Immature mating as a tactic of polygynous male western widow spiders

Abstract

In polygynous species, males typically mate with more than one female, and male investment in any one mating should decrease if securing that mating reduces future mating opportunities. In contrast, monogynous males mate only once, so they should invest maximally in that single mating. In two monogynous, sexually cannibalistic Latrodectus spider species (L. geometricus, L. hasselti), males can mate and fertilize immature females. This recently described tactic is time-consuming because males must wait days for females to be capable of mating. It is also risky since immature females approached too early may kill males outright. However, if males typically find only one female in their lifetime, increasing the opportunity to mate may be worth these costs. We investigated whether this tactic is also practiced by a polygynous congener, L. hesperus, in which males typically mate more than once and may avoid time-consuming, risky encounters. In laboratory trials, we showed that males copulate with immature females. Moreover, males mounted immatures more rapidly, copulated for longer, and fathered more offspring than males that mated adults females. We concluded that monogyny is not a necessary condition for immature mating to be favored as an alternative reproductive tactic and suggest that it may be common in other spider taxa.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Andrade MCB, Banta EM (2002) Value of male remating and functional sterility in redback spiders. Anim Behav 63:857–870

    Article  Google Scholar 

  2. Andrade MCB, Kasumovic MM (2005) Terminal investment strategies and male mate choice: extreme test of Bateman. Integr Comp Biol 45:838–847

    Article  Google Scholar 

  3. Andrade MCB, MacLeod EC (2015) Potential for CFC in black widows (genus Latrodectus): mechanisms and social context. In: Peretti AV, Aisenberg A (eds) Cryptic female choice in arthropods – patterns, Mechanisms and Prospects. Springer International Publishers Inc., Berlin, pp 27–53

    Google Scholar 

  4. Baruffaldi L, Andrade MCB (2015) Contact pheromones mediate male preference in black widow spiders: avoidance of hungry sexual cannibals? Anim Behav 102:25–32

    Article  Google Scholar 

  5. Baruffaldi L, Andrade MCB (2017) Neutral fitness outcomes contradict inferences of sexual ‘coercion’ derived from male’s damaging mating tactic in a widow spider. Sci Rep 7:17322

    Article  Google Scholar 

  6. Biaggio MD, Sandomirsky I, Lubin Y, Harari AR, Andrade MCB (2016) Copulation with immature females increases male fitness in cannibalistic widow spiders. Biol Lett 12:20160516

    Article  Google Scholar 

  7. Estrada C, Yildizhan S, Schulz S, Gilbert LE (2009) Sex-specific chemical cues from immatures facilitate the evolution of mate guarding in Heliconius butterflies. Proc R Soc Lond [Biol] 277:1680

    Google Scholar 

  8. Fromhage L, Elgar MA, Schneider JM (2005) Faithful without care: the evolution of monogyny. Evolution 59:1400–1405

    Article  Google Scholar 

  9. Herberstein ME, Painting CJ, Holwell GI (2017) Scramble competition polygyny in terrestrial arthropods. In: Naguib M, Podos J, Simmons LW, Barrett L, Healy SD, Zuk M (eds) Advances in the study of behavior. Elsevier, Cambridge, pp 237–295

    Google Scholar 

  10. Johnson JC, Trubl P, Blackmore V, Miles L (2011) Male black widows court well-fed females more than starved females: silken cues indicate sexual cannibalism risk. Anim Behav 82:383–390

    Article  Google Scholar 

  11. Kuntner M, Agnarsson I, Li D (2014) The eunuch phenomenon: adaptive evolution of genital emasculation in sexually dimorphic spiders. Biol Rev 90:279–296

    Article  Google Scholar 

  12. MacLeod EC, Andrade MCB (2014) Strong, convergent male mate choice along two preference axes in field populations of black widow spiders. Anim Behav 89:163–169

    Article  Google Scholar 

  13. Parker GA (1974) Courtship persistence and female-guarding as male time investment strategies. Behaviour 48:157–183

    Article  Google Scholar 

  14. Schneider JM, Fromhage L (2010) Monogynous mating strategies in spiders. In: Kappeler P (ed) Animal behaviour: evolution and mechanisms. Springer International Publishers Inc., Berlin, pp 441–464

    Google Scholar 

  15. Scott CE, McCann S, Andrade MCB (2019) Male black widows parasitize mate-searching effort of rivals to find females faster. Proc R Soc B 20191470

    Article  Google Scholar 

  16. Stoltz JA, Andrade MCB (2010) Female's courtship threshold allows intruding males to mate with reduced effort. Proc R Soc B 277:585–592

    CAS  Article  Google Scholar 

  17. Stoltz JA, Elias DO, Andrade MCB (2009) Male courtship effort determines female response to competing rivals in redback spiders. Anim Behav 77:79–85

    Article  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. Waner S, Motro U, Lubin Y, Harari AR (2018) Male mate choice in a sexually cannibalistic widow spider. Anim Behav 137:189–196

    Article  Google Scholar 

Download references

Acknowledgments

We thank S. Fry for collecting L. hesperus, Andrade lab volunteers for rearing spiders. We specially thank to C. Scott, reviewers and editors for their comments on the manuscript.

Funding

The work was funded by an NSERC Discovery grant to MCBA.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Luciana Baruffaldi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was conducted in accordance with animal care guidelines at the University of Toronto.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by: Matjaž Gregorič

Electronic supplementary material

ESM 1

(DOCX 15 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Baruffaldi, L., Andrade, M.C.B. Immature mating as a tactic of polygynous male western widow spiders. Sci Nat 107, 6 (2020). https://doi.org/10.1007/s00114-019-1663-4

Download citation

Keywords

  • Polygynous males
  • Immature mating
  • Mating behaviors
  • Fitness correlates