Skip to main content
Log in

Male remating and female fitness in the wolf spider Pardosa astrigera: the role of male mating history

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Although the effects of male mating history on female reproductive output and longevity have been studied in insects, few such studies have been carried out in spiders. In a mating system in which females are monandrous while males are polygynous, females may incur the risk by mating with successful males that have experienced consecutive matings and suffer from the possible depletion of sperm and/or associated ejaculates. Here, we examine the effects of male mating history on male courtship and copulation duration, female reproductive fitness, and female adult longevity of the wolf spider, Pardosa astrigera. Results indicated that male mating frequency had little effect on their subsequent copulation success, and of 35 males tested, about half of the males were able to copulate with five virgin females successively at an interval of 24 h. Male mating history had little effect on their courtship duration. However, male mating history significantly affected male copulation duration, female adult longevity, and reproductive output. Males that mated more frequently copulated longer and more likely failed to cause their mates to produce a clutch, although there was no significant difference in the number of eggs laid and the number of eggs hatched regardless of the first clutch or the second one. Multiple mating of male P. astrigera resulted in significant reduction in female adult longevity. Our results indicate that monandrous females mating with multiple-mated males may incur substantial fitness costs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arnqvist G, Danielsson I (1999) Postmating sexual selection: the effects of male body size and recovery period on paternity and egg production rate in a water strider. Behav Ecol 10:358–365

    Article  Google Scholar 

  • Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164

    Article  PubMed  Google Scholar 

  • Bateman PW (1998) Mate preference for novel partners in the cricket, Gryllus bimaculatus. Ecol Entomol 23:473–475

    Article  Google Scholar 

  • Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic, London

    Google Scholar 

  • Bressac C, Thi Khanh HD, Chevrier C (2009) Effects of age and repeated mating on male sperm supply and paternity in a parasitoid wasp. Entomol Exp Appl 130:207–213

    Article  Google Scholar 

  • Chapman T, Liddle LF, Kaib JM, Wolfner MF, Partridge L (1995) Cost of mating in Drosophila melanogaster females in mediated by male accessory gland productions. Nature 373:241–244

    Article  CAS  PubMed  Google Scholar 

  • Chapman T, Miyatake T, Smith HK, Partridge L (1998) Interactions of mating, egg production and death rates in females of the Mediterranean fruit fly Ceratitis capitata. Proc Roy Soc Lond B Biol 265:1879–1894

    Article  CAS  Google Scholar 

  • Civetta A, Clark AG (2000) Correlated effects of sperm competition and postmating female mortality. Proc Natl Acad Sci USA 97:13162–13165

    Article  CAS  PubMed  Google Scholar 

  • Cook PA (1999) Sperm numbers and female fertility in the moth Plodia interpunctella. J Insect Behav 12:767–779

    Article  Google Scholar 

  • Cordero C (1995) Ejaculate substances that affect female insect reproductive physiology and behavior: honest or arbitrary traits? J Theor Biol 174:453–461

    Article  CAS  Google Scholar 

  • Damiens D, Boivin G (2006) Why do sperm-depleted parasitoid males continue to mate? Behav Ecol 17:138–143

    Article  Google Scholar 

  • Gillot C (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu Rev Entomol 48:163–184

    Article  Google Scholar 

  • Harris WE, Moore PJ (2005) Female mate preference and sexual conflict: females prefer males that have had fewer consorts. Am Nat 165(Suppl):S64–S71

    Article  PubMed  Google Scholar 

  • Hayashi F (1998) Multiple mating and lifetime reproductive output in female dobsonflies that receive nuptial gifts. Ecol Res 13:283–289

    Article  Google Scholar 

  • Holland B, Rice WR (1999) Experimental removal of sexual selection reverses intersexual antagonistic co-evolution and removes reproductive load. Proc Natl Acad Sci USA 96:5083–5088

    Article  CAS  PubMed  Google Scholar 

  • Hosken DJ, Blanckenhorn WU (1999) Female multiple mating, inbreeding avoidance, and fitness: it is not only the magnitude of costs and benefits that counts. Behav Ecol 10:462–464

    Article  Google Scholar 

  • Hughes L, Siew-Woon Chang B, Wagner D, Pierce NE (2000) Effects of mating history on ejaculate size, fecundity, longevity, and copulation duration in the ant-tended lycaenid butterfly Jalmenus evagoras. Behav Ecol Sociobiol 47:119–128

    Article  Google Scholar 

  • Imhof M, Harr B, Brem G, Schlotterer C (1998) Multiple mating in wild Drosophila melanogaster revisited by microsatellite analysis. Mol Ecol 7:915–917

    Article  CAS  PubMed  Google Scholar 

  • Jacob S, Boivin G (2004) Insemination potential of male Trichogramma evanescens. Entomol Exp Appl 113:181–186

    Article  Google Scholar 

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev Camb Philos Soc 75:21–64

    Google Scholar 

  • Jiao X, Xuan W, Sheng C (2006) Effects of delayed mating and male mating history on longevity and reproductive performance of the rice stem borer Chilo suppressalis. J Appl Entomol 130:108–112

    Article  Google Scholar 

  • Jiménez-Pérez A, Wang Q (2004) Male remating behavior and its effect on female reproductive fitness in Cnephasia jactatana. J Insect Behav 17:685–694

    Article  Google Scholar 

  • Johnstone RA, Keller L (2000) How males can gain by harming their mates: sexual conflict, seminal toxins and the cost of mating. Am Nat 156:368–377

    Article  Google Scholar 

  • Jones TM (2001) A potential cost of monandry in the lekking sandfly Lutzomyia longipalpis. J Insect Behav 14:385–397

    Article  Google Scholar 

  • Jones TM, McNamara KB, Colvin P, Featherston R, Elgar MA (2006) Mating frequency, fecundity and fertilization success in the hide beetle, Dermestes maculatus. J Insect Behav 19:357–371

    Article  Google Scholar 

  • Karlsson B (1998) Nuptial gifts, resource budgets, and reproductive output in a polyandrous butterfly. Ecology 79:2931–2940

    Article  Google Scholar 

  • LaMunyon CW (1997) Increased fecundity, as a function of multiple mating, in an arctiid moth Uthetheisa ornatrix. Ecol Entomol 22:69–73

    Article  Google Scholar 

  • Lauwers K, Van Dyck H (2006) The cost of mating with a non-virgin male in a monandrous butterfly: experimental evidence from the speckled wood Pararge aegeria. Behav Ecol Sociobiol 60:69–76

    Article  Google Scholar 

  • Lemaître J-F, Rigaud T, Cornet S, Bollache L (2009) Sperm depletion, male mating behaviour and reproductive ‘time-out’ in Gammarus pulex (Crustacea, Amphipoda). Anim Behav 77:49–54

    Article  Google Scholar 

  • Mair J, Blackwell A (1998) Effect of age and multiple mating on the mating behavior of Culicoides nubeculosus. J Med Entomol 35:996–1001

    CAS  PubMed  Google Scholar 

  • Marcotte M, Delisle J, McNeil JN (2005) Impact of male mating history on the temporal sperm dynamics of Choristoneura rosaceana and C. fumiferana females. J Insect Physiol 51:537–544

    Article  CAS  PubMed  Google Scholar 

  • Marcotte M, Delisle J, McNeil JN (2006) Impact of male mating history on the postmating resumption of sexual receptivity and lifetime reproductive success in Choristoneura rosaceana females. Physiol Entomol 31:227–233

    Article  Google Scholar 

  • McNamara KB, Jones TM, Elgar MA (2007) No cost of male mating experience on female reproductive success in the almond moth Cadra cautella. Behav Ecol Sociobiol 61:1177–1184

    Article  Google Scholar 

  • McNamara KB, Elgar MA, Jones TM (2008) Seminal compounds, female receptivity and fitness in the almond moth Cadra cautella. Anim Behav 76:771–777

    Article  Google Scholar 

  • Michalik P, Uhl G (2005) The male genital system of the cellar spider. Pholcus phalangioides: development of spermatozoa and seminal secretion. Front Zool 2:12

    Article  PubMed  Google Scholar 

  • Michereff MFF, Vilela EF, Filho MM, Nery DMS, Thièbaut JT (2004) Effects of delayed mating and male mating history on the reproductive potential of Leucoptera coffeella (Lepidoptera: Lyonetiidae). Agric For Entomol 6:241–247

    Article  Google Scholar 

  • Montrose VT, Harris WE, Moore PJ (2004) Sexual conflict and cooperation under naturally occurring male enforced monogamy. J Evol Biol 17:443–452

    Article  CAS  PubMed  Google Scholar 

  • Norton S, Uetz GW (2005) Mating frequency in Schizocosa ocreata wolf spiders: evidence for a mating system with female monandry and male polygyny. J Archnol 33:16–24

    Article  Google Scholar 

  • Partrdge L, Harvey PH (1985) Costs of reproduction. Nature 316:20

    Article  Google Scholar 

  • Pérez-Staples D, Aluja M (2004) Anastrepha striata (Diptera: Tephritidae) females mated to virgin males live longer. Ann Entomol Soc Am 97:1336–1341

    Article  Google Scholar 

  • Pérez-Staples D, Aluja M (2006) Sperm allocation and cost of mating in a tropical tephritid fruit fly. J Insect Physiol 52:839–845

    Article  PubMed  Google Scholar 

  • Pérez-Staples D, Aluja M, Macías-Ordóñez R, Sivinski J (2008) Reproductive trade-offs from mating with a successful male: the case of the tephritid fly Anastrepha obliqua. Behav Ecol Sociobiol 62:1333–1340

    Article  Google Scholar 

  • Platnick NI (2008) The world spider catalog, version 8.5, American Museum of Natural History. Available from: http://research.amnh.org/entomology/spiders/catalog/index.html

  • Preston BT, Stevenson IR, Pemberton JM, Wilson K (2001) Dominant rams lose out by sperm depletion. Nature 409:681–682

    Article  CAS  PubMed  Google Scholar 

  • Ridley M (1988) Mating frequency and fecundity in insects. Biol Rev Camb Philos Soc 63:509–549

    Article  Google Scholar 

  • Robinson MH (1982) Courtship and mating behavior in spiders. Annu Rev Entomol 27:1–20

    Article  Google Scholar 

  • Rogers CE, Marti OG Jr (1997) Once-mated beet armyworm: effects of age at mating on fecundity, fertility and longevity. Environ Entomol 26:585–590

    Google Scholar 

  • Rogers DW, Chapman T, Fowler K, Poniankowski A (2005) Mating-induced reduction in accessory reproductive organ size in the stalk-eyed fly Cyrtodiopsis dalmanni. BMC Evol Biol 5:37

    Article  PubMed  Google Scholar 

  • Royer L, McNeill JN (1993) Male investment in the European corn borer Ostrinia nubilalis (Lepidoptera: Pyralidae): impact on female longevity and reproductive performance. Funct Ecol 7:209–215

    Article  Google Scholar 

  • Ruther J, Matschke M, Garbe L, Steiner S (2009) Quantity matters: male sex pheromone signals mate quality in the parasitic wasp Nasonia vitripennis. Proc Roy Soc Lond B Biol 276:3303–3310

    Article  Google Scholar 

  • Rutowski RL, Gilchrist GW, Terkanian B (1987) Female butterflies mated with recently mated males show reduced reproductive output. Behav Ecol Sociobiol 20:319–322

    Article  Google Scholar 

  • Sakurai T (1996) Multiple mating and its effect on female reproductive output in the bean bug Reptortus clavatus. Ann Entomol Soc Am 89:481–485

    Google Scholar 

  • Sato T, Goshima S (2006) Impact of male-only fishing and sperm limitation in manipulated populations of an unfished crab Hapalogaster dentata. Mar Ecol Prog Ser 313:193–204

    Article  Google Scholar 

  • Sato T, Goshima S (2007) Female choice in response to risk of sperm limitation by the stone crab Hapalogaster dentata. Anim Behav 73:331–338

    Article  Google Scholar 

  • Savalli UM, Fox CW (1999) The effects of male mating history on paternal investment, fecundity and female remating in the seed beetle Callosobruchus maculatus. Funct Ecol 13:169–177

    Article  Google Scholar 

  • Smith PH, Gillott C, Browne LB, Van Gerwen ACM (1990) The mating-induced refractoriness of Lucilia curpina females: manipulating the male contribution. Physiol Entomol 15:469–481

    Article  Google Scholar 

  • Snook R (2001) Sexual selection: conflict, kindness and chicancry. Curr Biol 11:337–341

    Article  Google Scholar 

  • Steele RH (1984) An investigation of male mating success in Drosophila subobscura. Ph.D. thesis, University of Edinburgh, Edinburgh

  • Steiner S, Henrich N, Ruther J (2007) Mating with sperm-depleted males does not increase female mating frequency in the parasitoid Lariophagus distinguendus. Entomol Exp Appl 126:131–137

    Article  Google Scholar 

  • Svärd L, Wiklund C (1986) Mass and production rate of ejaculates in relation to monandry/polyandry in butterflies. Behav Ecol Sociobiol 24:395–402

    Article  Google Scholar 

  • Svensson MGE, Marling E, Löfqvist J (1998) Mating behavior and reproductive potential in the turnip moth Agrotis segetum (Lepidoptera: Noctuidae). J Insect Behav 11:343–359

    Article  Google Scholar 

  • Szirányi A, Kiss B, Samu F, Harand W (2005) The function of long copulation in the wolf spider, Pardosa agrestis investigated in a controlled copulation duration experiment. J Archnol 33:408–414

    Article  Google Scholar 

  • Takakura K (1999) Active female courtship behavior and male nutritional contribution to female fecundity in Bruchidius dorsalis. Res Pop Ecol 41:269–273

    Article  Google Scholar 

  • Tamhankar AJ (1995) Host influence on mating behavior and spermatophore reception correlated with reproductive output and longevity of female Earias insulana. J Insect Behav 8:499–511

    Article  Google Scholar 

  • Thornhill R, Alcock J (1983) Sexual selection theory. Harvard University Press, Cambridge

    Google Scholar 

  • Torres-Vila LM, Jennions MD (2005) Male mating history and female fecundity in the Lepidoptera: do male virgins make better partners? Behav Ecol Sociobiol 57:318–326

    Article  Google Scholar 

  • Trivers RL (1972) Paternal investment and sexual selection. In: Campbell BG (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179

    Google Scholar 

  • Wagner WE, Kelley RJ, Tucker KR, Harper CJ (2001) Females receive a life-span benefit from male ejaculates in a field cricket. Evolution 55:994–1001

    Article  PubMed  Google Scholar 

  • Watanabe M, Wiklund C, Bon'no M (1998) The effect of repeated matings on sperm numbers in successive ejaculates of the cabbage white butterfly Pieris rapae. J Insect Behav 11:559–570

    Article  Google Scholar 

  • Wedell N (1996) Mate quality affects reproductive effort in a paternally investing species. Am Nat 148:1075–1088

    Article  Google Scholar 

  • Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320

    Article  Google Scholar 

  • Wiklund C, Kaitala A, Wedell N (1998) Decoupling of reproductive rates and parental expenditure in a polyandrous butterfly. Behav Ecol 9:20–25

    Article  Google Scholar 

  • Wilson N, Tufton TJ, Eady PE (1999) The effects of single, double, and triple matings on the lifetime fecundity of Callosobruchus analis and Callosobruchus maculates. J Insect Behav 12:295–306

    Article  Google Scholar 

  • Wu J, Jiao XG, Chen J, Peng Y, Liu FX (2008) Courtship and mating in the wolf spider Pardosa astrigera. Chin J Zool 43:9–12

    Google Scholar 

Download references

Acknowledgements

We thank Paula Stockley, Mark Elgar, and two anonymous reviewers for their helpful comments and suggestions on this manuscript. This work was supported by the National Natural Science Foundation of China (30800121).

Ethical standards

The experiments reported in this study comply with current China law.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaoguo Jiao.

Additional information

Communicated by M. Elgar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiao, X., Chen, Z., Wu, J. et al. Male remating and female fitness in the wolf spider Pardosa astrigera: the role of male mating history. Behav Ecol Sociobiol 65, 325–332 (2011). https://doi.org/10.1007/s00265-010-1049-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-010-1049-2

Keywords

Navigation