Abstract
Sperm competition is a potent driving force in evolution leading to a remarkable variety of male adaptations that prevent or reduce fertilization by rivals. An extraordinary defensive strategy against sperm competition has evolved in a number of web spiders where males break off parts of their paired genitalia in order to obstruct the copulatory openings of females (mating plug). A recent comparative analysis on the family level reports that genital damage is most frequent in species with sexual cannibalism although, as yet, a functional association between sexual cannibalism and genital damage has not been found. Using the moderately sexually cannibalistic orb-web spider Argiope lobata, we show for the first time that males cannibalized during their first copulation damaged their pedipalps with significantly higher probability (74%) than males that escaped (15%). Of all males that damaged their genitalia, 44% were able to place a genital fragment inside the copulatory opening of the female, resulting in a relatively low total plugging rate of 14%. Successful obstruction of the female copulatory opening reduced the share of paternity of subsequent males (P 2 = 0.06%), thus, indicating that genital damage may have evolved as a response to sperm competition in this species as well. However, the low incidence of successful plugging and the strong relationship between sexual cannibalism and genital damage suggest that apart from paternity protection, the nature of genital damage in A. lobata is further shaped by sexual conflict or cryptic female choice.
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References
Andrade MCB (1996) Sexual selection for male sacrifice in the Australian redback spider. Science 271:70–72
Andrade MCB, Banta EM (2002) Value of male remating and functional sterility in redback spiders. Anim Behav 63:857–870
Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton
Berendonck B, Greven H (2002) Morphology of female and male genitalia of Latrodetus revivensis Shulov, 1948 (Araneae, Theridiidae) with regard to sperm priority patterns. In: Toft S, Scharff N (eds) European Arachnology 2000, Proceedings of the 19th European Colloquium of Arachnology. Aarhus University Press, Aarhus, pp 157–167
Breene RG, Sweet MH (1985) Evidence of insemination of multiple females by the male black widow spider, Latrodectus mactans (Araneae, Theridiidae). J Arachnol 13:331–335
Eberhard WG (1985) Sexual selection and animal genitalia. Harvard University Press, Cambridge
Eberhard WG (2004) Why study spider sex: special traits of spiders facilitate studies of sperm competition and cryptic female choice. J Arachnol 32:545–556
Elgar MA (1992) Sexual cannibalism in spiders and other invertebrates. In: Elgar MA, Crespi BJ (eds) Cannibalism. Oxford, New York, pp 128–155
Elgar MA, Schneider JM (2004) The evolutionary significance of sexual cannibalism. Adv Study Behav 34:135–163
Elgar MA, Schneider JM, Herberstein ME (2000) Female control of paternity in the sexually cannibalistic spider Argiope keyserlingi. Proc R Soc Lond B 267:2439–2443
Foelix RF (1996) Biology of spiders, 2 edn. Oxford University Press, Oxford
Foellmer MW (2008) Broken genitals function as mating plugs and affect sex reatios in the orb-web spider Argiope aurantia. Evo Eco R 10:449–462
Foellmer MW, Fairbairn DJ (2003) Spontaneous male death during copulation in an orb-weaving spider. Proc R Soc Lond B Suppl 270:183–185
Fromhage L, Schneider JM (2005) Virgin doves and mated hawks: contest behaviour in a spider. Anim Behav 70:1099–1104
Fromhage L, Schneider JM (2006) Emasculation to plug up females: the significance of pedipalp damage in Nephila fenestrata. Behav Ecol 17:353–357
Fromhage L, Elgar MA, Schneider JM (2005) Faithful without care: the evolution of monogyny. Evolution 59:1400–1405
Gaskett AC, Herberstein ME, Downes BJ, Elgar MA (2004) Changes in male mate choice in a sexually cannibalistic orb-web spider (Araneae: Araneidae). Behaviour 141:1197–1210
Herberstein ME, Gaskett AC, Schneider JM, Vella NGF, Elgar MA (2005) Limits to male copulation frequency: Sexual cannibalism and sterility in St Andrew’s cross spiders (Araneae, Araneidae). Ethology 111:1050–1061
Jones TM, Elgar MA (2008) Male insemination decisions and sperm quality influence paternity in the golden orb-weaving spider. Behav Ecol 19:285–291
Kuntner M (2007) A monograph of Nephilengys, the pantropical ’hermit spiders’ (Araneae, Nephilidae, Nephilinae). Syst Entomol 32:95–135
Levi HW (1968) The spider genera Gea and Argiope in America. Bull Mus Comp Zool 136:319–352
Levi HW (1975) The orb-weaver genera Verrucosa, Acanthepeira, Wagneriana, Acacesia, Wixia, Scoloderus and Alpaida North of Mexico (Araneae: Araneidae). Bull Mus Comp Zool 147:351–391
Levi HW (1983) The orb-weaver genera Argiope, Gea and Neogea from the Western Pacific region (Araneae: Araneidae, Argiopinae). Bull Mus Comp Zool 150:247–338
Levi HW, Coddington J (1983) Progress report on the phylogeny of the orb-weaving family Araneidae and the superfamily Araneoidea (Arachnida: Araneae). Verh Naturwiss Ver Hamburg 26:151–154
Miller JA (2007) Repeated evolution of male sacrifice behavior in spiders correlated with genital mutilation. Evolution 61:1301–1315
Nessler SH, Uhl G, Schneider JM (2007) Genital damage in the orb-web spider Argiope bruennichi (Araneae: Araneidae) increases paternity success. Behav Ecol 18:174–181
Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567
Rovner JS (1967) Copulation and sperm induction by normal and palpless male linyphiid spiders. Science 157:835
Sasaki T, Iwahashi O (1995) Sexual cannibalism in an orb-weaving spider Argiope aemula. Anim Behav 49:1119–1121
Schneider JM, Thomas ML, Elgar MA (2001) Ectomised conductors in the golden orb-web spider, Nephila plumipes (Araneoidae): a mal adaptation to sexual conflict. Behav Ecol Sociobiol 49:410–415
Schneider JM, Gilberg S, Fromhage L, Uhl G (2006) Sexual conflict over copulation duration in a sexually cannibalistic spider. Anim Behav 71:781–788
Segoli M, Arieli R, Sierwald P, Harari AR, Lubin Y (2008) Sexual cannibalism in the Brown Widow Spider (Latrodectus geometricus). Ethology 114:279–286
Snow LSE, Abdel-Mesih A, Andrade MCB (2006) Broken copulatory organs are low-cost adaptations to sperm competition in redback spiders. Ethology 112:379–389
Uhl G, Nessler SH, Schneider JM (2007) Copulatory mechanism in a sexually cannibalistic spider with genital mutilation (Araneae: Araneidae. Argiope bruennichi). Zoology 110(5):398–408
Wiehle H (1967) Steckengebliebene Emboli in den Vulven von Spinnen (Arach., Araneae). Senckenb Biol 48:197–202
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We wish to thank Efrat Gavish and Jordi Moya-Laraño who helped us to collect the animals.
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Nessler, S.H., Uhl, G. & Schneider, J.M. Sexual cannibalism facilitates genital damage in Argiope lobata (Araneae: Araneidae). Behav Ecol Sociobiol 63, 355–362 (2009). https://doi.org/10.1007/s00265-008-0669-2
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DOI: https://doi.org/10.1007/s00265-008-0669-2