a burying beetle. Proceedings of the Royal Society B, 275, 1831–1838.PubMedCrossRefGoogle Scholar
  143. Stjernholm, F., & Karlsson, B. (2006). Reproductive expenditure affects utilization of thoracic and abdominal resources in male Pieris napi butterflies. Functional Ecology, 20, 442–448.CrossRefGoogle Scholar
  144. Svensson, G. P., Löfstedt, C., & Skals, N. (2004). The odour makes the difference: Male moths attracted by sex pheromones ignore the threat by predatory bats. Oikos, 104, 91–97.CrossRefGoogle Scholar
  145. Svensson, B. G., Petersson, E., & Forsgren, E. (1989). Why do males of the dance fly Empis borealis refuse to mate? The importance of female age and size. Journal of Insect Behavior, 2, 387–395.CrossRefGoogle Scholar
  146. Torres-Vila, L. M., & Jennions, M. D. (2005). Male mating history and female fecundity in the Lepidoptera: Do male virgins make better partners? Behavioral Ecology and Sociobiology, 57, 318–326.CrossRefGoogle Scholar
  147. Valtonen, T. M., Viitaniemi, H., & Rantala, M. J. (2010). Copulation enhances resistance against an entomopathogenic fungus in the mealworm beetle Tenebrio molitor. Parasitology, 137, 985–989.PubMedCrossRefGoogle Scholar
  148. Van Duren, L. A., & Videler, J. J. (1996). The trade-off between feeding, mate seeking and predator avoidance in copepods: Behavioural responses to chemical cues. Journal of Plankton Research, 18, 805–818.CrossRefGoogle Scholar
  149. Van Voorhies, W. A. (1992). Production of sperm reduces nematode lifespan. Nature, 360, 456–458.PubMedCrossRefGoogle Scholar
  150. Verdolin, J. L. (2006). Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behavioral Ecology and Sociobiology, 60, 457–464.CrossRefGoogle Scholar
  151. Waage, J. K. (1988). Confusion over residency and the escalation of damselfly territorial disputes. Animal Behaviour, 36, 586–595.CrossRefGoogle Scholar
  152. Ward, P. I. (1986). A comparative field study of the breeding behaviour of a stream and a pond population of Gammarus pulex (Amphipoda). Oikos, 46, 29–36.CrossRefGoogle Scholar
  153. Wedell, N. (2010). Variation in male courtship costs in butterflies. Behavioral Ecology and Sociobiology, 64, 1385–1391.CrossRefGoogle Scholar
  154. Wedell, N., Gage, M. J. G., & Parker, G. A. (2002). Sperm competition, male prudence and sperm-limited females. Trends in Ecology & Evolution, 17, 313–319.CrossRefGoogle Scholar
  155. Zahavi, A., & Zahavi, A. (1997). The handicap principle: A missing piece of Darwin’s puzzle. Oxford: Oxford University Press.Google Scholar
  156. Zuk, M., & Kolluru, G. R. (1998). Exploitation of sexual signals by predators and parasitoids. Quarterly Review of Biology, 73, 415–438.CrossRefGoogle Scholar
  157. Zuk, M., & McKean, K. A. (1996). Sex differences in parasite infections: Patterns and processes. International Journal of Parasitology, 26, 1009–1024.PubMedGoogle Scholar
  158. Zuk, M., Rotenberry, J. T., & Simmons, L. W. (1998). Calling songs of field crickets (Teleogryllus oceanicus) with and without phonotactic parasitoid infection. Evolution, 52, 166–171.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Inon Scharf
    • 1
  • Franziska Peter
    • 2
  • Oliver Y. Martin
    • 2
  1. 1.Department of Zoology, Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael
  2. 2.Experimental Ecology, Institute of Integrative Biology IBZETH ZürichZurichSwitzerland

Personalised recommendations