A comparative analysis of the morphology and evolution of permanent sperm depletion in spiders

Peter Michalik, Clare C. Rittschof

Research output: Contribution to journalArticlepeer-review

50 Scopus citations

Abstract

Once thought to be energetically cheap and easy to produce, empirical work has shown that sperm is a costly and limited resource for males. In some spider species, there is behavioral evidence that sperm are permanently depleted after a single mating. This extreme degree of mating investment appears to co-occur with other reproductive strategies common to spiders, e.g. genital mutilation and sexual cannibalism. Here we corroborate that sperm depletion in the golden orb-web spider Nephila clavipes is permanent by uncovering its mechanistic basis using light and electron microscopy. In addition, we use a phylogeny-based statistical analysis to test the evolutionary relationships between permanent sperm depletion (PSD) and other reproductive strategies in spiders. Male testes do not produce sperm during adulthood, which is unusual in spiders. Instead, spermatogenesis is nearly synchronous and ends before the maturation molt. Testis size decreases as males approach their maturation molt and reaches its lowest point after sperm is transferred into the male copulatory organs (pedipalps). As a consequence, the amount of sperm available to males for mating is limited to the sperm contained in the pedipalps, and once it is used, males lose their ability to fertilize eggs. Our data suggest that PSD has evolved independently at least three times within web-building spiders and is significantly correlated with the evolution of other mating strategies that limit males to monogamy, including genital mutilation and sexual cannibalism. We conclude that PSD may be an energy-saving adaptation in species where males are limited to monogamy. This could be particularly important in webbuilding spiders where extreme sexual size dimorphism results in large, sedentary females and small, searching males who rarely feed as adults and are vulnerable to starvation. Future work will explore possible energetic benefits and the evolutionary lability of PSD relative to other mate-limiting reproductive behaviors.

Original languageEnglish
Article numbere16014
JournalPLoS ONE
Volume6
Issue number1
DOIs
StatePublished - 2011

Bibliographical note

Funding Information:
We are especially grateful to Gabriele Uhl (Zoological Institute and Museum, University of Greifswald, Germany) for her invaluable support and helpful discussions. We are indebted to Marion Sandhop (Zoological Institute and Museum, University of Greifswald, Germany) for her technical support especially with the ultramicrotomy, and Oliver Vöcking and Christine Putzar (Zoological Institute and Museum, University of Greifswald, Germany) for rearing the animals. We thank Matjaž Kuntner and Simona Kralj-Fišer (Scientific Research Centre, Slovenian Academy of Sciences and Arts, Ljubljana, Slovenia) for the Nephilengys specimen and Klaas Welke (University of Hamburg, Germany) for the specimen of Argiope lobata. We are grateful to Scott Pitnick (Syracuse University, Syracuse NY, USA), Jutta Schneider (Zoological Institute, University of Hamburg, Germany), and H. Jane Brockmann (University of Florida, USA) for their valuable comments and discussions. We thank the University of Greifswald and the National Science Foundation (DDIG Grant No. IOS-0909367) for financial support, as well as the Ordway-Swisher Biological Station for use of their site for specimen collections.

ASJC Scopus subject areas

  • General Biochemistry, Genetics and Molecular Biology
  • General Agricultural and Biological Sciences
  • General

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