Elsevier

Animal Behaviour

Volume 81, Issue 5, May 2011, Pages 933-939
Animal Behaviour

Eunuchs are better fighters

https://doi.org/10.1016/j.anbehav.2011.02.010Get rights and content

Genital amputation, that is, genital damage or loss, seems maladaptive because it renders the amputee functionally sterile, but is nevertheless common in sexually dimorphic spiders. In these species, male genital amputation correlates with plugging of female genitals and with sexual cannibalism. Genital amputation in male spiders may be partial or full; the latter is known as the eunuch phenomenon. We tested two adaptive hypotheses about eunuch behaviour in an orb web spider, Nephilengys malabarensis: (1) the plugging hypothesis (i.e. broken male genitals (palps) effectively plug the female genitals) and (2) the better fighter hypothesis (i.e. eunuch males are better fighters than their intact rivals). By staging mating trials, we documented genital amputation (occurrence and frequency), sexual cannibalism and genital organ reuse, morphologically examined plugs to infer their effectiveness, and conducted a series of male–male contests to determine whether eunuch males were better fighters. Copulations always resulted in amputation of the palps: 87.5% of males became eunuchs directly during copulation and plugged females, while 12.5% of males first partially damaged the palps and then severed them after copulation. Sexual cannibalism and plugging effectiveness both reached 75%. Eunuchs guarded females, were highly aggressive and active, and initiated and won contests more often, whereas intact males and half-eunuchs showed significantly lower levels of guarding behaviour, aggression and general activity. Thus, both hypotheses are supported and we conclude that the eunuch phenomenon is adaptive.

Section snippets

Study System

We collected N. malabarensis spiders between December 2009 and January 2010 in Singapore: Labrador Park (1°15′58″N, 103°48′10″E), Pulau Ubin (1°24′30″N, 103°57′40″E) and Kent Ridge Park (1°17′10″N, 103°47′10″E). To examine rematings using the same genital organ, we needed spiders with known mating histories. Therefore, we collected subadults and reared them to adulthood in the laboratory (N = 21, N = 14). In addition to subadults, we collected adult females and males for contest trials (N = 20, N =

Results

In N. malabarensis, a male placed on the female’s web usually starts courtship by plucking the threads of the web, and attaching silk to it. If the female shows receptive behaviour, that is, she orients towards the male or comes out of the retreat the male eventually establishes physical contact and climbs onto her dorsal abdomen. The male then switches to her venter and attempts to insert one of the palps (see Supplementary Material, Video and Fig. S1). Figure 2 shows a detailed ethogram of

Discussion

Male N. malabarensis exhibit obligatory damage to their genitals during copulation either through direct or indirect amputation, the latter involving initial sclerite damage followed by subsequent, voluntary palpal removal. Their obligate genital amputation (direct or indirect), also termed the eunuch phenomenon, may be logical from the perspective of very limited sperm in each palp; new research shows that their palps can be charged only once because spermiogenesis in this species, as in

Acknowledgments

We thank Mark Elgar and an anonymous referee for their most helpful reviews, Jutta Schneider and Mariella Herberstein for commenting on our experimental design, and Ingi Agnarsson for commenting on the manuscript. Cene Fišer and Irena Kuntner kindly offered logistic help and Singapore National Parks supplied the research and collection permits. This work was funded by grants to M.K. from the Slovenian Research Agency (J1-2063) and the Raffles Museum for Biodiversity Research Fellowship,

References (49)

  • J.J. Boomsma et al.

    The evolution of male traits in social insects

    Annual Review of Entomology

    (2005)
  • T.E. Christenson et al.

    Costs and benefits of male–male competition in the orb weaving spider, Nephila clavipes

    Behavioral Ecology and Sociobiology

    (1979)
  • J.A. Downes

    Feeding and mating in the insectivorous Ceratopogoninae (Diptera)

    Memoirs of the Entomological Society of Canada

    (1978)
  • W.G. Eberhard

    Female Control: Sexual Selection by Cryptic Female Choice

    (1996)
  • M.A. Elgar

    Sperm competition and sexual selection in spiders and other arachnids

  • M.A. Elgar et al.

    Female control of paternity in the sexually cannibalistic spider Argiope keyserlingi

    Proceedings of the Royal Society B

    (2000)
  • M.W. Foellmer et al.

    Spontaneous male death during copulation in an orb-weaving spider

    Proceedings of the Royal Society B

    (2003)
  • L. Fromhage et al.

    Safer sex with feeding females: sexual conflict in a cannibalistic spider

    Behavioral Ecology

    (2005)
  • L. Fromhage et al.

    Emasculation to plug up females: the significance of pedipalp damage in Nephila fenestrata

    Behavioral Ecology

    (2006)
  • L. Fromhage et al.

    Faithful without care: the evolution of monogyny

    Evolution

    (2005)
  • B.A. Huber

    Sexual selection research on spiders: progress and biases

    Biological Reviews

    (2005)
  • B. Knoflach et al.

    Palpal loss, single palp copulation and obligatory mate consumption in Tidarren cuneolatum (Tullgren, 1910) (Araneae, Theridiidae)

    Journal of Natural History

    (2000)
  • B. Knoflach et al.

    Tidarren argo sp nov (Araneae: Theridiidae) and its exceptional copulatory behaviour: emasculation, male palpal organ as a mating plug and sexual cannibalism

    Journal of Zoology

    (2001)
  • M. Kuntner

    A revision of Herennia (Araneae: Nephilidae: Nephilinae), the Australasian ‘coin spiders’

    Invertebrate Systematics

    (2005)
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    1

    S. Zhang and D. Li are at the Department of Biological Sciences, National University of Singapore, 14 Sciences Drive 4, 117543 Singapore.

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