Skip to main content
SpringerLink
Log in

Does traumatic secretion transfer manipulate mating roles or reproductive output in a hermaphroditic sea slug?

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Copulation in the simultaneous hermaphrodite Siphopteron sp. involves injection of prostate fluids into the mating partner with a stylet-shaped penile appendage before insemination. It has been hypothesised that such traumatic secretion transfer manipulates sex roles or the recipient’s short-term reproductive output. To test manipulative effects of traumatic secretion transfer, we ablated the stylet of male-acting individuals and then paired them to untreated focal individuals. Mating behaviour and egg output of focal individuals was then compared between this ‘no injection group’ and a ‘control group’ with sham-treated mating partners. We found that penile stylets were inserted at different areas prior to and during insemination, but prostate fluid injection was restricted to the first phase. Here, injections were into the anterior foot region, indicating that prostate secretions target the nearby male or female copulatory tracts. Our experimental manipulation of traumatic secretion transfer did not affect the exhibited mating roles. Matings in both treatments were usually reciprocal so that both partners acted in the male as well as female mating role. Moreover, sperm recipient reproductive output did not differ between treatments. We conclude that traumatic secretion transfer in this species either affects currently unmeasured traits, for instance the donor’s paternity share, or that these sea slugs are so well-adapted to traumatic secretion transfer that the effects were too subtle to be detected in our current assays.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11(7):36–42

    Google Scholar 

  • Anthes N (2010) Mate choice and reproductive conflict in simultaneous hermaphrodites. In: Kappeler P (ed) Animal behaviour: evolution and mechanisms. Springer, Berlin. doi:10.1007/978-3-642-02624-9_12

  • Anthes N, Michiels NK (2005) Do “sperm trading” simultaneous hermaphrodites always trade sperm? Behav Ecol 16:188–195

    Article  Google Scholar 

  • Anthes N, Michiels NK (2007a) Precopulatory stabbing, hypodermic injections and unilateral matings in a hermaphroditic sea slug. Biol Lett 3:121–124

    Article  PubMed  Google Scholar 

  • Anthes N, Michiels NK (2007b) Reproductive morphology, mating behaviour, and spawning ecology of cephalaspid sea slugs (Aglajidae and Gastropteridae). Invertebr Biol 126(4):335–365

    Article  Google Scholar 

  • Anthes N, Putz A, Michiels NK (2006a) Hermaphrodite sex role preferences: the role of partner body size, mating history and female fitness in the sea slug Chelidonura sandrana. Behav Ecol Sociobiol 60:359–367

    Article  Google Scholar 

  • Anthes N, Putz A, Michiels NK (2006b) Sex role preferences, gender conflict and sperm trading in simultaneous hermaphrodites: a new framework. Anim Behav 72:1–12

    Article  Google Scholar 

  • Arnqvist G, Rowe L (2005) Sexual conflict. Monographs in behavior and ecology. Princeton University Press, Princeton

    Google Scholar 

  • Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF (2011) Insect seminal fluid proteins: identification and function. Annu Rev Entomol 56(1):21–40

    Article  PubMed  CAS  Google Scholar 

  • Backhouse A, Sait SM, Cameron TC (2012) Multiple mating in the traumatically inseminating Warehouse pirate bug, Xylocoris flavipes: effects on fecundity and longevity. Biol Lett 8(5):706–709. doi:10.1098/rsbl.2012.0091

    Article  PubMed  Google Scholar 

  • Bates D, Sarkar D (2007) lme4: Linear mixed-effects models using S4 classes.

  • Blanckenhorn WU, Hosken DJ, Martin OY, Reim C, Teuschl Y, Ward PI (2002) The costs of copulating in the dung fly Sepsis cynipsea. Behav Ecol 13(3):353–358

    Article  Google Scholar 

  • Charnov EL (1979) Simultaneous hermaphroditism and sexual selection. PNAS 76(5):2480–2484

    Article  PubMed  CAS  Google Scholar 

  • Chase R, Blanchard KC (2006) The snail’s love-dart delivers mucus to increase paternity. Proc R Soc B 273:1471–1475

    Article  PubMed  Google Scholar 

  • Chung DJD (1986) Stimulation of genital eversion in the land snail Helix aspersa by extracts of the glands of the dart apparatus. J Exp Zool 238(2):129–139

    Article  Google Scholar 

  • Fox CW, Czesak ME (2000) Evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 45:341–369. doi:10.1146/annurev.ento.45.1.341

    Article  PubMed  CAS  Google Scholar 

  • Gosliner TM (1989) Revision of the Gastropteridae (Opisthobranchia: Cephalaspidea) with descriptions of a new genus and six new species. Veliger 32:333–381

    Google Scholar 

  • Hoffer J, Ellers J, Koene J (2010) Costs of receipt and donation of ejaculates in a simultaneous hermaphrodite. BMC Evol Biol 10(1):393

    Article  PubMed  Google Scholar 

  • Houck LD, Reagan NL (1990) Male courtship pheromones increase female receptivity in a plethodontid salamander. Anim Behav 39:729–734. doi:10.1016/s0003-3472(05)80384-7

    Article  Google Scholar 

  • Ito K (1997) Egg-size and -number variations related to maternal size and age, and the relationship between egg size and larval characteristics in an annual marine gastropod, Haloa japonica (Opisthobranchia; Cephalaspidea). Mar Ecol Prog Ser 152(1–3):187–195

    Article  Google Scholar 

  • Koene JM, Pförtner T, Michiels NK (2005) Piercing the partner’s skin influences sperm uptake in the earthworm Lumbricus terrestris. Behav Ecol Sociobiol 59:243–249

    Article  Google Scholar 

  • Koene JM, Sloot W, Montagne-Wajer K, Cummins SF, Degnan BM, Smith JS, Nagle GT, ter Maat A (2010) Male accessory gland protein reduces egg laying in a simultaneous hermaphrodite. PLoS One 5(4): Article No.: e10117. doi:10.1371/journal.pone.0010117

  • Koene JM, Sundermann G, Michiels NK (2002) On the function of body piercing during copulation in earthworms. Invertebr Reprod Dev 41:35–40

    Article  Google Scholar 

  • Koene JM, ter Maat A (2001) “Allohormones”: a class of bioactive substances favoured by sexual selection. J Comp Physiol A 187(5):323–326

    Article  PubMed  CAS  Google Scholar 

  • Lange R, Gerlach T, Beninde J, Werminghausen J, Reichel V, Anthes N (2012) Female fitness optimum at intermediate mating rates under traumatic mating. PLoS One 7(8):e43234. doi:10.1371/journal.pone.0043234

    Article  PubMed  CAS  Google Scholar 

  • Lange R, Reinhardt K, Michiels NK, Anthes N (2013) Functions, diversity, and evolution of traumatic mating. Biol Rev. doi:10.1111/brv.12018

    PubMed  Google Scholar 

  • Leonard JL, Lukowiak K (1984) Male–female conflict in a simultaneous hermaphrodite resolved by sperm trading. Am Nat 124:282–286

    Article  Google Scholar 

  • Marshall DJ, Keough MJ (2008) The evolutionary ecology of offspring size in marine invertebrates. Adv Mar Biol 53:1–60. doi:10.1016/s0065-2881(07)53001-4. Editor: Sims DW (ed) Elsevier Academic Press Inc, San Diego

  • Michiels NK (1998) Mating conflicts and sperm competition in simultaneous hermaphrodites. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, London, pp 219–254

    Chapter  Google Scholar 

  • Michiels NK, Newman LJ (1998) Sex and violence in hermaphrodites. Nature 391:647

    Article  CAS  Google Scholar 

  • Morrow EH, Arnqvist G (2003) Costly traumatic insemination and a female counter-adaptation in bed bugs. Proc R Soc Lond - B Biol Sci 270:2377–2381

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RDC (2013) nlme: linear and nonlinear mixed effects models. R package version 3.1-108,

  • R Development Core Team (2012) R: A Language and Environment for Statistical Computing. 2.15.0 edn. R Foundation for Statistical Computing, Vienna, Austria

  • Reinhardt K, Naylor RA, Siva-Jothy MT (2003) Reducing a cost of traumatic insemination: female bed bugs evolve a unique organ. Proc R Soc Lond - B Biol Sci 270:2371–2375

    Article  Google Scholar 

  • Sakai S, Harada Y (2001) Why do large mothers produce large offspring? Theory and a test. Am Nat 157(3):348–359

    Article  PubMed  CAS  Google Scholar 

  • Sirot LK, Wolfner MF, Wigby S (2011) Protein-specific manipulation of ejaculate composition in response to female mating status in Drosophila melanogaster. PNAS 108(24):9922–9926. doi:10.1073/pnas.1100905108

    Article  PubMed  CAS  Google Scholar 

  • Smith PH, Brown LB, Vangerwen ACM (1989) Causes and correlates of loss and recovery of sexual receptivity in Lucilia cuprina females after their 1st mating. J Insect Behav 2(3):325–337. doi:10.1007/bf01068059

    Article  Google Scholar 

  • Smith PH, Gillott C, Browne LB, Vangerwen ACM (1990) The mating-induced refractoriness of Lucilia cuprina females—manipulating the male contribution. Physiol Entomol 15(4):469–481

    Article  Google Scholar 

  • Smolensky N, Romero MR, Krug PJ (2009) Evidence for costs of mating and self-fertilization in a simultaneous hermaphrodite with hypodermic insemination, the opisthobranch Alderia willowi. Biol Bull 216(2):188–199

    PubMed  Google Scholar 

  • Sprenger D, Anthes N, Michiels NK (2008a) Multiple mating affects offspring size in the opisthobranch Chelidonura sandrana. Mar Biol 153:891–897

    Article  Google Scholar 

  • Sprenger D, Faber J, Michiels NK, Anthes N (2008b) Natural female mating rate maximizes hatchling size in a marine invertebrate. J Anim Ecol 77(4):696–701. doi:10.1111/j.1365-2656.2008.01376.x

    Article  CAS  Google Scholar 

  • Sprenger D, Lange R, Anthes N (2011) Population density and group size effects on reproductive behavior in a simultaneous hermaphrodite. BMC Evol Biol 11:107. doi:10710.1186/1471-2148-11-107

  • Stutt AD, Siva-Jothy MT (2001) Traumatic insemination and sexual conflict in the bed bug Cimex lectularius. PNAS 98(10):5683–5687

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Anne Hoggett, Marianne & Lance Pearce and Lyle Vail from Lizard Island Research station for invaluable support during field work. Comments by Jack O’Connor, Katja Heubel and three anonymous referees helped to improve earlier versions of this manuscript. The German Science Foundation (DFG) provided funds for field work and manuscript preparation (AN549/2-1).

Ethical standards

The experiment reported in this article complies with the current laws of Australia and a permit had been acquired to collect and perform experiments on Siphopteron sp. (GBRMPA permit no G09/30973.1).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Animal Evolutionary Ecology Group, Faculty of Sciences, University of Tuebingen, Auf der Morgenstelle 28, 72076, Tuebingen, Germany

    Rolanda Lange, Johanna Werminghausen & Nils Anthes

Authors
  1. Rolanda Lange
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Johanna Werminghausen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nils Anthes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rolanda Lange.

Additional information

Communicated by M. Elgar

Electronic supplementary material

Below is the link to the electronic supplementary material.

(MPG 13005 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lange, R., Werminghausen, J. & Anthes, N. Does traumatic secretion transfer manipulate mating roles or reproductive output in a hermaphroditic sea slug?. Behav Ecol Sociobiol 67, 1239–1247 (2013). https://doi.org/10.1007/s00265-013-1551-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-013-1551-4

Keywords

Search

Navigation