Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE (Open Access)

The extraordinary mating system of Zeus bugs (Heteroptera : Veliidae : Phoreticovelia sp.)*

Göran Arnqvist A C , Therésa M. Jones B and Mark A. Elgar B
+ Author Affliations
- Author Affliations

A Department of Animal Ecology, Evolutionary Biology Centre, Norbyv. 18D, University of Uppsala, SE-752 36 Uppsala, Sweden.

B Department of Zoology, The University of Melbourne, Vic. 3010, Australia.

C Corresponding author. Email: goran.arnqvist@ebc.uu.se

Australian Journal of Zoology 55(2) 131-137 https://doi.org/10.1071/ZO06090
Submitted: 3 November 2006  Accepted: 28 February 2007   Published: 28 May 2007

Abstract

Wingless female Zeus bugs (genus: Phoreticovelia) produce a secretion from dorsal glands that males feed upon when riding on females. This unique form of sex-role-reversed nuptial feeding may have set the stage for an unusual mating system. Here, we provide natural history details of the mating behaviour for two Zeus bug species. While these species have many mating behaviours in common, the wing morphs within species exhibit entirely different mating strategies. Adult wingless females are ridden permanently by adult wingless males. In the wild, adult sex-ratios among the wingless morph are male-biased; few unmounted adult females exist and many males instead ride immature females who also produce glandular secretions. In contrast, sex-ratios among the winged morph is not male-biased, sexual size dimorphism is less pronounced, females have no dorsal glands and are, consequently, not ridden by males. Field and laboratory observations show that mating is strongly assortative by wing morph. This assortment may allow evolutionary divergence between the two morphs. We discuss the implications of this mating system and suggest that it adds to those studies showing that sexually antagonistic coevolution can be a driver of mating system evolution.


Acknowledgements

We thank two anonymous referees for their invaluable comments; the Queensland Parks and Wildlife Service for permissions to sample Zeus bugs in the field; and the Australian Research Council (Grant No. DP0583994) and The Swedish Research Council for financial support.


References

Amano, H. , and Hayashi, K. (1998). Costs and benefits for water strider (Aquarius paladum) females of carrying guarding, reproductive males. Ecological Research 13, 263–272.
CrossRef |

Andersen, N. M. , and Weir, T. A. (2001). New genera of Veliidae (Hemiptera: Heteroptera) from Australia, with notes on the generic classification of the subfamily Microveliinae. Invertebrate Taxonomy 15, 217–258.
CrossRef |

Andersson, M. (2005). Evolution of classical polyandry: three steps to female emancipation. Ethology 111, 1–23.
CrossRef |

Arnqvist G. (1997). The evolution of water strider mating systems: causes and consequences of sexual conflicts. In ‘The Evolution of Mating Systems in Insects and Arachnids’. (Eds J. C. Choe and B. J. Crespi.) pp. 146–163. (Cambridge University Press: Cambridge.)

Arnqvist G., and Rowe L. (2005). ‘Sexual Conflict.’ (Princeton University Press: Princeton, NJ.)

Arnqvist, G. , Jones, T. M. , and Elgar, M. A. (2003). Reversal of sex roles in nuptial feeding. Nature 424, 387.
CrossRef | PubMed |

Arnqvist, G. , Jones, T. M. , and Elgar,, M. A. (2006). Sex-role reversed nuptial feeding reduces male kleptoparasitism of females in Zeus bugs. Biology Letters 2, 491–493.
CrossRef | PubMed |

Arnqvist, G. , Rowe, L. , Krupa, J. , and Sih, A. (1996). Assortative mating by size: a meta-analysis of mating patterns in water striders. Evolutionary Ecology 10, 265–284.
CrossRef |

Bennett N. C., and Faulkes C. G. (2000). ‘African Mole-rats: Ecology and Eusociality.’ (Cambridge University Press: Cambridge.)

Bolnick, D. I. (2004). Waiting for sympatric speciation. Evolution 58, 895–899.
CrossRef | PubMed |

Crow, J. F. , and Felsenstein, J. (1968). The effect of assortative mating on the genetic composition of a population. Eugenics Quarterly 15, 85–91.
PubMed |

Deinert, E. I. , Longino, J. T. , and Gilbert, L. E. (1994). Mate competition in butterflies. Nature 370, 23–24.
CrossRef |

Denno, R. F. , and Peterson, M. A. (2000). Caught between the devil and the deep blue sea, mobile planthoppers elude natural enemies and deteriorating host plants. American Entomologist 46, 95–109.


Dieckmann, U. , and Doebeli, M. (1999). On the origin of species by sympatric speciation. Nature 400, 354–357.
CrossRef | PubMed |

Elgar M. A. (1998). Sperm competition and sexual selection in spiders and other arachnids. In ‘Sperm Competition and Sexual Selection’. (Eds T. R. Birkhead and A. P. Møller.) pp. 307–339. (Academic Press: New York.)

Elgar, M. A. , and Schneider, J. M. (2004). Evolutionary significance of sexual cannibalism. Advances in the study of Animal Behavior , 135–163.


Emlen, S. T. , and Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science 197, 215–223.
CrossRef | PubMed |

Fairbairn, D. J. (1988). Sexual selection for homogamy in the Gerridae: an extension of Ridely’s comparative approach. Evolution 42, 1212–1222.
CrossRef |

Frith C., and Frith D. (2004). ‘The Bowerbirds.’ (Oxford University Press: Oxford.)

Fromhage, L. , Elgar, M. A. , and Schneider, J. M. (2005). Faithful without care: the evolution of monogyny. Evolution 59, 1400–1405.
CrossRef | PubMed |

Höglund J., and Alatalo R. V. (1995). ‘Leks.’ (Princeton University Press: Princeton, NJ.)

Houde A. E. (1997). ‘Sex, Color, and Mate Choice in Guppies.’ (Princeton University Press: Princeton, NJ.)

Jormalainen, V. (1998). Precopulatory mate guarding in crustaceans: male competitive strategy and intersexual conflict. Quarterly Review of Biology 73, 275–304.
CrossRef |

Koenig W., and Dickinson J. (2004). ‘Ecology and Evolution of Cooperative Breeding in Birds.’ (Cambridge University Press: Cambridge.)

Munday, P. L. , Buston, P. M. , and Warner, R. R. (2006). Diversity and flexibility of sex-change strategies in animals. Trends in Ecology & Evolution 21, 89–95.
CrossRef |

Parker G. A. (1979). Sexual selection and sexual conflict. In ‘Sexual Selection and Reproductive Competition in Insects’. (Eds M. S. Blum and N. A. Blum.) pp. 123–163. (Academic Press: New York.)

Polhemus, D. A. , and Polhemus, J. T. (2000). Additional new genera and species of Microveliinae (Heteroptera: Veliidae) from New Guinea and adjacent regions. Tijdschrift voor Entomologie 143, 91–123.


Rice, W. R. (1996). Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381, 232–234.
CrossRef | PubMed |

Roff, D. A. , and Fairbairn, D. J. (1991). Wing dimorphisms and the evolution of migratory polymorphisms among the Insecta. American Zoologist 31, 243–251.


Shuster S. M., and Wade M. J. (2003). ‘Mating Systems and Strategies.’ (Princeton University Press: Princeton, NJ.)

Spence, J. R. (1989). The habitat templet and life-history strategies of pond skaters (Heteroptera: Gerridae) – reproductive potential, phenology, and wing polymorphism. Canadian Journal of Zoology 67, 2432–2447.


Spence, J. R. , and Andersen, N. M. (1994). The biology of water striders – interactions between systematics and ecology. Annual Review of Entomology 39, 101–128.
CrossRef |




* This contribution is dedicated to the memory of Nils Møller Andersen, whose pioneering work on the biology and systematics of semiaquatic Heteroptera is a continual source of inspiration.

Full Text PDF (240 KB) Export Citation Cited By (6)