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.
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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
Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164
Bateman PW (1998) Mate preference for novel partners in the cricket, Gryllus bimaculatus. Ecol Entomol 23:473–475
Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic, London
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
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
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
Civetta A, Clark AG (2000) Correlated effects of sperm competition and postmating female mortality. Proc Natl Acad Sci USA 97:13162–13165
Cook PA (1999) Sperm numbers and female fertility in the moth Plodia interpunctella. J Insect Behav 12:767–779
Cordero C (1995) Ejaculate substances that affect female insect reproductive physiology and behavior: honest or arbitrary traits? J Theor Biol 174:453–461
Damiens D, Boivin G (2006) Why do sperm-depleted parasitoid males continue to mate? Behav Ecol 17:138–143
Gillot C (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu Rev Entomol 48:163–184
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
Hayashi F (1998) Multiple mating and lifetime reproductive output in female dobsonflies that receive nuptial gifts. Ecol Res 13:283–289
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
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
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
Imhof M, Harr B, Brem G, Schlotterer C (1998) Multiple mating in wild Drosophila melanogaster revisited by microsatellite analysis. Mol Ecol 7:915–917
Jacob S, Boivin G (2004) Insemination potential of male Trichogramma evanescens. Entomol Exp Appl 113:181–186
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev Camb Philos Soc 75:21–64
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
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
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
Jones TM (2001) A potential cost of monandry in the lekking sandfly Lutzomyia longipalpis. J Insect Behav 14:385–397
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
Karlsson B (1998) Nuptial gifts, resource budgets, and reproductive output in a polyandrous butterfly. Ecology 79:2931–2940
LaMunyon CW (1997) Increased fecundity, as a function of multiple mating, in an arctiid moth Uthetheisa ornatrix. Ecol Entomol 22:69–73
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
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
Mair J, Blackwell A (1998) Effect of age and multiple mating on the mating behavior of Culicoides nubeculosus. J Med Entomol 35:996–1001
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
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
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
McNamara KB, Elgar MA, Jones TM (2008) Seminal compounds, female receptivity and fitness in the almond moth Cadra cautella. Anim Behav 76:771–777
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
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
Montrose VT, Harris WE, Moore PJ (2004) Sexual conflict and cooperation under naturally occurring male enforced monogamy. J Evol Biol 17:443–452
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
Partrdge L, Harvey PH (1985) Costs of reproduction. Nature 316:20
Pérez-Staples D, Aluja M (2004) Anastrepha striata (Diptera: Tephritidae) females mated to virgin males live longer. Ann Entomol Soc Am 97:1336–1341
Pérez-Staples D, Aluja M (2006) Sperm allocation and cost of mating in a tropical tephritid fruit fly. J Insect Physiol 52:839–845
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
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
Ridley M (1988) Mating frequency and fecundity in insects. Biol Rev Camb Philos Soc 63:509–549
Robinson MH (1982) Courtship and mating behavior in spiders. Annu Rev Entomol 27:1–20
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
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
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
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
Rutowski RL, Gilchrist GW, Terkanian B (1987) Female butterflies mated with recently mated males show reduced reproductive output. Behav Ecol Sociobiol 20:319–322
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
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
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
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
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
Snook R (2001) Sexual selection: conflict, kindness and chicancry. Curr Biol 11:337–341
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
Svärd L, Wiklund C (1986) Mass and production rate of ejaculates in relation to monandry/polyandry in butterflies. Behav Ecol Sociobiol 24:395–402
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
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
Takakura K (1999) Active female courtship behavior and male nutritional contribution to female fecundity in Bruchidius dorsalis. Res Pop Ecol 41:269–273
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
Thornhill R, Alcock J (1983) Sexual selection theory. Harvard University Press, Cambridge
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
Trivers RL (1972) Paternal investment and sexual selection. In: Campbell BG (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179
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
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
Wedell N (1996) Mate quality affects reproductive effort in a paternally investing species. Am Nat 148:1075–1088
Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320
Wiklund C, Kaitala A, Wedell N (1998) Decoupling of reproductive rates and parental expenditure in a polyandrous butterfly. Behav Ecol 9:20–25
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
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
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).
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The experiments reported in this study comply with current China law.
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The authors declare that they have no conflict of interest.
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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
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DOI: https://doi.org/10.1007/s00265-010-1049-2