Behavioral Ecology Vol. 15 No. 4: 602-606
Behavioral Ecology vol. 15 no. 4 © International Society for Behavioral Ecology 2004; all rights reserved
Sexual advertisement and immune function in an arachnid species (Lycosidae)
Department of Biological and Environmental Science, University of Jyväskylä, FIN-40351 Jyväskylä, Finland
Address correspondence to J. J. Ahtiainen. E-mail: jjahti{at}bytl.jyu.fi. R. Kortet is now at Neurobiology, Physiology & Behavior, University of California, Davis, CA 95616, USA. M. J. Rantala is now at Department of Biology, University of California, Riverside, CA 92521, USA
Received 15 October 2002; revised 22 July 2003; accepted 20 September 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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A simple version of the immunocompetence handicap hypothesizes that through condition-dependence, the size of the sexual trait may be positively related to immune function at the population level. In the present study, we investigated the relationship between sexual advertisement and immune function in a natural population of male wolf spiders, Hygrolycosa rubrofasciata (Araneae: Lycosidae). Males of H. rubrofasciata have a costly and condition-dependent acoustic signal, courtship drumming. In the mating season, males drum against dry leaves while wandering around the habitat searching for receptive females. Males increase their mating success by increasing their drumming rate and mobility. We used drumming rate and mobility measured without female proximity as estimates of sexual advertisement. As estimates of male immune function, we used encapsulation rate and lytic activity. Encapsulation rate is a common challenging technique, which measures immune response against multicellular parasites. Lytic activity is a monitoring technique, which measures immune response against pathogens. Our results show that males with higher drumming rate had higher encapsulation rate. This suggests that females might use drumming rate as a signal for choosing males with good immunocompetence. Moreover, our results show that males with higher mobility had higher lytic activity. As females are more likely to encounter those males that have higher mobility, this might also select males with better immune function. Our results suggest that the immunocompetence handicap might work also among spiders, although we could not assess the causality of the relationship between sexual selection and immune function in this correlational study.
Key words: Araneae, Hygrolycosa rubrofasciata, immunity, immunocompetence handicap, reproductive behavior, sexual selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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According to the immunocompetence handicap hypothesis, individuals face a trade-off between the expression of the sexual trait and immune function (Folstad and Karter, 1992
; Gustafsson et al., 1994; McKean and Nunney, 2001; Møller, 1995; Sheldon and Verhulst, 1996). At the population level, the "size" of the sexual trait and immune function may be positively related owing to condition-dependent expression of both traits (Møller and Saino, 1994; see also Møller et al., 1999; van Noordwijk and de Jong, 1986). For example, males may vary in their ability to withstand costs of sexual traits and immune function, so that males in poor condition have both smaller sexual trait and weaker immune function than do males in good condition. By choosing males with larger sexual traits, females may gain immunological benefits either directly or indirectly. The size of the sexual trait may indicate directly parasite burden of the mate (see Hurst et al., 1995; Saino and Møller, 1994) or indirectly the heritable component of the ability to resist various pathogens (see Johnsen et al., 2000; Kurtz and Sauer, 1999; Møller, 1990).
The term immunocompetence is often used to refer to the ability of the individual's immune system to resist and control pathogens and parasites (see Norris and Evans, 2000). In arthropods, one of the most informative ways to assay immunocompetence is to measure the magnitude of encapsulation response to a novel and standardized antigen, such as nylon monofilament (see Köning and Schmid-Hempel, 1995; Rantala et al., 2000, 2002; Siva-Jothy et al., 1998). Encapsulation is an immune response through which arthropods defend themselves against endoparasitoid wasps and flies (Salt, 1970). During the encapsulation process, hemocytes recognize invading particles as nonself and cause other hemocytes to aggregate and form capsules around particles. A cascade of reactions involving the tyrosine-phenyloxidase pathway causes melanization of the capsule, which results in the death of the parasite, for example, by asphyxiation (Fisher, 1963), or through the production of necrotizing compounds (Nappi et al., 1995). The invertebrate immune system is also comprised of a myriad of soluble proteins and enzyme cascades, which act in recognizing, signaling, and attacking microbial pathogens (Leonard et al., 1985) and probably in coordinating cellular responses (Pech and Strand, 1995). An informative monitoring technique in ecological immunology is to quantify lytic activity over time, which measures the status of the invertebrate immune system (see Ellis, 1990; Rantala and Kortet, 2003).
Male wolf spiders of Hygrolycosa rubrofasciata (Araneae: Lycosidae; Ohlert, 1865) have a drumming signal that is used for sexual communication (Kronestedt, 1996). During the mating season, males drum while wandering around the habitat searching for receptive females, which are more stationary than are males. Males produce drumming signals by hitting their abdomen on dry leaves or other suitable substrate to court females. One drumming consists of approximately 30–40 separate pulses, lasts approximately 1 s (Rivero et al., 2000), and is audible to the human ear up to a distance of several meters. In H. rubrofasciata, male courtship drumming has been shown to be an honest indicator of heritable viability (for review, see Ahtiainen et al., 2001). Females prefer more actively drumming males as mating partners (Kotiaho et al., 1996). There is considerable within-male repeatability and among-male variability in drumming rate (Kotiaho et al., 1996). Male drumming incurs both physiological (Kotiaho et al., 1998a; Mappes et al., 1996) and predation costs (Kotiaho et al., 1998b) that eventually cause the death of males in the end of the mating season (data not shown). The more actively drumming males have better viability (Kotiaho et al., 1996, 1999; Mappes et al., 1996). Survival costs of male drumming are condition dependent, being manifested in decreased viability of males in poorer condition (Kotiaho, 2000; Mappes et al., 1996). By choosing males with the highest drumming rates, females benefit through better offspring survival (Alatalo et al., 1998). Also, male mobility is positively associated with male mating success (Kotiaho et al., 1998b). Body mass is one of the most common sexually selected male traits among animal taxa (Andersson, 1994). However, male body mass does not seem to be intersexually selected and is not correlated with male mating success in H. rubrofasciata (Kotiaho et al., 1996; Mappes et al., 1996). In this correlational study, we investigated the relationship between sexual advertisement and immune function in a natural population of male wolf spiders, H. rubrofasciata, by using drumming rate and mobility measured without female proximity as estimates of sexual advertisement, and encapsulation rate and lytic activity as estimates of immune function. This is the first study, to our knowledge, examining the relationship between sexual selection and immune function in spiders.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Males of H. rubrofasciata were collected by using pitfall traps from a bog in Sipoo, Southern Finland (60°16' N and 25°14' E), from 3–4 May 2001 at the beginning of the mating season. Spiders were individually placed in small plastic film jars with some moss (Sphagnum spp.). They were kept in cool temperature (approximately 10°C) to keep their activity levels low. In the laboratory, spiders were weighed to the nearest 0.1 mg with an analytical balance (AND HA-202M). After body mass measurements, spiders were individually kept in film jars filled with some moss (Sphagnum spp.) at 5 ± 2°C in darkness. Food (Drosophila melanogaster) was provided ad libitum. These jars were moistened regularly.
For drumming rate and mobility measurements, we took each male randomly from the sample of all specimens and placed them individually in plastic arenas (125 x 88 x 110 mm high). The bottom of plastic arenas was covered with a piece of white paper (8 x 4 cm). To enable mobility measurements, each arena was divided with a line into two equal rectangles. Two dry even-sized birch leaves were placed in rectangles as drumming substrates (one leaf per rectangle). The laboratory was illuminated with fluorescent tubes and lamps with 40-W bulbs placed 30 cm above the floors of plastic arenas to give extra heat and light. On the day before behavioral observations, males were kept in the laboratory temperature (31 ± 1°C) for 2 h to trigger their sexual activity. Drumming rate was measured as the number of separate drumming bouts; mobility, as the number of times the male crossed a line between the rectangles. Drumming rate and mobility were measured five times for 2 min during the trial day, and this procedure was repeated on three consecutive days. Between and after the trial days, males were fed with fruit flies (D. melanogaster), and kept in moistened film jars filled with some moss (Sphagnum spp.) in cool temperature (5 ± 2°C) in darkness. The repeatabilities for drumming rate and mobility across trial days were moderate (drumming rate: R =.401; F192,386 = 3.012, p <.001; mobility: R =.379; F192,386 = 2.828, p <.001; for methods, see Krebs, 1989). After drumming rate and mobility measurements, males were randomly assigned to two different experimental treatments, that is, encapsulation rate (n = 94) and lytic activity experiment (n = 99).
In the encapsulation rate experiment, the first set of males (n = 94) was transferred from the cool-storage room (5 ± 2°C) to the laboratory (22°C) 60 min before the start of the experiment. Spiders were individually CO2-anaesthetized and taped laterally onto separate glass slides. One research assistant made all the implantations to eliminate the between-observer variation in measurements. A single sterile 1-mm-long piece of nylon monofilament (diameter = 0.08 ± 0.001 mm, Stroft) was inserted into the spider's hemocoel through a sterile incision made on the abdomen membrane between the epigastric furrow and the spiracle. The spider's immune system was allowed to encapsulate a microfilament for exactly 240 min, which had been preliminary tested to yield considerable between-individual variation to encapsulation rate (data not shown). Because the first test animal was 60 min in room temperature before the insertion of a microfilament, whereas the last test animal was over 200 min in room temperature before the manipulation, we took premanipulation time as a covariate. Premanipulation time is the time an animal is in warm temperature before the insertion of a microfilament. Premanipulation time takes into account the possible effect of increasing time in warm temperature on the animal's encapsulation rate. For the 240 min of encapsulation, spiders were kept in room temperature with constant moisture. The implant was then removed and dried. All the spiders died as a consequence of the microfilament removal, preventing us from calculating the within-individual correlation between encapsulation rate and lytic activity, and evaluating the repeatability of individual immune response. There is a scarce knowledge about parasite species in the wolf spider, H. rubrofasciata, but there are at least two parasitoids, a nematode (Mermithidae: Aranimermis spp.) and a fly (Acroceridae: Ogcodes pallipes; data not shown). These parasitoids cause reproductive failure and eventually the death of infected individuals. The prevalence of parasitoids was checked from each individual, ensuring that no spider was parasitized. The removed monofilament was photographed from three random angles under a light microscope with a digital video recorder. The pictures were then analyzed by using the Image Pro Plus – software (version 4.1). The degree of encapsulation was analyzed as a grey value of reflecting light from implants. As a measure of the individual's encapsulation rate, we used the average grey value calculated from three video pictures. The scale was calibrated to indicate that the darkest grey received the highest encapsulation rate. To measure the repeatability of this method, we randomly chose 16 implants and analyzed them as above. Repeatability was very high (R =.999, F15,16 = 731.5, p <.001).
In the lytic activity experiment, the second set of males (n = 99) was individually CO2-anaesthetized and taped laterally onto separate glass slides. One of the investigators took all the hemolymph samples. A 0.5 µl hemolymph sample was pipetted from a sterile puncture made on the abdomen membrane between the epigastric furrow and the spiracle. All the males died as a consequence of hemolymph sampling. The prevalence of parasitoids was checked from each individual, ensuring that no spider was parasitized. The lysozyme activity of the hemolymph was assayed turbidimetrically (see Ellis, 1990; Rantala and Kortet, 2003). A hemolymph sample was mixed with 20 µl phosphate buffered saline solution (PBS; 0.067 M phosphate and 0.9 % NaCl, at pH 6.4) and frozen at –80°C. After thawing, samples were vortexed and pipetted into a well microplate (Labsystems). PBS was used as a negative control. Then, samples and controls were mixed with 80 µl suspension-containing lyophilized cells of Micrococcus lysodeicticus bacterium (Sigma Chemical Co.; 0.20 mg/ml PBS). To minimize the time difference in the initiation of lytic reaction, bacterial solution was quickly pipetted to each sample (and control). Immediately after that, the optical density at 492 nm was measured at 22°C in minute intervals on a plate reader (Multiskan Plus, Flow Laboratories). The first value was taken at the onset of the assay. The enzymatic reaction in all samples took place during the first 10 min. As the optical density of control samples increased during the 10-min interval, the mean control value was subtracted from the observed values of the samples. This increase in optical density is likely to occur owing to the sedimentation of bacterial suspension, because plates cannot be vortexed during the plate reader analysis. Lytic activity was expressed as the change in optical density of a sample in the 10-min interval.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In the first set of males (n = 94), encapsulation rate was higher among males with higher drumming rates (Figure 1). Mobility or body mass had no effect on encapsulation rate. Encapsulation rate was partly explained by premanipulation time, but the partial effect of drumming rate remained significant (partial linear regression: R2 =.139, F4,89 = 3.61, p =.009; drumming rate ß = 0.35, t = 2.46, p =.016; mobility ß = –0.23, t = –1.65, p =.102; body mass ß = 0.064, t = 0.644, p =.521; premanipulation time ß = 0.24, t = 2.34, p =.022). The swap between dependent (encapsulation rate) and independent variable (drumming rate) in the regression analysis did not change the results.
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In the second set of males (n = 99), lytic activity was higher among males with higher mobility (Figure 2). Drumming rate or body mass had no effect on lytic activity (partial linear regression: R2 =.085, F3,95 = 2.96, p =.036; drumming rate ß = –0.18, t = –1.40, p =.17; mobility ß = 0.37, t = 2.88, p =.005; body mass ß = –0.048, t = –0.49, p =.62). The swap between dependent (lytic activity) and independent variable (mobility) in the regression analysis did not change the results.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In this correlational study with a wild population of H. rubrofasciata, males with higher drumming rate had higher encapsulation rate (Figure 1). In male wolf spiders, H. rubrofasciata, courtship drumming has been shown to be an honest viability indicator for choosy females (for review, see Ahtiainen et al., 2001
). Our results suggest that females might use drumming rate also as a signal for choosing males with good immunocompetence. Our results also showed that males with higher mobility had higher lytic activity (Figure 2). As females are more likely to encounter those males that have higher mobility, this might also select males with better immune function. Future studies should focus on a simultaneous manipulation of both immune function and sexual traits coupled with an examination of the effects of different combinations of these two on survival. Such experimental tests would give us an insight into whether sexual traits may be evolutionarily costly through reduced immune response.
Our results are consistent with previous findings with insects, which have shown that the size of male sexual traits is positively associated with male immune function. For example, it has been shown that the size of the male ornament, wing spots, is positively correlated with male immunocompetence in the damselfly, Calopteryx splendens (Rantala et al., 2000; see also Siva-Jothy, 2000). In C. splendens, the size of male wing spots is condition dependent and sexually selected, females preferring males with larger wing spots (Siva-Jothy, 1999). In mealworm beetles (Tenebrio molitor), Rantala et al. (2002) have demonstrated that females prefer pheromones from males with good immunocompetence. Preferred males had a faster encapsulation rate against a novel antigen and higher levels of phenoloxidase in hemolymph. In male house crickets, Acheta domesticus, Ryder and Siva-Jothy (2000) have found a positive relationship between the number of syllables per chirp and hemocyte load. As A. domesticus females favor males with more syllables per chirp, it is plausible that this preference also selects males with high pathogen resistance ability. In field crickets (Gryllus bimaculatus), Rantala and Kortet (2003) have shown that females prefer courtship song from males with high encapsulation rate.
Our results that there was not any relationship between encapsulation rate and mobility, or between lytic activity and drumming rate stress the need for multiple measures of immune function before making any further conclusions. One way of testing whether encapsulation process is actively taking part on immune defense is to vary the time animals are in warm temperature before implantation, that is, premanipulation time (60–233 min in the present study). If encapsulation process is effectively taking place, one could expect a positive relationship between encapsulation rate and premanipulation time. Interestingly, encapsulation rate increased with premanipulation time in males of H. rubrofasciata. This indicates that there was a clear activation of melanization process over the time males were in warm temperature.
It is possible that males with better immune function could also have better viability, indicated by higher drumming rate (see Kotiaho, 2000; Kotiaho et al., 1996, 1999). Unfortunately, we were not able to answer to that question in the present study, because all the males died as a consequence of the immunological sampling. Saino et al. (1997) have found evidence for the positive relationship between immunocompetence and viability in male barn swallows, Hirundo rustica. H. rustica males that showed the highest immune response to sheep red blood cells were more likely to survive until the breeding season. Also, H. rustica males with comparatively long tails had better survival compared with that of males with short tails. Therefore, by preferring males with long tails, H. rustica females may acquire the "good genes" for high immunocompetence.
The costs of maintaining a certain level of immune function may be smaller in individuals in good than in poor condition, as individuals in good condition have more resources to allocate on immune function (see Møller et al., 1998). Also, there can be condition dependence in the expression of sexual traits: Individuals in good condition are better able to bear costs of sexual traits and, therefore, produce larger sexual traits than do individuals in poor condition (for review, see Kotiaho, 2001). Through condition dependence of both the size of the sexual trait and immune function, the size of the sexual trait may be positively related to immune function at the population level (Møller and Saino, 1994; see also Møller et al., 1999; Van Noordwijk and de Jong, 1986). In H. rubrofasciata, survival costs of male courtship drumming have demonstrated to be condition dependent (Kotiaho, 2000; Mappes et al., 1996). However, whether immune function of H. rubrofasciata is condition dependent is not known. In literature, there has not been found any general pattern between immune function and condition in insects. In Anopheles gambiae (Diptera: Culicidae), nutritional deprivation during larval stages decreases the ability of adults to respond to synthetic immune challenge (Suwanchaichinda and Paskewitz, 1998). In Drosophila melanogaster, short-term nutritional deprivation decreases encapsulation percentage of eggs of a larval parasitoid (Vass and Nappi, 1998). Conversely, noctuids (Lepidoptera: Noctuidae) die faster from the infection of baculoviruses, when hosts increase their nutritional intake (Hoover et al., 1998).
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ACKNOWLEDGEMENTS |
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We thank Ville Hahkala, Panu Halme, Pasi Hiljanen, Jani Koskimäki, Marjo Laurikainen, Helinä Nisu, Tapio van Ooik, Mira Patja, Jaana Suutari, Katja Tynkkynen, and Ilona Yliniemi for assistance in the field and laboratory. We thank Ilmari Jokinen, Janne Kilpimaa, and anonymous referees for valuable comments on the earlier version of the manuscript. The work was financed by the Academy of Finland to R.V.A., and by the Emil Aaltonen Foundation to R.K.
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