Evolutionary Ecology

, Volume 25, Issue 1, pp 107–119 | Cite as

A paternity advantage for speedy males? Sperm precedence patterns and female re-mating frequencies in a sexually cannibalistic praying mantid

  • Katherine L. Barry
  • Gregory I. Holwell
  • Marie E. Herberstein
Original Paper


Scramble competition polygyny is expected when females and/or resources are widely dispersed and not easily monopolized by males, or when there is an abundance of mates during an extremely restricted reproductive period. Additional factors such as first male sperm precedence or low female re-mating rate might further explain the propensity of males to engage in scramble competition. The sexually cannibalistic praying mantid Pseudomantis albofimbriata exhibits a polygynous mating system, where females exist in low-density populations and male competition manifests as the race to find females rather than as direct physical fighting. Here, we aim to determine whether there is a paternity advantage for the first-male to mate and/or a low frequency of female re-mating. First, we determined sperm precedence patterns in P. albofimbriata using the sterile male technique. Second, we tested the likelihood of female re-mating in P. albofimbriata by comparing the close-range approach behaviour and frequency of successful mating attempts for males when paired with virgin as opposed to recently mated females, and by comparing the frequency of long-distance male attraction between virgin and mated females. We found no paternity advantage for the first male to mate, rather a second male advantage. Although mated females were not rejected by males when approached from close-range, they were chemically unattractive to males searching from a distance. Since initial mate attraction in many praying mantids, including P. albofimbriata, is mediated via long-distance chemical communication, we believe the latter result is more ecologically relevant and therefore more important. These results suggest that the relatively low frequency of female re-mating observed in P. albofimbriata may be an additional factor driving scramble competition in this system.


Sperm precedence Paternity allocation Female re-mating Scramble competition Praying mantid Pseudomantis albofimbriata 



Many thanks to Jody Tropiano, Louise Allen and Katy Breakwell for help with mantid collection and maintenance, and to Fernando Soley and Katy Breakwell for assistance with experiments. To Darrell Kemp and two anonymous reviewers for their helpful comments regarding the manuscript and to Macquarie University and the Linnean Society of NSW for funding this research.


  1. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  2. Andrade MCB (1996) Sexual selection for male sacrifice in the Australian redback spider. Science 271:70–72CrossRefGoogle Scholar
  3. Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, PrincetonGoogle Scholar
  4. Austad SN (1982) 1st male sperm priority in the bowl and doily spider. Frontinella pyramitela (Walckenaer) Evolution 36:777–785Google Scholar
  5. Austad SN (1984) Evolution of sperm priority patterns in spiders. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, London, pp 223–249Google Scholar
  6. Barry KL (in review) Influence of nutritional status on mating dynamics in a sexually cannibalistic praying mantid. Animal BehavGoogle Scholar
  7. Barry KL, Kokko H (in press) Male mate choice: why sequential choice can make its evolution difficult. Animal BehavGoogle Scholar
  8. Barry KL, Holwell GI, Herberstein ME (2008) Female praying mantids use sexual cannibalism as a foraging strategy to increase fecundity. Behav Ecol 19:710–715CrossRefGoogle Scholar
  9. Barry KL, Holwell GI, Herberstein ME (2009) Male mating behaviour reduces the risk of sexual cannibalism in an Australian praying mantid. J Ethol 27:377–383CrossRefGoogle Scholar
  10. Barry KL, Holwell GI, Herberstein ME (2010) Multimodal mate assessment by male praying mantids in a sexually cannibalistic mating system. Animal Behav 79(5):1165–1172Google Scholar
  11. Bertin A, Cezilly F (2003) Sexual selection, antennae length and the mating advantage of large males in Asellus aquaticus. J Evol Biol 16:698–707CrossRefPubMedGoogle Scholar
  12. Berwaerts K, Van Dyck H (2004) Take-off performance under optimal and suboptimal thermal conditions in the butterfly Pararge aegeria. Oecologia 141:536–545CrossRefPubMedGoogle Scholar
  13. Birkhead TR, Lee KE, Young P (1988) Sexual Cannibalism in the praying mantis Hierodula membranacea. Behaviour 106:112–118CrossRefGoogle Scholar
  14. Bonduriansky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev 76:305–339CrossRefPubMedGoogle Scholar
  15. Boorman EB, Parker GA (1976) Sperm (ejaculate) competition in Drosophila melanogaster and the reproductive value of females to males in relation to female age and mating status. Ecol Entomol 1:145–155CrossRefGoogle Scholar
  16. Bretman A, Fricke C, Chapman T (2009) Plastic responses of male Drosophila melanogaster to the level of sperm competition increase male reproductive fitness. Proc R Soc B-Biol Sci 276:1705–1711CrossRefGoogle Scholar
  17. Carroll SP, Salamon MH (1995) Variation in sexual selection on male body size within and between populations of the soapberry bug. Anim Behav 50:1463–1474CrossRefGoogle Scholar
  18. Chapman T (2001) Seminal fluid-mediated fitness traits in Drosophila. Heredity 87:511–521CrossRefPubMedGoogle Scholar
  19. Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L (1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:241–244CrossRefPubMedGoogle Scholar
  20. Davies NB (1993) Mating systems. In: Krebs JR, Davies NB (eds) An introduction to behavioural ecology. Blackwell, Oxford, pp 263–294Google Scholar
  21. Dickinson JL (1986) Prolonged mating in the milkweed leaf Beetle Labidomera clivicollis clivicollis (Coleoptera: Chrysomelidae): a test of the “Sperm-Loading” hypothesis. Behav Ecol Sociobiol 18:331–338CrossRefGoogle Scholar
  22. Dubey S, Brown GP, Madsen T, Shine R (2009) Sexual selection favours large body size in males of a tropical snake (Stegonotus cucullatus, Colubridae). Anim Behav 77:177–182CrossRefGoogle Scholar
  23. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223CrossRefPubMedGoogle Scholar
  24. Foltz DW, Schwagmeyer PL (1989) Sperm competition in the 13-lined ground squirrel—differential fertilisation success under field conditions. Am Nat 133:257–265CrossRefGoogle Scholar
  25. Foster SP (1993) Neural inactivation of sex-pheromone production in mated ligtbrown apple moths, Epiphyas postvittana (Walker). J Insect Physiol 39:267–273CrossRefGoogle Scholar
  26. Gaskett AC, Herberstein ME, Downes BJ, Elgar MA (2004) Changes in male mate choice in a sexually cannibalistic orb-web spider (Araneae : Araneidae). Behaviour 141:1197–1210CrossRefGoogle Scholar
  27. Gemeno C, Claramunt J, Dasca J (2005) Nocturnal calling behavior in mantids. J Insect Behav 18:389–403CrossRefGoogle Scholar
  28. Hanks LM, Millar JG, Paine TD (1996) Body size influences mating success of the eucalyptus longhorned borer (Coleoptera: Cerambycidae). J Insect Behav 9:369–382CrossRefGoogle Scholar
  29. Holwell GI, Barry KL, Herberstein ME (2007) Mate location, antennal morphology and ecology in two praying mantids (Insecta: Mantodea). Biol J Linn Soc 91:307–313CrossRefGoogle Scholar
  30. Huber BA (2005) Sexual selection research on spiders: progress and biases. Biol Rev 80:363–385CrossRefPubMedGoogle Scholar
  31. Jablonski P, Vepsalainen K (1995) Conflict between sexes in the water strider, Gerris lacustris: a test of two hypotheses for male guarding behavior. Behav Ecol 6:388–392CrossRefGoogle Scholar
  32. Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67CrossRefGoogle Scholar
  33. Kasumovic MM, Andrade MCB (2009) A change in competitive context reverses sexual selection on male size. J Evol Biol 22:324–333CrossRefPubMedGoogle Scholar
  34. Kingan TG, Thomaslaemont PA, Raina AK (1993) Male accessory gland factors elicit change from virgin to mated behavior in the female corn-earworm moth Helicoverpa zea. J Exp Biol 183:61–76Google Scholar
  35. Lawrence S (1991) Sexual Cannibalism in praying Mantids. In: PhD dissertation. University of Sheffield, SheffieldGoogle Scholar
  36. Lelito JP, Brown WD (2008) Mate attraction by females in a sexually cannibalistic praying mantis. Behav Ecol Sociobiol 63:313–320CrossRefGoogle Scholar
  37. Marcotte M, Delisle J, McNeil JN (2003) Pheromonostasis is not directly associated with post-mating sperm dynamics in Choristoneura fumiferana and C. rosaceana females. J Insect Physiol 49:81–90CrossRefPubMedGoogle Scholar
  38. Maxwell MR (1999) Mating behavior. In: Prete FR (ed) The praying Mantids. Johns Hopkins University Press, Baltimore, pp 69–89Google Scholar
  39. Maxwell MR, Barry KL, Johns PM (2010) Examinations of female pheromone use in two praying mantids, Stagmomantis limbata and Tenodera aridifolia sinensis (Mantodea: Mantidae). Ann Entomol Soc Am 100(1):108–114Google Scholar
  40. McNamara KB, Elgar MA, Jones TM (2008) Seminal compounds, female receptivity and fitness in the almond moth, Cadra cautella. Anim Behav 76:771–777CrossRefGoogle Scholar
  41. Moya-Larano J, Vinkovic D, Allard CM, Foellmer MW (2009) Optimal climbing speed explains the evolution of extreme sexual size dimorphism in spiders. J Evol Biol 22:954–963CrossRefPubMedGoogle Scholar
  42. Parker GA (1970) Sperm competition and its evolutionary effect on copula duration in the fly Scatophaga stercoraria. J Insect Physiol 16:1301–1328CrossRefGoogle Scholar
  43. Parker GA (1978) Searching for mates. In: Krebs JR, Davies NB (eds) Behavioral ecology: an evolutionary approach. Sinauer, Sunderland, pp 214–244Google Scholar
  44. Parker GA (1990) Sperm competition games: raffles and roles. Proc R Soc London 242:120–126CrossRefGoogle Scholar
  45. Perampaladas K, Stoltz JA, Andrade MCB (2008) Mated redback spider females re-advertise receptivity months after mating. Ethology 114:589–598CrossRefGoogle Scholar
  46. Perez B (2005) Calling behaviour in the female praying mantis, Hierodula patellifera. Physiol Entomol 30:42–47CrossRefGoogle Scholar
  47. Raina AK, Kingan TG, Giebultowicz JM (1994) Mating-induced loss of sex pheromone and sexual receptivity in insects with emphasis on Helicoverpa zea and Lymantria dispar, pp 317–327Google Scholar
  48. Ramaswamy SB, Qiu Y, Park YI (1996) Neuronal control of post-coital pheromone production in the moth Heliothis virescens. J Exp Zool 274:255–263CrossRefGoogle Scholar
  49. Roberts JA, Uetz GW (2005) Information content of female chemical signals in the wolf spider, Schizocosa ocreata: male discrimination of reproductive state and receptivity. Anim Behav 70:217–223CrossRefGoogle Scholar
  50. Robinson MH, Robinson B (1979) By Dawn’s early light: matutinal mating and sex attractants in a neotropical mantid. Science 205:825–827CrossRefPubMedGoogle Scholar
  51. Schiestl FP, Ayasse M (2000) Post-mating odor in females of the solitary bee, Andrena nigroaenea (Apoidea, Andrenidae), inhibits male mating behavior. Behav Ecol Sociobiol 48:303–307CrossRefGoogle Scholar
  52. Schulz S, Toft S (1993) Identification of a sex pheromone from a spider. Science 260:1635–1637CrossRefPubMedGoogle Scholar
  53. Schwagmeyer PL, Parker GA (1987) Queuing for mates in 13-lined ground squiurrels. Anim Behav 35:1015–1025CrossRefGoogle Scholar
  54. Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, PrincetonGoogle Scholar
  55. Solensky MJ, Oberhauser KS (2009) Male monarch butterflies, Danaus plexippus, adjust ejaculates in response to the intensity of sperm competition. Anim Behav 77:465–472CrossRefGoogle Scholar
  56. Stoltz JA, McNeil JN, Andrade MCB (2007) Males assess chemical signals to discriminate just-mated females from virgins in redback spiders. Anim Behav 74:1669–1674CrossRefGoogle Scholar
  57. Thornhill R, Alcock J (1983) The evolution of insect mating systems. Harvard University Press, CambridgeGoogle Scholar
  58. Tram U, Wolfner MF (1998) Seminal fluid regulation of female sexual attractiveness in Drosophila melanogaster. Proc Nat Acad Sci 95:4051–4054CrossRefPubMedGoogle Scholar
  59. Umbers K (2006) Natural paternity in Ciulfina. In: Honours thesis, Department of Biological Sciences. Macquarie University, SydneyGoogle Scholar
  60. Vencl FV (2004) Allometry and proximate mechanisms of sexual selection in Photinus fireflies, and some other beetles. Soc Integr Comp Biol 242–249Google Scholar
  61. Watson PJ (1986) Transmission of female sex-pheromone thwarted by males in the spider Linyphia litigiosa (Linyphiidae). Science 233:219–221CrossRefPubMedGoogle Scholar
  62. Wiklund C, Forsberg J (1985) Courtship and male discrimination between virgin and mated females in the orange tip butterfly Anthocharis cardamines. Anim Behav 34:328–332CrossRefGoogle Scholar
  63. Winnick CG, Holwell GI, Herberstein ME (2008) Internal reproductive anatomy of the praying mantid Ciulfina klassi (Mantodea: Liturgusidae). Arthropod Struct Dev 38(1):60–69CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Katherine L. Barry
    • 1
  • Gregory I. Holwell
    • 1
    • 2
  • Marie E. Herberstein
    • 1
  1. 1.Department of Biological SciencesMacquarie UniversitySydneyAustralia
  2. 2.School of Biological SciencesUniversity of AucklandAucklandNew Zealand

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