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Effects of copulation temperature on female reproductive output and longevity in the wolf spider Pardosa astrigera (Araneae: Lycosidae)
ARTICLE IN PRESS Journal of Thermal Biology 35 (2010) 125–128
Contents lists available at ScienceDirect
Journal of Thermal Biology journal homepage: www.elsevier.com/locate/jtherbio
Effects of copulation temperature on female reproductive output and longevity in the wolf spider Pardosa astrigera (Araneae: Lycosidae) Zhanqi Chen, Xiaoguo Jiao n, Jun Wu, Jian Chen, Fengxiang Liu College of Life Sciences, Hubei University, Xueyuan Road 11, Wuchang, Wuhan 430062, Hubei, China
a r t i c l e in fo
abstract
Article history: Received 7 August 2009 Accepted 5 January 2010
The copulation duration of male wolf spider Pardosa astrigera, was significantly influenced by environmental temperature, as had been found in some insect species. Therefore, temperature during male courtship and copulation may influence the amount of sperm and seminal fluids transferred during copulation, which in turn could influence female fitness. In order to test this hypothesis, we subjected pairs of male and female P. astrigera to five temperature groups from 16 to 32 1C at an interval of 4 1C, and investigated whether and to what extent the various temperatures during male courtship and copulation influenced female reproductive output and female adult longevity under controlled laboratory conditions. With the increase of copulation temperature, females were more likely to lay egg sacs. The total egg sacs and lifetime fecundity of female were positively influenced by copulation temperature, whereas female lifetime spiderlings and adult longevity were independent of copulation temperature. & 2010 Elsevier Ltd. All rights reserved.
Keywords: Wolf spider Pardosa astrigera Copulation temperature Reproduction Longevity
1. Introduction Copulation duration plays important roles in male and female fitness (Edvardsson and Canal, 2006). Males may attempt to prolong the copulation duration for several fitness benefits, such as transferring amounts of sperm to fertilize fully female eggs (Schneider et al., 2000; Elgar et al., 2003). These include increasing sperm-associated seminal fluids that could decrease female sexual receptivity to subsequent suitors and stimulate oviposition (Bukowski and Christenson, 1997; Aisenberg et al., 2009), ensuring appropriate storage of the transferred sperm (Bukowski and Christenson, 1997) and/or preventing the female from remating with other males before oviposition (Edvardsson and Canal, 2006; Katsuki and Miyatake, 2009). Females may also benefit from controlling copulation duration if it helps to avoid harassment from other males (Andersson et al., 2000), to obtain more resources (Smedly and Eisner, 1996) or gain information about the quality of their mates (Eberhard, 1994). However, the prolonged copulation duration may incur costs to both sexes in terms of time, energy and higher risk exposure to predators and pathogens (Daly, 1978; Szira´nyi et al., 2005). Whatever its potential functions, there may exist a trade-off between the costs and benefits on the evolutionarily maintenance of the copulation duration within a species.
n
Corresponding author. Tel./fax: + 86 27 88661237. E-mail address: [email protected] (X. Jiao).
0306-4565/$ - see front matter & 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jtherbio.2010.01.002
Copulation duration of some insects and spiders is affected by a number of factors. To date, much attention has been paid to the biotic factors influencing copulation duration (e.g., species strains: Field et al., 1999; age: Field et al., 1999; Wilder and Rypstra, 2007; body size: Field et al., 1999; Schneider et al., 2000, 2005; Engqvist and Sauer, 2003; Wilder and Rypstra, 2007; body condition: Engqvist and Sauer, 2003; Wilder and Rypstra, 2007; mating status: Andre´s and Cordero Rivera, 2000; Bukowski et al., 2001; Danielson-Franc- ois and Bukowski, 2005; Schneider et al., 2005; Friberg, 2006; risk of sperm competition: Andre´s and Cordero Rivera, 2000; Schneider et al., 2000; Aisenberg et al., 2009; diet: Pe´rez-Staples and Aluja, 2004), whereas fewer studies have been focused on the abiotic factors, particularly the environmental temperature, a potential factor influencing copulation duration (but see Costa and Sotelo, 1984; Cook, 1994; Horton et al., 2002; Martin and Hosken, 2002; Jiao et al., 2009; Katsuki and Miyatake, 2009). Generally, copulation duration is negatively related to temperature in most invertebrates (Costa and Sotelo, 1984; Cook, 1994; Horton et al., 2002; Martin and Hosken, 2002; Jiao et al., 2009; Katsuki and Miyatake, 2009). With the increase of temperature, copulation duration decreases and the quantity of sperm and/or seminal fluids transferred decline (Katsuki and Miyatake, 2009). Considering the fact that temperature influences the rates of ectotherm physiological processes, it is unsurprising that the thermal environment may have a marked influence on spider growth (reviewed in Li and Jackson, 1996; Li, 1998), development (reviewed in Li and Jackson, 1996; Li, 2002), survival (reviewed in
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Li and Jackson, 1996; Li, 2002) and reproduction (reviewed in Li and Jackson, 1996) as well. Even though the effects of environmental temperature on female spider reproductive fitness, such as fecundity (reviewed in Li and Jackson, 1996) and fertility (reviewed in Li and Jackson, 1996; Hanna and Cobb, 2006) are well-documented, most studies are only carried out to determine the long-term temperature effect of the time window on reproductive performance from their sexual interaction to death (Demoraes and McMurtry, 1987; reviewed in Li and Jackson, 1996; Medeiros et al., 2003; Sa´nchez-Ramos et al., 2007). However, the potential effects of the temperature during male courtship and copulation on female reproductive output and female adult longevity remain largely unexplored. To understand such potential effects, there is a prerequisite for us to separate the effects of copulation temperature from the rearing temperature after female has been inseminated. The wolf spider P. astrigera is a wandering spider widely distributed in China. In most central provinces of China, there are two generations a year. P. astrigera overwinters as subadult in the soil or in the litter in natural habitats. Their reproductive peaks occur in early May (ca. 12 1C) of the overwintering generation and in early September (ca. 28 1C) of the next generation, respectively (Zhao, 1993). In a previous study, male P. astrigera copulation duration was negatively related to the copulation temperature (Jiao et al., 2009). The question arises whether male P. astrigera copulation duration is positively related to the quantity of sperm and/or seminal fluids transferred for such a relationship has been found in some insect species (Engqvist and Sauer, 2003; Bailey and Nuhardiyati, 2005). Female P. astrigera may receive fewer sperm and/or less seminal fluids from their mates under higher temperature (summer generation) relative to that under lower temperature (spring generation), which may decrease female reproductive fitness and longevity. In order to test this hypothesis, we aim to investigate whether and to what extent the various temperatures during male courtship and copulation influence female reproductive output and female adult longevity.
2. Materials and methods 2.1. Spiders We collected the overwintering P. astrigera subadults from cotton fields at Huazhong Agricultural University, Wuhan, Hubei Province, China, from November to December 2007. Spiders were kept visually isolated from each other in opaque Plexiglas enclosures (5.0 5.0 7.5 cm3, length width height) (SAIFU Inc., Ningbo, Zhejing, China) under laboratory conditions of 13:11 L:D photoperiod, 2470.5 1C and 50–70% RH. Each spider was fed with a combination of fruit flies, Drosophila melanogaster, and/or crickets, Acheta domesticus, every 3 days and had continual access to water by way of a soaked cotton wick inserted through a hole in the enclosure floor into a reservoir below. After their final molt, the spiders were weighted using an electronic analytical balance (to the nearest 0.1 mg, METTLER TOLEDO AB104-S, Switzerland) and used in experiments between 5 and 7 days postmolt. All test spiders were virgin and used not more than once.
2.2. Experimental design We began the experiment with virgin P. astrigera females and matched females for body mass in groups of five and randomly assigned each of them to one of the five temperatures: 16, 20, 24, 28 and 32 1C.
The mating experiment was carried out in a clear cylindrical glass container (10.5 12.0 cm2, diameter height) (SAIFU Inc., Ningbo, Zhejing, China). White filter paper covered the bottom of the container to provide a substrate suitable for spider locomotion. In each run, the experimental spiders were first held separately in the rearing enclosures at their prescribed temperature in the environmental chamber for 1 h prior to pairing. One randomly selected female and a male were introduced simultaneously into the glass container, and the courtship and copulation were observed constantly until a mating occurred or up to 30 min. We paired male and female and observed their mating until up to 20 females being successfully inseminated in each temperature group. Between experimental runs, the arenas were swabbed with alcohol, allowed to dry and the filter paper was replaced. After successful mating, the inseminated females in the glass container were kept out of the environmental chamber, and maintained under laboratory conditions of 13:11 L:D photoperiod, 2470.5 1C and 50 70% RH. Female reproductive behavior was monitored daily until their death. Egg laying and spiderling hatching were inspected and counted. After hatching of the young, empty egg sacs were collected from the bottom of the enclosures and the number of un-hatched eggs was counted. Female lifetime egg sacs (the total number of egg sacs female produced throughout her lifetime), female lifetime fecundity (total eggs female laid throughout her lifetime), female lifetime spiderlings (total eggs hatched throughout female lifetime) and female adult longevity (days from their final molt to death) were calculated and recorded, respectively. 2.3. Statistical analysis Data sets were analysed by ANOVA if they initially met the assumptions of normal distribution (Kolmogorov–Smirnov test) and equal variance (Levene test), or met after being square root transformed. Female lifetime fecundity and spiderlings were compared among various temperature groups using the ANCOVA procedure with copulation temperature as fixed factor and female body mass as a covariate as the latter strongly influences female lifetime fecundity and spiderlings. When there were significant differences among various copulation temperatures, comparisons for significant effects between copulation temperatures were performed using LSD post hoc tests. Because the number of egg sacs were not normally distributed even after being square root transformed, Kruskal–Wallis H test was used. Once the difference of Kruskal–Wallis H test was significant, Mann–Whitney U test at Bonferroni corrected P value was subsequently applied. All results are reported as mean7SE. Statistical analyses were performed with SPSS 13.0 (SPSS Inc., Chicago, IL, USA).
3. Results With the increase of copulation temperature, females were more likely to produce egg sacs (Pearson Chi-Square test: w2 =17.344, df= 4, P =0.002). Mated females that failed to lay egg sac throughout their lifetime were excluded from subsequent reproductive output analysis. The total number of egg sacs female produced throughout their lifetime differed significantly among various copulation temperatures (Kruskal–Wallis H test: H=30.066, Po0.0001). Multiple comparisons revealed that the number of egg sacs under higher copulation temperature (i.e., 28 and 32 1C) were significantly higher than those under lower copulation temperature (16 and 20 1C) (Fig. 1). Lifetime fecundity of female P. astrigera was positively influenced by female body mass (ANCOVA, F1.75 = 4.768, P=0.032) and by copulation temperature (F4.75 =3.038, P=0.022
ARTICLE IN PRESS Z. Chen et al. / Journal of Thermal Biology 35 (2010) 125–128
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Fig. 1. Effects of copulation temperature on the production of egg sacs of Pardosa astrigera. Bars with the same letter are not significantly different. The number within the column indicating sample sizes. Error bars represent standard errors about the mean.
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Fecundity
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Temperature ( °C) Fig. 2. Effects of copulation temperature on lifetime fecundity of Pardosa astrigera. Bars with the same letter are not significantly different. The number within the column indicating sample sizes. Error bars represent standard errors about the mean.
Fig. 2). Female lifetime fecundity under the copulation temperatures of 16 and 20 1C was significantly lower relative to those under the higher copulation temperatures of 24, 28 and 32 1C. There were no significant differences in female lifetime fecundity across other copulation temperature. Although total spiderlings females produced throughout their lifetime were also positively influenced by female body mass (ANCOVA, F1.75 =4.897, P= 0.030), they were independent of copulation temperature (16 1C: 48.2 79.0; 20 1C: 49.577.2; 24 1C: 66.6 77.4; 28 1C: 66.1 77.6; 32 1C: 65.2 77.7; F4.75 = 1.590, P= 0.186). ANCOVA revealed that P. astrigera female adult longevity was neither significantly influenced by female body mass (ANCOVA, F1.93 =0.236, P=0.628), nor by copulation temperature (16 1C: 79.1 710.9; 20 1C: 82.879.4; 24 1C: 97.2 710.4; 28 1C: 102.2711.5; 32 1C: 98.4711.8; ANCOVA, F4.93 = 0.838, P= 0.504).
4. Discussion Our results demonstrate that the temperature during male courtship and copulation has unexpectedly positive effects on the production of egg sacs and lifetime fecundity in the wolf spider P. astrigera. However, copulation temperature has little effect on female lifetime spiderlings and female adult longevity. In the present study, contrary to our expectation, the number of egg sacs and lifetime fecundity of female were significantly higher under higher copulation temperature relative to those under lower copulation temperature. There are several possible explanations for such unexpected results. One possibility is that a
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correlation may exist between the rate of sperm transfer and copulation temperature. Although male P. astrigera copulation duration is negatively related to copulation temperature (Jiao et al., 2009), male may transfer sperm more efficiently under higher temperature relative to that under lower temperature. Such a temperature-dependent sperm transferring pattern is also found in three species of predatory bugs (Horton et al., 2002). Alternatively, the volume of seminal fluids male P. astrigera transferred under higher temperature is significantly larger, thus the females inseminated under higher temperature may receive more ovulation promoters derived from the ejaculate, such as hormones and/or neurotransmitters. And these stimuli may result in the marked increase of egg sacs and lifetime fecundity. Similar results are found in some insects (Horton et al., 2002; reviewed in Gillott, 2003). It should be acknowledged that the above two explanations are not mutually exclusive. Ultimately, we could not rule out the possibility that physical difficulty may occur when males transfer sperm and/or seminal fluids under lower temperature. Similar studies have been found in several insect species (Horton et al., 2002; Katsuki and Miyatake, 2009). Although a positive relationship between sperm transfer and copulation duration has been found in several spider species (Schneider et al., 2000, 2006; Schneider and Elgar, 2001). The pattern of duration-dependent sperm transfer is far from a general rule. A growing handful of studies have revealed a nonlinear relationship between the sperm transferred and copulation duration (Suter and Parkhill, 1990; Bukowski and Christenson, 1997; Bukowski et al., 2001; Snow and Andrade, 2004; Schneider and Fromhage, 2005; Szira´nyi et al., 2005). Therefore, the pattern of sperm transfer is apparently speciesspecific, and copulation duration may be not a reliable predictor for the quantity of the sperm transferred during copulation. Although the dynamics of sperm transfer of the male wolf spider P. astrigera is not well known, it has been indirectly evaluated in the closely related wolf spider Pardosa agrestis by interrupting copulation (Szira´nyi et al., 2005). This study showed that only 10 min of copulation was sufficient for male to fertilize all the eggs of female P. agrestis (Szira´nyi et al., 2005). Thus, we assume that the dynamics of sperm transfer of male P. astrigera is not duration-dependent and sperm transfer occurs relatively early. Such a pattern has been found in previous works (Suter and Parkhill, 1990; Bukowski and Christenson, 1997; Snow and Andrade, 2004; Schneider and Fromhage, 2005; Szira´nyi et al., 2005). Considering the lifetime spiderlings of female P. astrigera is independent of copulation temperature, the variation of female lifetime fecundity under various copulation temperature is presumably due to the variation of seminal fluids, rather than the quantity of sperm. The tentative conclusion is further supported by the fact that females are more likely to produce egg sacs with the increase of copulation temperature (Fig. 1). In the present study, despite female lifetime fecundity is significantly higher under higher copulation temperature relative to that under lower copulation temperature, female lifetime spiderlings remain constant. A similar temperature-dependent eggproducing pattern, with female producing higher numbers of eggs under higher temperature relative to that under lower temperature, is found in the tropical butterfly, Bicyclus anynana (Geister et al., 2008). Although female P. astrigera produces more eggs under higher copulation temperature, female lifetime spiderlings may to some extent be balanced by the detrimental influence of higher copulation temperature on sperm damage. Like the spider Stegodyphus lineatus (Maklakov and Lubin, 2006), wolf spider P. astrigera males, neither present their mates with nuptial gifts, nor do they deposit sperm in spermatophores. It is unlikely that female P. astrigera could receive direct material (nutrients) from males beyond sperm during copulation, which could at least in
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part account for the fact that female adult longevity is independent of copulation temperature. During copulation, male may transfer sperm and/or associated seminal fluids which affect female remating propensity and the rate of offspring production (reviewed in Gillott, 2003; Aisenberg and Costa, 2005; Edvardsson and Canal, 2006; Aisenberg et al., 2009). Generally, the depletion of sperm and/or seminal fluids transferred during copulation shortens female remating delay and decreases the rate of offspring production (reviewed in Gillott, 2003). The variation of the quantity of sperm and/or seminal fluids transferred during copulation due to copulation temperature may in turn affect female remating propensity (Cook, 1994; Katsuki and Miyatake, 2009). In the present study, given the substantial reduction in female reproductive output under lower copulation temperature, female may adopt adaptive behavior, such as remating to offset the reproductive cost. Whether female P. astrigera remains sexually receptive or not after she has been inseminated under lower copulation temperature deserves further determination. To our knowledge, this is the first study suggesting that the temperature during male courtship and copulation influences female lifetime fecundity. Considering the limited duration of the temperature during male courtship and copulation, the variation of female lifetime fecundity may not be directly related to temperature per se, but to the variation of copulation duration derived from copulation temperature. In order to account for the underlying mechanism by which the effects of copulation temperature on reproductive consequences in the wolf spider P. astrigera, the relationship between copulation duration and the amount of sperm and/or seminal fluids transferred under various temperatures demands further investigation.
Acknowledgements We thank two anonymous referees for their helpful comments and suggestions on the manuscript. Financial assistance was provided by the National Natural Science Foundation of China (30800121). References Aisenberg, A., Costa, F.G., 2005. Females mated without sperm transfer maintain high sexual receptivity in the wolf spider Schizocosa malitiosa. Ethology 111, 545–558. Aisenberg, A., Estramil, N., Toscano-Gadea, C., Gonza´lez, M., 2009. Timing of female sexual unreceptivity and male adjustment of copulatory behaviour under competition risk in the wolf spider Schizocosa malitiosa. J. Ethol. 27, 43–50. Andersson, J., Borg-Karlson, A., Wiklund, C., 2000. Sexual cooperation and conflict in butterflies: a male-transferred anti-aphrodisiac reduces harassment of recently mated females. Proc. R. Soc. London Ser. B 267, 1271–1275. Andre´s, J., Cordero Rivera, A., 2000. Copulation duration and fertilization success in a damselfly: an example of cryptic female choice? Anim. Behav. 59, 695–703. Bailey, W.J., Nuhardiyati, M., 2005. Copulation, the dynamics of sperm transfer and female refractoriness in the leafhopper Balclutha incisa. Physiol. Entomol. 30, 343–352. Bukowski, T.C., Christenson, T.E., 1997. Determinants of sperm release and storage in a spiny orbweaving spider. Anim. Behav. 53, 381–395. Bukowski, T.C., Linn, C.D., Christenson, T.E., 2001. Copulation and sperm in Gasteracantha cancriformis: differential male behavior based on female mating history. Anim. Behav. 62, 887–895. Cook, D.F., 1994. Influence of temperature on copula duration and mating propensity in Lucilia cuprina (Diptera: Calliphoridae). J. Aust. Entomol. 33, 5–8. Costa, F.G., Sotelo Jr, J.R., 1984. Influence of temperature on the copulation duration of Schizocosa malitiosa. J. Arachnol. 12, 273–277. Daly, M., 1978. The cost of mating. Am. Nat. 112, 771–774. Danielson-Franc-ois, A.M., Bukowski, T.C., 2005. Female mating history influences copulation behavior but not sperm release in the orb-weaving spider Tetragnatha versicolor. J. Insect Behav. 18, 131–148.
Demoraes, G.J., McMurtry, J.A., 1987. Effect of temperature and sperm supply on the reproductive potential of Tetranychus evansi (Acari: Tetranychidae). Exp. Appl. Acarol. 3, 95–107. Eberhard, W.G., 1994. Evidence for widespread courtship during copulation in 131 species of insects and spiders, and implications for cryptic female choice. Evolution 48, 711–733. Edvardsson, M., Canal, D., 2006. The effects of copulation duration in the bruchid beetle Callosobruchus maculates. Behav. Ecol. 17, 430–434. Elgar, M.A., Champion de Crespigny, F.E., Ramamurthy, S., 2003. Male copulation behaviour and the risk of sperm competition. Anim. Behav. 66, 211–216. Engqvist, L., Sauer, K.P., 2003. Determinants of sperm transfer in the scorpionfly Panorpa cognata: male variation, female condition and copulation duration. J. Evol. Biol. 16, 1196–1204. Field, S.A., Taylor, P.W., Yuval, B., 1999. Sources of variability in copula duration of Mediterranean fruit flies. Entomol. Exp. Appl. 92, 271–276. Friberg, U., 2006. Male perception of female mating status: its effects on copulation duration, sperm defence and female fitness. Anim. Behav. 72, 1259–1268. Geister, T.L., Lorenz, M.W., Meyering-Vos, M., Hoffmann, K.H., Fischer, K., 2008. Effects of temperature on reproductive output, egg provisioning, juvenile hormone and vitellogenin titres in the butterfly Bicyclus anynana. J. Insect Physiol. 54, 1253–1260. Gillott, C., 2003. Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu. Rev. Entomol. 48, 163–184. Hanna, C.J., Cobb, V.A., 2006. Effect of temperature on hatching and nest site selection in the Green lynx spider, Peucetia viridans. J. Therm. Biol. 31, 262–267. Horton, D.R., Lewis, T.M., Hinojosa, T., 2002. Copulation duration in three species of anthocoris at different temperatures and effects on insemination and ovarian development. Pan-Pac. Entomol. 78, 43–55. Jiao, X.G., Wu, J., Chen, Z.Q., Chen, J., Liu, F.X., 2009. Effects of temperature on courtship and copulatory behaviours of a wolf spider Pardosa astrigera (Araneae: Lycosidae). J. Therm. Biol. 34, 348–352. Katsuki, M., Miyatake, T., 2009. Effects of temperature on mating duration, sperm transfer and remating frequency in Callosobruchus chinensis. J. Insect Physiol. 55, 113–116. Li, D., 1998. A linear model for description of the relationship between the lower threshold temperature and thermal constant in spiders. J. Therm. Biol. 23, 23–30. Li, D., 2002. The combined effects of temperature and diet on development and survival of a crab spider, Misumenops tricuspidatus. J. Therm. Biol. 27, 83–93. Li, D., Jackson, R.R., 1996. How temperature affects development and reproduction in spiders: a review. J. Therm. Biol. 21, 245–274. Martin, O.Y., Hosken, D.J., 2002. Strategic ejaculation in the common dung fly Sepsis cynipsea. Anim. Behav. 63, 541–546. Maklakov, A.A., Lubin, Y., 2006. Indirect genetic benefits of polyandry in a spider with direct costs of mating. Behav. Ecol. Sociobiol. 61, 31–38. Medeiros, R.S., Ramalho, F.S., Serra~ o, J.E., Zanuncio, J.C., 2003. Temperature influence on the reproduction of Podisus nigrispinus, a predator of the noctuid larva Alabama argillacea. BioControl 48, 695–704. Pe´rez-Staples, D., Aluja, M., 2004. Anastrepha striata females that mate with virgin males live longer. Ann. Entomol. Soc. Am. 97, 1336–1341. ˜ era, P., 2007. Reproduction, longSa´nchez-Ramos, I., A´lvarez-Alfageme, F., Castan evity and life table parameters of Tyrophagus neiswanderi (Acari: Acaridae) at constant temperatures. Exp. Appl. Acarol. 43, 213–226. Schneider, J.M., Elgar, M.A., 2001. Sexual cannibalism and sperm competition in the golden orb-web spider Nephila plumipes: female and male perspectives. Behav. Ecol. 12, 547–552. Schneider, J.M., Fromhage, L., 2005. Extremely short copulations do not affect hatching success in Argiope bruennichi (Araneae, Araneidae). J. Arachnol. 33, 663–669. Schneider, J.M., Fromhage, L., Uhl, G., 2005. Copulation patterns in the golden orbweb spider Nephila madagascariensis. J. Ethol. 23, 51–55. Schneider, J.M., Gilberg, S., Fromhage, L., Uhl, G., 2006. Sexual conflict over copulation duration in a cannibalistic spider. Anim. Behav. 71, 781–788. Schneider, J.M., Herberstein, M.E., DeCrespigny, F.C., Ramamurthy, S., Elgar, M.A., 2000. Sperm competition and small male size advantage for males of the golden orbweb spider Nephila edulis. J. Evol. Biol. 13, 939–946. Smedly, S.R., Eisner, T., 1996. Sodium: a male moth’s gift to its offspring. Proc. Natl. Acad. Sci. USA 93, 809–813. Snow, L.S.E., Andrade, M.C.B., 2004. Pattern of sperm transfer in redback spiders: implications for sperm competition and male sacrifice. Behav. Ecol. 15, 785–792. Suter, R.B., Parkhill, V.S., 1990. 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Contents lists available at ScienceDirect
Journal of Thermal Biology journal homepage: www.elsevier.com/locate/jtherbio
Effects of copulation temperature on female reproductive output and longevity in the wolf spider Pardosa astrigera (Araneae: Lycosidae) Zhanqi Chen, Xiaoguo Jiao n, Jun Wu, Jian Chen, Fengxiang Liu College of Life Sciences, Hubei University, Xueyuan Road 11, Wuchang, Wuhan 430062, Hubei, China
a r t i c l e in fo
abstract
Article history: Received 7 August 2009 Accepted 5 January 2010
The copulation duration of male wolf spider Pardosa astrigera, was significantly influenced by environmental temperature, as had been found in some insect species. Therefore, temperature during male courtship and copulation may influence the amount of sperm and seminal fluids transferred during copulation, which in turn could influence female fitness. In order to test this hypothesis, we subjected pairs of male and female P. astrigera to five temperature groups from 16 to 32 1C at an interval of 4 1C, and investigated whether and to what extent the various temperatures during male courtship and copulation influenced female reproductive output and female adult longevity under controlled laboratory conditions. With the increase of copulation temperature, females were more likely to lay egg sacs. The total egg sacs and lifetime fecundity of female were positively influenced by copulation temperature, whereas female lifetime spiderlings and adult longevity were independent of copulation temperature. & 2010 Elsevier Ltd. All rights reserved.
Keywords: Wolf spider Pardosa astrigera Copulation temperature Reproduction Longevity
1. Introduction Copulation duration plays important roles in male and female fitness (Edvardsson and Canal, 2006). Males may attempt to prolong the copulation duration for several fitness benefits, such as transferring amounts of sperm to fertilize fully female eggs (Schneider et al., 2000; Elgar et al., 2003). These include increasing sperm-associated seminal fluids that could decrease female sexual receptivity to subsequent suitors and stimulate oviposition (Bukowski and Christenson, 1997; Aisenberg et al., 2009), ensuring appropriate storage of the transferred sperm (Bukowski and Christenson, 1997) and/or preventing the female from remating with other males before oviposition (Edvardsson and Canal, 2006; Katsuki and Miyatake, 2009). Females may also benefit from controlling copulation duration if it helps to avoid harassment from other males (Andersson et al., 2000), to obtain more resources (Smedly and Eisner, 1996) or gain information about the quality of their mates (Eberhard, 1994). However, the prolonged copulation duration may incur costs to both sexes in terms of time, energy and higher risk exposure to predators and pathogens (Daly, 1978; Szira´nyi et al., 2005). Whatever its potential functions, there may exist a trade-off between the costs and benefits on the evolutionarily maintenance of the copulation duration within a species.
n
Corresponding author. Tel./fax: + 86 27 88661237. E-mail address: [email protected] (X. Jiao).
0306-4565/$ - see front matter & 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jtherbio.2010.01.002
Copulation duration of some insects and spiders is affected by a number of factors. To date, much attention has been paid to the biotic factors influencing copulation duration (e.g., species strains: Field et al., 1999; age: Field et al., 1999; Wilder and Rypstra, 2007; body size: Field et al., 1999; Schneider et al., 2000, 2005; Engqvist and Sauer, 2003; Wilder and Rypstra, 2007; body condition: Engqvist and Sauer, 2003; Wilder and Rypstra, 2007; mating status: Andre´s and Cordero Rivera, 2000; Bukowski et al., 2001; Danielson-Franc- ois and Bukowski, 2005; Schneider et al., 2005; Friberg, 2006; risk of sperm competition: Andre´s and Cordero Rivera, 2000; Schneider et al., 2000; Aisenberg et al., 2009; diet: Pe´rez-Staples and Aluja, 2004), whereas fewer studies have been focused on the abiotic factors, particularly the environmental temperature, a potential factor influencing copulation duration (but see Costa and Sotelo, 1984; Cook, 1994; Horton et al., 2002; Martin and Hosken, 2002; Jiao et al., 2009; Katsuki and Miyatake, 2009). Generally, copulation duration is negatively related to temperature in most invertebrates (Costa and Sotelo, 1984; Cook, 1994; Horton et al., 2002; Martin and Hosken, 2002; Jiao et al., 2009; Katsuki and Miyatake, 2009). With the increase of temperature, copulation duration decreases and the quantity of sperm and/or seminal fluids transferred decline (Katsuki and Miyatake, 2009). Considering the fact that temperature influences the rates of ectotherm physiological processes, it is unsurprising that the thermal environment may have a marked influence on spider growth (reviewed in Li and Jackson, 1996; Li, 1998), development (reviewed in Li and Jackson, 1996; Li, 2002), survival (reviewed in
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Li and Jackson, 1996; Li, 2002) and reproduction (reviewed in Li and Jackson, 1996) as well. Even though the effects of environmental temperature on female spider reproductive fitness, such as fecundity (reviewed in Li and Jackson, 1996) and fertility (reviewed in Li and Jackson, 1996; Hanna and Cobb, 2006) are well-documented, most studies are only carried out to determine the long-term temperature effect of the time window on reproductive performance from their sexual interaction to death (Demoraes and McMurtry, 1987; reviewed in Li and Jackson, 1996; Medeiros et al., 2003; Sa´nchez-Ramos et al., 2007). However, the potential effects of the temperature during male courtship and copulation on female reproductive output and female adult longevity remain largely unexplored. To understand such potential effects, there is a prerequisite for us to separate the effects of copulation temperature from the rearing temperature after female has been inseminated. The wolf spider P. astrigera is a wandering spider widely distributed in China. In most central provinces of China, there are two generations a year. P. astrigera overwinters as subadult in the soil or in the litter in natural habitats. Their reproductive peaks occur in early May (ca. 12 1C) of the overwintering generation and in early September (ca. 28 1C) of the next generation, respectively (Zhao, 1993). In a previous study, male P. astrigera copulation duration was negatively related to the copulation temperature (Jiao et al., 2009). The question arises whether male P. astrigera copulation duration is positively related to the quantity of sperm and/or seminal fluids transferred for such a relationship has been found in some insect species (Engqvist and Sauer, 2003; Bailey and Nuhardiyati, 2005). Female P. astrigera may receive fewer sperm and/or less seminal fluids from their mates under higher temperature (summer generation) relative to that under lower temperature (spring generation), which may decrease female reproductive fitness and longevity. In order to test this hypothesis, we aim to investigate whether and to what extent the various temperatures during male courtship and copulation influence female reproductive output and female adult longevity.
2. Materials and methods 2.1. Spiders We collected the overwintering P. astrigera subadults from cotton fields at Huazhong Agricultural University, Wuhan, Hubei Province, China, from November to December 2007. Spiders were kept visually isolated from each other in opaque Plexiglas enclosures (5.0 5.0 7.5 cm3, length width height) (SAIFU Inc., Ningbo, Zhejing, China) under laboratory conditions of 13:11 L:D photoperiod, 2470.5 1C and 50–70% RH. Each spider was fed with a combination of fruit flies, Drosophila melanogaster, and/or crickets, Acheta domesticus, every 3 days and had continual access to water by way of a soaked cotton wick inserted through a hole in the enclosure floor into a reservoir below. After their final molt, the spiders were weighted using an electronic analytical balance (to the nearest 0.1 mg, METTLER TOLEDO AB104-S, Switzerland) and used in experiments between 5 and 7 days postmolt. All test spiders were virgin and used not more than once.
2.2. Experimental design We began the experiment with virgin P. astrigera females and matched females for body mass in groups of five and randomly assigned each of them to one of the five temperatures: 16, 20, 24, 28 and 32 1C.
The mating experiment was carried out in a clear cylindrical glass container (10.5 12.0 cm2, diameter height) (SAIFU Inc., Ningbo, Zhejing, China). White filter paper covered the bottom of the container to provide a substrate suitable for spider locomotion. In each run, the experimental spiders were first held separately in the rearing enclosures at their prescribed temperature in the environmental chamber for 1 h prior to pairing. One randomly selected female and a male were introduced simultaneously into the glass container, and the courtship and copulation were observed constantly until a mating occurred or up to 30 min. We paired male and female and observed their mating until up to 20 females being successfully inseminated in each temperature group. Between experimental runs, the arenas were swabbed with alcohol, allowed to dry and the filter paper was replaced. After successful mating, the inseminated females in the glass container were kept out of the environmental chamber, and maintained under laboratory conditions of 13:11 L:D photoperiod, 2470.5 1C and 50 70% RH. Female reproductive behavior was monitored daily until their death. Egg laying and spiderling hatching were inspected and counted. After hatching of the young, empty egg sacs were collected from the bottom of the enclosures and the number of un-hatched eggs was counted. Female lifetime egg sacs (the total number of egg sacs female produced throughout her lifetime), female lifetime fecundity (total eggs female laid throughout her lifetime), female lifetime spiderlings (total eggs hatched throughout female lifetime) and female adult longevity (days from their final molt to death) were calculated and recorded, respectively. 2.3. Statistical analysis Data sets were analysed by ANOVA if they initially met the assumptions of normal distribution (Kolmogorov–Smirnov test) and equal variance (Levene test), or met after being square root transformed. Female lifetime fecundity and spiderlings were compared among various temperature groups using the ANCOVA procedure with copulation temperature as fixed factor and female body mass as a covariate as the latter strongly influences female lifetime fecundity and spiderlings. When there were significant differences among various copulation temperatures, comparisons for significant effects between copulation temperatures were performed using LSD post hoc tests. Because the number of egg sacs were not normally distributed even after being square root transformed, Kruskal–Wallis H test was used. Once the difference of Kruskal–Wallis H test was significant, Mann–Whitney U test at Bonferroni corrected P value was subsequently applied. All results are reported as mean7SE. Statistical analyses were performed with SPSS 13.0 (SPSS Inc., Chicago, IL, USA).
3. Results With the increase of copulation temperature, females were more likely to produce egg sacs (Pearson Chi-Square test: w2 =17.344, df= 4, P =0.002). Mated females that failed to lay egg sac throughout their lifetime were excluded from subsequent reproductive output analysis. The total number of egg sacs female produced throughout their lifetime differed significantly among various copulation temperatures (Kruskal–Wallis H test: H=30.066, Po0.0001). Multiple comparisons revealed that the number of egg sacs under higher copulation temperature (i.e., 28 and 32 1C) were significantly higher than those under lower copulation temperature (16 and 20 1C) (Fig. 1). Lifetime fecundity of female P. astrigera was positively influenced by female body mass (ANCOVA, F1.75 = 4.768, P=0.032) and by copulation temperature (F4.75 =3.038, P=0.022
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Fig. 1. Effects of copulation temperature on the production of egg sacs of Pardosa astrigera. Bars with the same letter are not significantly different. The number within the column indicating sample sizes. Error bars represent standard errors about the mean.
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Fecundity
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Temperature ( °C) Fig. 2. Effects of copulation temperature on lifetime fecundity of Pardosa astrigera. Bars with the same letter are not significantly different. The number within the column indicating sample sizes. Error bars represent standard errors about the mean.
Fig. 2). Female lifetime fecundity under the copulation temperatures of 16 and 20 1C was significantly lower relative to those under the higher copulation temperatures of 24, 28 and 32 1C. There were no significant differences in female lifetime fecundity across other copulation temperature. Although total spiderlings females produced throughout their lifetime were also positively influenced by female body mass (ANCOVA, F1.75 =4.897, P= 0.030), they were independent of copulation temperature (16 1C: 48.2 79.0; 20 1C: 49.577.2; 24 1C: 66.6 77.4; 28 1C: 66.1 77.6; 32 1C: 65.2 77.7; F4.75 = 1.590, P= 0.186). ANCOVA revealed that P. astrigera female adult longevity was neither significantly influenced by female body mass (ANCOVA, F1.93 =0.236, P=0.628), nor by copulation temperature (16 1C: 79.1 710.9; 20 1C: 82.879.4; 24 1C: 97.2 710.4; 28 1C: 102.2711.5; 32 1C: 98.4711.8; ANCOVA, F4.93 = 0.838, P= 0.504).
4. Discussion Our results demonstrate that the temperature during male courtship and copulation has unexpectedly positive effects on the production of egg sacs and lifetime fecundity in the wolf spider P. astrigera. However, copulation temperature has little effect on female lifetime spiderlings and female adult longevity. In the present study, contrary to our expectation, the number of egg sacs and lifetime fecundity of female were significantly higher under higher copulation temperature relative to those under lower copulation temperature. There are several possible explanations for such unexpected results. One possibility is that a
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correlation may exist between the rate of sperm transfer and copulation temperature. Although male P. astrigera copulation duration is negatively related to copulation temperature (Jiao et al., 2009), male may transfer sperm more efficiently under higher temperature relative to that under lower temperature. Such a temperature-dependent sperm transferring pattern is also found in three species of predatory bugs (Horton et al., 2002). Alternatively, the volume of seminal fluids male P. astrigera transferred under higher temperature is significantly larger, thus the females inseminated under higher temperature may receive more ovulation promoters derived from the ejaculate, such as hormones and/or neurotransmitters. And these stimuli may result in the marked increase of egg sacs and lifetime fecundity. Similar results are found in some insects (Horton et al., 2002; reviewed in Gillott, 2003). It should be acknowledged that the above two explanations are not mutually exclusive. Ultimately, we could not rule out the possibility that physical difficulty may occur when males transfer sperm and/or seminal fluids under lower temperature. Similar studies have been found in several insect species (Horton et al., 2002; Katsuki and Miyatake, 2009). Although a positive relationship between sperm transfer and copulation duration has been found in several spider species (Schneider et al., 2000, 2006; Schneider and Elgar, 2001). The pattern of duration-dependent sperm transfer is far from a general rule. A growing handful of studies have revealed a nonlinear relationship between the sperm transferred and copulation duration (Suter and Parkhill, 1990; Bukowski and Christenson, 1997; Bukowski et al., 2001; Snow and Andrade, 2004; Schneider and Fromhage, 2005; Szira´nyi et al., 2005). Therefore, the pattern of sperm transfer is apparently speciesspecific, and copulation duration may be not a reliable predictor for the quantity of the sperm transferred during copulation. Although the dynamics of sperm transfer of the male wolf spider P. astrigera is not well known, it has been indirectly evaluated in the closely related wolf spider Pardosa agrestis by interrupting copulation (Szira´nyi et al., 2005). This study showed that only 10 min of copulation was sufficient for male to fertilize all the eggs of female P. agrestis (Szira´nyi et al., 2005). Thus, we assume that the dynamics of sperm transfer of male P. astrigera is not duration-dependent and sperm transfer occurs relatively early. Such a pattern has been found in previous works (Suter and Parkhill, 1990; Bukowski and Christenson, 1997; Snow and Andrade, 2004; Schneider and Fromhage, 2005; Szira´nyi et al., 2005). Considering the lifetime spiderlings of female P. astrigera is independent of copulation temperature, the variation of female lifetime fecundity under various copulation temperature is presumably due to the variation of seminal fluids, rather than the quantity of sperm. The tentative conclusion is further supported by the fact that females are more likely to produce egg sacs with the increase of copulation temperature (Fig. 1). In the present study, despite female lifetime fecundity is significantly higher under higher copulation temperature relative to that under lower copulation temperature, female lifetime spiderlings remain constant. A similar temperature-dependent eggproducing pattern, with female producing higher numbers of eggs under higher temperature relative to that under lower temperature, is found in the tropical butterfly, Bicyclus anynana (Geister et al., 2008). Although female P. astrigera produces more eggs under higher copulation temperature, female lifetime spiderlings may to some extent be balanced by the detrimental influence of higher copulation temperature on sperm damage. Like the spider Stegodyphus lineatus (Maklakov and Lubin, 2006), wolf spider P. astrigera males, neither present their mates with nuptial gifts, nor do they deposit sperm in spermatophores. It is unlikely that female P. astrigera could receive direct material (nutrients) from males beyond sperm during copulation, which could at least in
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part account for the fact that female adult longevity is independent of copulation temperature. During copulation, male may transfer sperm and/or associated seminal fluids which affect female remating propensity and the rate of offspring production (reviewed in Gillott, 2003; Aisenberg and Costa, 2005; Edvardsson and Canal, 2006; Aisenberg et al., 2009). Generally, the depletion of sperm and/or seminal fluids transferred during copulation shortens female remating delay and decreases the rate of offspring production (reviewed in Gillott, 2003). The variation of the quantity of sperm and/or seminal fluids transferred during copulation due to copulation temperature may in turn affect female remating propensity (Cook, 1994; Katsuki and Miyatake, 2009). In the present study, given the substantial reduction in female reproductive output under lower copulation temperature, female may adopt adaptive behavior, such as remating to offset the reproductive cost. Whether female P. astrigera remains sexually receptive or not after she has been inseminated under lower copulation temperature deserves further determination. To our knowledge, this is the first study suggesting that the temperature during male courtship and copulation influences female lifetime fecundity. Considering the limited duration of the temperature during male courtship and copulation, the variation of female lifetime fecundity may not be directly related to temperature per se, but to the variation of copulation duration derived from copulation temperature. In order to account for the underlying mechanism by which the effects of copulation temperature on reproductive consequences in the wolf spider P. astrigera, the relationship between copulation duration and the amount of sperm and/or seminal fluids transferred under various temperatures demands further investigation.
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