Abstract
Females of many species mate multiply, yet some taxon females mate with only one male, also known as monandry. Although the underlying mechanism behind female monandry is poorly understood relative to female polyandry, there are two contrasting hypotheses, male control and female control, for the maintenance of monandry. Since females generally benefit from multiple mating for material and/or genetic benefits, cases of monandry may reflect male manipulation on female remating at the expense of female fitness (male control). Alternatively, monandry may be favored by females, if females maximize their fitness by mating once (female control). Here, we tested two hypotheses by manipulating the number of mating (repeated mating and polyandry) on female fitness in a largely monandrous wolf spider, Pardosa astrigera. We allowed females to be inseminated once, twice with the same males (repeated mating) or with two males (polyandry) and determined female fitness consequences. The number of female mating, regardless of a single mating, repeated mating, or polyandry, had no significant effects on female fecundity, fertility, and survival and size of their spiderlings. However, the fitness cost of female multiple mating may to some extent be underestimated under laboratory conditions. In addition, female survival was adversely affected by induced multiple mating. Therefore, our results suggest that monandry of the wolf spider (P. astrigera) may be under the control of females, rather than under the control of males.
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References
Andersson M (1994) Sexual selection. Princeton University Press, Princeton
Arnqvist G (1989) Multiple mating in a water strider: mutual benefits or intersexual conflict. Anim Behav 38:749–756
Arnqvist G, Andrés JA (2006) The effects of experimentally induced polyandry on female reproduction in a monandrous mating system. Ethology 112:748–756
Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164
Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton
Baer B, Morgan ED, Schmid-Hempel P (2001) A nonspecific fatty acid within the bumblebee mating plug prevents females from remating. Proc Natl Acad Sci USA 98:3926–3928
Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368
Chapman T, Liddle LF, Kalb JM, Wolfner M, Partridge L (1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:211–217
Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:42–47
Cook PA (1999) Sperm numbers and female fertility in the moth Plodia interpunctella. J Insect Behav 12:767–779
Daly M (1978) The cost of mating. Am Nat 112:771–774
DiBattista JD, Feldheim KA, Gruber SH, Hendry AP (2008) Are indirect genetic benefits associated with polyandry? Testing predictions in a natural population of lemon sharks. Mol Ecol 17:783–795
Drnevich JM, Papke RS, Rauser CL, Rutowski RL (2001) Material benefits from multiple mating in female mealworm beetles. J Insect Behav 14:215–230
Engqvist L (2006) Female benefits from mating with different males in the scorpionfly Panorpa cognata. Behav Ecol 17:435–440
Fedorka KM, Mousseau TA (2002) Material and genetic benefits of female multiple mating and polyandry. Anim Behav 64:361–367
Fox CW, Rauter CM (2003) Bet-hedging and the evolution of multiple mating. Evol Ecol Res 5:273–286
Gillot C (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu Rev Entomol 48:163–184
Holland B, Rice WR (1999) Experimental removal of sexual selection reverses intersexual antagonistic coevolution 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
Hosken DJ, Stockley P, Tregenza T, Wedell N (2009) Monogamy and the battle of the sexes. Annu Rev Entomol 54:361–378
Ivy TM, Sakaluk SK (2005) Polyandry promotes enhanced offspring survival in decorated crickets. Evolution 59:152–159
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64
Jennions MD, Drayton JM, Brooks R, Hunt J (2007) Do female black field crickets Teleogryllus commodus benefit from polyandry? J Evol Biol 20:1469–1477
Jiao XG, Chen ZQ, Wu J, Du HY, Liu FX, Chen J, Li DQ (2011) Male remating and female fitness in the wolf spider Pardosa astrigera: the role of male mating history. Behav Ecol Sociobiol 65:325–332
Johnson SL, Brockmann HJ (2010) Costs of multiple mates: an experimental study in horseshoe crabs. Anim Behav 80:773–782
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 14:385–399
King BH, Bressac C (2010) No fitness consequences of experimentally induced polyandry in a monandrous wasp. Behaviour 147:85–102
Klowden MJ (1999) The check is in the male: male mosquitoes affect female physiology and behavior. J Am Mosquito Contr 15:213–220
Klowden MJ (2001) Sexual receptivity in Anopheles gambiae mosquitoes: absence of control by male accessory gland substances. J Insect Physiol 47:661–666
Kraus FB, Neumann P, Praagh J, Moritz RFA (2004) Sperm limitation and the evolution of extreme polyandry in honeybees (Apis mellifera L.). Behav Ecol Sociobiol 55:494–501
Mair J, Blackwell A (1998) Effect of age and multiple mating on the mating behavior of Culicoides nubeculosus. J Med Entomol 35:996–1001
Maklakov AA, Lubin Y (2004) Sexual conflict over mating in a spider: increased fecundity does not compensate for the costs of polyandry. Evolution 58:1135–1140
Maklakov AA, Lubin Y (2006) Indirect genetic benefits of polyandry in a spider with direct costs of mating. Behav Ecol Sociobiol 61:31–38
Maklakov AA, Bilde T, Lubin Y (2005) Sexual conflict in the wild: elevated mating rate reduces female lifetime reproductive success. Am Nat 165:S38–S45
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
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 rate in Schizocosa ocreata wolf spiders: evidence for a mating system with female monandry and male polygyny. J Arachnol 33:16–24
Ojanguren AF, Evans JP, Magurran AE (2005) Multiple mating influences offspring size in guppies. J Fish Biol 67:1184–1188
Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic, New York
Reinhardt K, Kohler G, Schumacher J (1999) Females of the grasshopper Chorthippus parallelus do not remate for fresh sperm. Proc Roy Soc Lond B Biol 266:2003–2009
Ridley M (1988) Mating rate and fecundity in insects. Biol Rev Camb Philos Soc 63:509–549
Riemann JG, Thorson BJ (1969) Effect of accessory material on oviposition and mating by female houseflies. Ann Entomol Soc Am 62:828–834
Riemann JG, Moen JM, Thorson BJ (1967) Female monogamy and its control in houseflies. J Insect Physiol 13:407–418
Ronkainen K, Kaitala A, Kivelä SM (2009) Polyandry, multiple mating, and female fitness in a water strider Aquarius paludum. Behav Ecol Sociobiol 64:657–664
Schneider JM, Lubin Y (1998) Intersexual conflict in spiders. Oikos 83:496–506
Simmons LW (2001) The evolution of polyandry: an examination of the genetic incompatibility and good-sperm hypotheses. J Evol Biol 14:585–594
Song SD, Drew RAI, Hughes JM (2007) Multiple paternity in a natural population of a wild tobacco fly, Bactocera cacuminata, assessed by microsatellite DNA markers. Mol Ecol 16:2353–2361
South A, Lewis SM (2011) The influence of male ejaculate quantity on female fitness: a meta-analysis. Biol Rev 86:299–309
Sprenger D, Anthes N, Michiels NK (2008a) Multiple mating affects offspring size in the opisthobranch Chelidonura sandrana. Mar Biol 153:891–897
Sprenger D, Faber J, Michiels NK, Anthes N (2008b) Natural female mating rate maximizes hatching size in a marine invertebrate. J Anim Ecol 77:696–701
Steiner S, Henrich N, Ruther J (2008) Mating with sperm-depleted males does not increase female mating frequency in the parasitoid Lariophagus distinguendus. Entomol Exp Appl 126:131–137
Szirányi A, Kiss B, Samu F, Harand W (2005) The function of long copulation in the wolf spider Pardosa agrestis (Araneae, Lycosidae) investigated in a controlled copulation. J Arachnol 33:408–414
Thornhill R, Alcock J (1983) The evolution of insect mating systems. Harvard University Press, Cambridge
Tregenza T, Wedell N (1998) Benefits of multiple mates in the crickets Gryllus bimaculatus. Evolution 52:1726–1730
Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71–73
Uhl G, Schmitt S, Schäfer MA (2005) Fitness benefits of multiple mating versus female mate choice in the cellar spider (Pholcus phalangioides). Behav Ecol Sociobiol 59:69–76
Wang Q, Davis LK (2006) Females remate for sperm replenishment in a seed bug: evidence from offspring viability. J Insect Behav 19:337–346
Watson PJ (1998) Multi-male mating and female choice increase offspring growth in the spider Neriene litigiosa. Anim Behav 55:387–403
Wilder SM, Rypstra AL (2007) Male control of copulation duration in a wolf spider (Araneae, Lycosidae). Behaviour 144:471–484
Wu J, Jiao XG, Chen J, Peng Y, Liu FX (2008) Courtship and mating of the wolf spider Pardosa astrigera. Chin J Zool 43:9–12
Yasui Y (1997) A ‘good-sperm’ model can explain the evolution of costly multiple mating by females. Am Nat 149:573–584
Yasui Y (1998) The ‘genetic benefits’ of female multiple mating reconsidered. Trends Ecol Evol 13:246–250
Zeh JA, Zeh DW (2003) Toward a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109:929–950
Zhao JZ (1993) Spiders in the cotton fields in China. Wuhan Press, Wuhan
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The work was funded by the National Natural Science Foundation of China (30800121).
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Jiao, X., Guo, L., Chen, Z. et al. Experimental evidence for female-driven monandry in the wolf spider, Pardosa astrigera . Behav Ecol Sociobiol 65, 2117–2123 (2011). https://doi.org/10.1007/s00265-011-1220-4
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DOI: https://doi.org/10.1007/s00265-011-1220-4