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Optimal ultra-short copulation duration in a sexually cannibalistic spider

  • Braulio A. Assis
  • Matthias W. FoellmerEmail author
Original Article

Abstract

Sexual conflict has been shown to shape many behaviors in the reproductive context, such as the duration of copulation, across a broad taxonomic range. In spiders, copulation duration is one of the most variable reproductive traits, ranging from seconds to hours. Some species in the araneid genus Argiope exhibit very short copulations of a few seconds per pedipalp insertion. This has been hypothesized to be the result of cannibalistic females imposing selection on males to escape the attack by reducing insertion duration to a minimum. However, copulation duration is positively correlated with the number of sperm transferred and fertilization success in many species. Thus, given the tradeoff between sperm transfer and the risk of being cannibalized, males may optimize the duration of copulation to maximize lifetime reproductive success. Here we test whether males in the orb-weaver Argiope aurantia, which exhibits the shortest copulation in any spider and rivals the honey bee for shortest copulation reported for any arthropod with internal genital coupling, are optimizing the insertion duration of the first pedipalp to maximize the number of sperm transferred and eggs fertilized. We analyzed total sperm transferred to the female, and male fertilization success as a function of the first insertion’s duration, using data collected in previous staged-mating experiments and determined optimal copulations of 3–4 s, which is close to the averages of the source populations. Thus, we present evidence for sexual cannibalism as a driver of the extremely short copulations in A. aurantia.

Significance statement

Females and males often conflict over mating frequency. In spiders, both sexes have paired reproductive organs and can remain half virgin if only one of the two possible copulations are completed. In the orb-weaver Argiope aurantia, males place mating plugs and females almost always immediately attack males in copula, probably to prevent them from achieving both copulations and to be able to upgrade to a second mate. We find an optimal duration of 3–4 s for males to terminate copulation, which reduces the risk of being killed, while at the same time maximizing sperm transfer and fertilization success because copulation duration is positively related to the number of sperm transferred and allows males to achieve the second copulation. The optimal duration detected here is very close to average copulation durations in nature. Hence, we document the adaptive value of the shortest copulation known for any spider.

Keywords

Sexual cannibalism Copulation duration Sexual conflict Araneae Sexual size dimorphism Mating plug 

Notes

Acknowledgements

We thank the Nature Conservancy’s Uplands Farm Sanctuary in Cold Spring Harbor, NY, for the permission to collect the spiders. We are grateful for comments by Matjaž Kuntner and one anonymous referee which improved the manuscript.

Data availability statement

All data analyzed during this study are available as part of the supplementary information files.

Funding information

We thank the Biology Department at Adelphi University for financial support.

Supplementary material

265_2019_2733_MOESM1_ESM.xlsx (20 kb)
ESM 1 (XLSX 19 kb)
265_2019_2733_MOESM2_ESM.docx (26 kb)
ESM 2 (DOCX 25 kb)

References

  1. Anderson AG, Hebets EA (2017) Increased insertion number leads to increased sperm transfer and fertilization success in a nursery web spider. Anim Behav 132:121–127.  https://doi.org/10.1016/j.anbehav.2017.08.007 CrossRefGoogle Scholar
  2. Andrade MCB (1996) Sexual selection for male sacrifice in the Australian redback spider. Science 271(80):70–72CrossRefGoogle Scholar
  3. Andrés JA, Cordero Rivera A (2000) Copulation duration and fertilization success in a damselfly: an example of cryptic female choice? Anim Behav 59:695–703.  https://doi.org/10.1006/anbe.1999.1372 CrossRefPubMedGoogle Scholar
  4. Arnqvist G, Henriksson S (1997) Sexual cannibalism in the fishing spider and a model for the evolution of sexual cannibalism based on genetic constraints. Evol Ecol 11:255–273CrossRefGoogle Scholar
  5. Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton, New JerseyCrossRefGoogle Scholar
  6. Assis BA, Foellmer MW (2016) One size fits all? Determinants of sperm transfer in a highly dimorphic orb-web spider. J Evol Biol 29:1106–1120.  https://doi.org/10.1111/jeb.12848 CrossRefPubMedGoogle Scholar
  7. Barry KL, Holwell GI, Herberstein ME (2008) Female praying mantids use sexual cannibalism as a foraging strategy to increase fecundity. Behav Ecol 19:710–715.  https://doi.org/10.1093/beheco/arm156 CrossRefGoogle Scholar
  8. Blamires SJ (2011) Nutritional implications for sexual cannibalism in a sexually dimorphic orb web spider. Austral Ecol 36:389–394.  https://doi.org/10.1111/j.1442-9993.2010.02161.x CrossRefGoogle Scholar
  9. Breheny P, Burchett W (2017) Visualization of regression models using visreg. R J 9:56–71.  https://doi.org/10.32614/rj-2017-046 CrossRefGoogle Scholar
  10. Chapman T (2018) Sexual conflict: mechanisms and emerging themes in resistance biology. Am Nat 192:217–229.  https://doi.org/10.1086/698169 CrossRefPubMedGoogle Scholar
  11. Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47.  https://doi.org/10.1016/S0169-5347(02)00004-6 CrossRefGoogle Scholar
  12. Cheng RC, Kuntner M (2014) Phylogeny suggests nondirectional and isometric evolution of sexual size dimorphism in argiopine spiders. Evolution (N Y) 68:2861–2872.  https://doi.org/10.1111/evo.12504 CrossRefGoogle Scholar
  13. Elgar MA (1991) Sexual cannibalism, size dimorphism, and courtship behavior in orb-weaving spiders (Araneidae). Evolution (N Y) 45:444–448Google Scholar
  14. Elgar MA (1995) The duration of copulation in spiders: comparative patterns. Rec West Aust Museum Suppl 52:1–11Google Scholar
  15. Elgar MA, Schneider JM (2004) Evolutionary significance of sexual cannibalism. Adv Study Behav 34:135–163CrossRefGoogle Scholar
  16. Elgar MA, Schneider JM, Herberstein ME (2000) Female control of paternity in the sexually cannibalistic spider Argiope keyserlingi. Proc R Soc B Biol Sci 267:2439–2443.  https://doi.org/10.1098/rspb.2000.1303 CrossRefGoogle Scholar
  17. Foelix RF (2010) Biology of spiders, 3rd edn. Oxford University Press, New YorkGoogle Scholar
  18. Foellmer MW (2008) Broken genitals function as mating plugs and affect sex ratios in the orb-web spider Argiope aurantia. Evol Ecol Res 10:449–462Google Scholar
  19. Foellmer MW, Fairbairn DJ (2003) Spontaneous male death during copulation in an orb-weaving spider. Proc R Soc Lond Ser B Biol Sci 270:S183–S185CrossRefGoogle Scholar
  20. Foellmer MW, Fairbairn DJ (2004) Males under attack: sexual cannibalism and its consequences for male morphology and behaviour in an orb-weaving spider. Evol Ecol Res 6:1–19Google Scholar
  21. Foellmer MW, Fairbairn DJ (2005) Competing dwarf males: sexual selection in an orb-weaving spider. J Evol Biol 18:629–641CrossRefGoogle Scholar
  22. Foellmer MW, Khadka KK (2013) Does personality explain variation in the probability of sexual cannibalism in the orb-web spider Argiope aurantia? Behaviour 150:1731–1746.  https://doi.org/10.1163/1568539X-00003117 CrossRefGoogle Scholar
  23. Foellmer MW, Moya-Laraño J (2007) Sexual size dimorphism in spiders: patterns and processes. In: Fairbairn DJ, Blanckenhorn WU, Székely T (eds) Sex, size and gender roles: evolutionary studies of sexual size dimorphism. Oxford University Press, Oxford, pp 71–81CrossRefGoogle Scholar
  24. Friesen CR, Uhrig EJ, Squire MK, Mason RT, Brennan PLR (2013) Sexual conflict over mating in red-sided garter snakes (Thamnophis sirtalis) as indicated by experimental manipulation of genitalia. Proc R Soc B Biol Sci 281:302.  https://doi.org/10.1098/rspb.2013.2694 CrossRefGoogle Scholar
  25. Friesen CR, Uhrig EJ, Mason RT, Brennan PLR (2016) Female behaviour and the interaction of male and female genital traits mediate sperm transfer during mating. J Evol Biol 29:952–964.  https://doi.org/10.1111/jeb.12836 CrossRefPubMedGoogle Scholar
  26. Fromhage L, Uhl G, Schneider JM (2003) Fitness consequences of sexual cannibalism in female Argiope bruennichi. Behav Ecol Sociobiol 55:60–64CrossRefGoogle Scholar
  27. Fromhage L, Elgar MA, Schneider JM (2005) Faithful without care: the evolution of monogyny. Evolution (N Y) 59:1400–1405Google Scholar
  28. Gabel E, Uhl G (2013) How to prepare spider sperm for quantification. Arachnology 16:109–112CrossRefGoogle Scholar
  29. Helfenstein F, Wagner RH, Danchin E (2003) Sexual conflict over sperm ejection in monogamous pairs of kittiwakes Rissa tridactyla. Behav Ecol Sociobiol 54:370–376.  https://doi.org/10.1007/s00265-003-0636-x CrossRefGoogle Scholar
  30. Juusola M, French AS (1998) Adaptation properties of two types of sensory neurons in a spider mechanoreceptor organ. J Neurophysiol 80:2781–2784CrossRefGoogle Scholar
  31. Knoflach B, van Harten A (2000) Palpal loss, single palp copulation and obligatory mate consumption in Tidarren cuneolatum (Tullgren, 1910) (Araneae, Theridiidae). J Nat Hist 34:1639–1659.  https://doi.org/10.1080/00222930050117530 CrossRefGoogle Scholar
  32. Koeniger G, Koeniger N, Ellis J, Lawrence JC (2015) Mating biology of honey bees (Apis mellifera). Wicwas Press, Kalamazoo, Michigan, p 156 Google Scholar
  33. Kralj-Fišer S, Schneider JM, Justinek Ž, Kalin S, Gregorič M, Pekár S, Kuntner M (2011) Mate quality, not aggressive spillover, explains sexual cannibalism in a size-dimorphic spider. Behav Ecol Sociobiol 66:145–151.  https://doi.org/10.1007/s00265-011-1262-7 CrossRefGoogle Scholar
  34. Kuntner M, Coddington JA, Schneider JM (2009) Intersexual arms race? Genital coevolution in nephilid spiders (Araneae, Nephilidae). Evolution (N Y) 63:1451–1463.  https://doi.org/10.1111/j.1558-5646.2009.00634.x CrossRefGoogle Scholar
  35. Kuntner M, Agnarsson I, Li D (2015) The eunuch phenomenon: adaptive evolution of genital emasculation in sexually dimorphic spiders. Biol Rev Camb Philos Soc 90:279–296.  https://doi.org/10.1111/brv.12109 CrossRefPubMedGoogle Scholar
  36. Kuntner M, Agnarsson I, Lokovšek T et al (2018) Golden orbweavers ignore biological rules: phylogenomic and comparative analyses unravel a complex evolution of sexual size dimorphism. Syst Biol 68:1–18.  https://doi.org/10.1093/sysbio/syy082 CrossRefGoogle Scholar
  37. Maier L, Root TM, Seyfarth E-A (1987) Heterogeneity of spider leg muscle: histochemistry and electrophysiology of identified fibers in the claw levator. J Comp Physiol B Biochem Syst Environ Physiol 157:285–294.  https://doi.org/10.1007/BF00693355 CrossRefGoogle Scholar
  38. Maklakov AA, Lubin Y (2006) Indirect genetic benefits of polyandry in a spider with direct costs of mating. Behav Ecol Sociobiol 61:31–38CrossRefGoogle Scholar
  39. Mammola S, Michalik P, Hebets EA, Isaia M (2017) Record breaking achievements by spiders and the scientists who study them. PeerJ 5:e3972.  https://doi.org/10.7717/peerj.3972 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Maupin JL (2005) Polyandry in the orb-web spider Argiope trifasciata: its prevalence, fitness consequences, and effects on male and female mating strategies. PhD thesis. Princeton University, Princeton, NJGoogle Scholar
  41. Mazzi D, Kesäniemi J, Hoikkala A, Klappert K (2009) Sexual conflict over the duration of copulation in Drosophila montana: why is longer better? BMC Evol Biol 9:132.  https://doi.org/10.1186/1471-2148-9-132 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Miller JA (2007) Repeated evolution of male sacrifice behavior in spiders correlated with genital mutilation. Evolution (N Y) 61:1301–1315Google Scholar
  43. Parker, G.A. 1970. Sperm competition and its evolutionary consequences in the insects. Biol Rev 45: 525–567CrossRefGoogle Scholar
  44. Peretti A V., Aisenberg A (2015) Cryptic female choice in arthropods: patterns, mechanisms and prospectsGoogle Scholar
  45. Persons MH, Uetz GW (2005) Sexual cannibalism and mate choice decisions in wolf spiders: influence of male size and secondary sexual characters. Anim Behav 69:83–94CrossRefGoogle Scholar
  46. Pilastro A, Mandelli M, Gasparini C, Dadda M, Bisazza A (2007) Copulation duration, insemination efficiency and male attractiveness in guppies. Anim Behav 74:321–328.  https://doi.org/10.1016/j.anbehav.2006.09.016 CrossRefGoogle Scholar
  47. Prenter J, Robert CM, Elwood W (2006) Sexual cannibalism and mate choice. Anim Behav 71:481–490CrossRefGoogle Scholar
  48. RCoreTeam (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.
  49. RStudioTeam (2016) RStudio: Integrated Development for R. RStudio, Inc., Boston, MA. URL http://www.rstudio.com/
  50. Schneider JM, Elgar MA (2001) Sexual cannibalism and sperm competition in the golden orb-web spider Nephila plumipes (Araneoidea): female and male perspectives. Behav Ecol 12:547–552CrossRefGoogle Scholar
  51. Schneider JM, Gilberg S, Fromhage L, Uhl G (2006) Sexual conflict over copulation duration in a cannibalistic spider. Anim Behav 71:781–788CrossRefGoogle Scholar
  52. Schneider JM, Uhl G, Herberstein ME (2015) Cryptic female choice within the genus Argiope: a comparative approach. In: Cryptic female choice in arthropods. Springer International Publishing, Cham, pp 55–77CrossRefGoogle Scholar
  53. Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, PrincetonGoogle Scholar
  54. Snow LSE, Andrade MCB (2004) Pattern of sperm transfer in redback spiders: implications for sperm competition and male sacrifice. Behav Ecol 15:785–792CrossRefGoogle Scholar
  55. Uhl G, Schmitt S, Schäfer MA (2005) Fitness benefits of multiple mating versus female mate choice in the cellar spider (Pholcus phalangioides). Behav Ecol Sociobiol 59:69–76.  https://doi.org/10.1007/s00265-005-0010-2 CrossRefGoogle Scholar
  56. Uhl G, Nessler SH, Schneider JM (2007) Copulatory mechanism in a sexually cannibalistic spider with genital mutilation (Araneae: Araneidae: Argiope bruennichi). Zoology 110:398–408.  https://doi.org/10.1016/j.zool.2007.07.003 CrossRefPubMedGoogle Scholar
  57. Uhl G, Nessler SH, Schneider JM (2009) Securing paternity in spiders? A review on occurrence and effects of mating plugs and male genital mutilation. Genetica 138:75–104.  https://doi.org/10.1007/s10709-009-9388-5 CrossRefGoogle Scholar
  58. Uhl G, Nessler SH, Schneider JM (2010) Securing paternity in spiders? A review on occurrence and effects of mating plugs and male genital mutilation. Genetica 138:75–104.  https://doi.org/10.1007/s10709-009-9388-5 CrossRefPubMedGoogle Scholar
  59. Uhl G, Zimmer SM, Renner D, Schneider JM (2015) Exploiting a moment of weakness: male spiders escape sexual cannibalism by copulating with moulting females. Sci Rep 5:16928.  https://doi.org/10.1038/srep16928 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Venables W, Ripley B (2002) Modern applied statistics with S. Springer, New YorkCrossRefGoogle Scholar
  61. Welke KW, Schneider JM (2009) Inbreeding avoidance through cryptic female choice in the cannibalistic orb-web spider Argiope lobata. Behav Ecol 20:1056–1062CrossRefGoogle Scholar
  62. Welke KW, Schneider JM (2012) Sexual cannibalism benefits offspring survival. Anim Behav 83:201–207.  https://doi.org/10.1016/j.anbehav.2011.10.027 CrossRefGoogle Scholar
  63. Wilder SM, Rypstra AL (2008a) Sexual size dimorphism predicts the frequency of sexual cannibalism within and among species of spiders. Am Nat 172:431–440CrossRefGoogle Scholar
  64. Wilder SM, Rypstra AL (2008b) Diet quality affects mating behaviour and egg production in a wolf spider. Anim Behav 76:439–445.  https://doi.org/10.1016/j.anbehav.2008.01.023 CrossRefGoogle Scholar
  65. Zimmer SM, Welke KW, Schneider JM (2012) Determinants of natural mating success in the cannibalistic orb-web spider Argiope bruennichi. PLoS One 7:e31389.  https://doi.org/10.1371/journal.pone.0031389 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Zuur AF, Ieno EN (2016) A protocol for conducting and presenting results of regression-type analyses. Methods Ecol Evol 7:636–645.  https://doi.org/10.1111/2041-210X.12577 CrossRefGoogle Scholar
  67. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14.  https://doi.org/10.1111/j.2041-210X.2009.00001.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiologyAdelphi UniversityGarden CityUSA
  2. 2.Department of Biology, Intercollege Graduate Degree Program in EcologyThe Pennsylvania State UniversityState CollegeUSA

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