Density-dependent plasticity of sequential mate choice in a bushcricket

Density-dependent plasticity of sequential mate choice in a bushcricket (Orthoptera: Tettigoniidae)

Gerlind U.C. Lehmann¹

Department of Zoology, University of Western Australia

Dr. Gerlind U.C. Lehmann

Freie Universität Berlin

Institut für Zoologie

Abteilung Evolutionsbiologie

Königin-Luise-Straße 1-3

14195 Berlin

Germany

Fax: ++49 - 3329 - 69 79 645

e-mail: gerlind.lehmann@t-online.de

www.guclehmann.de
word count: 6834

Abstract

Mate choice is a common phenomenon in animals and several factors have been proposed as being involved in the acceptance or rejection of a partner. I investigated the effect of population density on the mate sampling behaviour of female Xederra charactus bushcrickets. In my study, female bushcrickets adjusted the tactic of sequential mate sampling in response to mate density, visiting a series of up to five different males per night. Females under low-density conditions visited fewer males in a night and were less likely to reject a copulation attempt than females under high-density conditions. Rejection of a male during copulation was 29 percent in areas of high population density, but only eight percent in areas of low population density. Moreover, at low densities, females were less likely to reject mates later in the night, which can be interpreted as a reaction to the time constraints of a finite nightly mating period. Females in high-density populations also more often chose males with a higher mass of the spermatophore producing accessory glands. Due to such choice, females might receive a larger nuptial gift at mating. These results are consistent with tactical models of search behaviour in which females adjust their behaviour to the number of potential mates and the length of the mating period.

Introduction

Animals of most species do not mate indiscriminately but prefer some partners over others (Andersson 1994). Mate choice is the outcome of female preference and of female sampling behaviour (Wagner 1998; Cotton et al. 2006; Kokko and Rankin 2006). Several benefits may be gained by discriminating among potential mates, especially when they provide direct benefits (Johnstone 1995; Møller and Jennions 2001; Kokko et al. 2003). Sexually reproducing individuals must find and select appropriate mates. The number of potential mates can therefore have an important influence on reproductive strategies. There is no reason to assume that selective pressures should be the same at high and low-density populations. However it is surprising that the number, or density, of potential mates has received scant attention when examining evolutionary processes in mating systems (Kokko and Rankin 2006). Population density might influence the decisions of individuals, since time and energy expenditure, and predation risk (due to greater search times), are likely to increase with decreasing mate density (Härdling and Kaitala 2005; Kokko and Rankin 2006). Individuals may also become less choosy as the mating season advances (Real 1990; Collins and McNamara 1993; Luttbeg 2004). This is because fewer opportunities for mating remain, and the expected future fitness gains from continuing to search for a mate is consequently lower (Johnstone 1997).

There is evidence that in many animals individuals must assess mates sequentially rather than simultaneously, but they are nevertheless able to choose more “attractive partners” (Gibson and Langen 1996; Mazalov et al. 1996; Milinski 2001). Theoretical analyses of a range of sequential sampling tactics (fixed threshold rule, sequential comparison rule, one-step-decision rule or best-of-n-rule; see Reid and Stamps 1997; Bateman et al. 2001, for overviews) suggest that when choice is costly, the optimal tactic is to accept mates who exceed some critical level of quality, this level being adjusted to the expected return from continued search (Real 1990; Dombrovsky and Perrin 1994; Getty 1995). Such an “adjustable threshold” will result in the acceptance of a high quality mating partner if the search costs are low. With an increase of costs individuals will accept a partner of lower quality to minimise the search costs. Potential costs include time and energy expenditures (Thornhill 1984; Alatalo et al. 1988; Milinski and Bakker 1992) or increased susceptibility to predation (Magnhagen 1991; Forsgren 1992; Hedrick and Dill 1993; Godin and Briggs 1996; Grafe 1997; deRiviera et al. 2003).

In non-flying bushcricket species, mortality increases with travel distance (Heller and von Helversen 1990; Heller 1992), so population density might influence directly the predation risk during mate searching. Laboratory experiments with two other Australian bushcricket species, Kawanaphila nartee and Requena verticalis, indicate some role for population density on mate choice; male bushcrickets mating behaviour changes with previous female encounter rate (Shelly and Bailey 1992; Allen and Bailey 1994). Also female crickets of the genus Gryllus alter their mate choice depending on previous experience with males or song models (Wagner et al. 2001; Bateman et al. 2001, 2004). The flightless species Xederra charactus used here might in general, behave similarly as other bushcricket species studied so far, as males call to attract females.

In several bushcricket species, larger or heavier males are favoured by females (overview in Gwynne 2001). In the bushcricket P. zimmeri the preference of heavier males is a preference for the provider of a larger spermatophore (Lehmann and Lehmann in press). In the majority of bushcricket species, males transfer a nuptial gift during mating (Gwynne 2001). Ingredients in the spermatophore, which are incorporated into the somatic tissue by females (Voigt et al. 2006), also induce a refractory period in males and females, during which they are reluctant to remate (review in Gwynne 1997; see also Lehmann and Lehmann 2000). Larger spermatophores may have fecundity-enhancing benefits for females or increase offspring survival (reviews in Vahed 1998, 2007; Gwynne 2001).

In this study, I tested the hypothesis that density affects the mating responses of the Australian bushcricket, Xederra charactus. I established different mate densities in field enclosures. Manipulating the density on the same area also reduces the number of available mating partners. However, the alternative approach to manipulate density by having the identical number of bushcrickets on different areas, has other limitations; travel distances will than be different and therefore the implicit risk of predation. I assumed that female bushcrickets exhibit more choosy behaviour in high-density populations. Female bushcrickets have control over the copulation by approaching males for mating and are able to reject unsolicited mating attempts. Therefore I assume females are the choosing sex. There are situations in which bushcrickets show role reversal in mate choice, but these situations are only found under food limiting conditions (Gwynne and Simmons 1990; Simmons and Bailey 1990; Simmons 1992). Male rejection is therefore hypothesised to reflect female preferences.

Specifically, I tested the following predictions about changes in mate selectivity under high versus low population density:

Because mated male and female bushcrickets show a “time out” from reproductive activity (Lehmann and Lehmann 2007) the number and variance of matings should be quite similar between the densities, given a primary sex ratio of 1:1.

As in most insects (Bonduriansky 2001), X. charactus mates are accessed sequentially. Under high density, the expected costs (energy, predation and time) are lower. I expected females to sequentially visit more males under high compared to low population density. As a result, the acceptance rate for the first male might be higher under low, compared to high-density populations.

The bushcricket species tested here is nocturnal, with mating activities restricted to the short dark cycle. Towards the end of the night the probability of finding a mate decreases as more and more males drop out of the mating pool, because males only mate once a night. I therefore predicted that a single night represents a finite time horizon for the mating behaviour (see Backwell and Passmore 1996; Thomas et al. 1998) of a bushcricket, leading to a decreasing mate choice with the time of night. However, females in a lower density population might have a higher first male acceptance rate, at any given time, than females at high population density, because opportunities to choose between males is more restricted.

In several bushcricket species nuptial feeding provide females with direct benefits (Gwynne 2001; Vahed 2007). It is therefore not surprising, that females of the bushcricket species P. zimmeri prefer heavier males, which provide larger spermatophores (Lehmann and Lehmann in press). In the Australian bushcricket Kawanaphila mirla males with larger spermatophore producing accessory glands obtained more matings with virgin females (Lehmann and Lehmann 2007). Therefore I predict that males with larger spermatophore producing accessory glands will get more matings at high density. Under low density, such female preference might diminish, because the opportunity for a choice, and therefore to opportunity for sexual selection, might be weak.

By observing all contacts between marked individuals it is possible to analyse female sampling behaviour. Any comparison tactic (including pooling sampling tactics) of mate choice, like “best-of-n”, requires at least the sampling of two males by females during the search process. Any comparison tactic of mate choice also requires that females revisit previous encountered males in the same night. In contrast, threshold tactics assume that females establish a threshold criterion for male acceptance. Such threshold tactics predict that females will sometimes accept the first male they encounter, depending on male quality. Threshold tactics do not predict revisits of particular males, except by chance.

The Species and Study Area

Collection of Individuals

For the experimental study, virgin adults were released into field enclosures randomly located in the Tuart Forest NP. Three mosquito nets were hung between trees, each of them covering a ground area of two square meters. These "gauze cages" were fixed along their base to keep out predators, such as spiders, ants and beetles. The cages were established with an equal primary sex ratio (1:1). Two cages contained six males and six females each (low population density), the third cage contained 18 individuals of each of the two sexes (high population density). These densities are realistic, as I observed densities from five to 20 individuals per square meter in the field (unpublished data), which corresponded with the availability of their natural food source, germinating grasses. Each individual was uniquely identified by marking it with a numbered reflecting tape around the hind femur (Heller and Helversen 1990) and a colour code on the pronotum.

In X. charactus, females and males approach each other until the antennae come into contact. This phase of antennae contact can last for more than thirty minutes, during which time both partners sit motionlessly, one beneath the other but showing mutual antennation. I identified this phase as antennae contact. Mate rejection occurred when females walked away from the male, sometimes followed by the male. No incident of rejection by the male was observed during these experiments. If pair formation proceeds, the male crawls under the female. The undersides of both sexes are in physical contact, but the heads are turned in opposite directions, leading to a head-to-genitalia position. This is an unusual position for bushcrickets and is followed by an attempt by the male to grasp the female with his cerci. To achieve this, the male bends down his abdomen towards the female’s basal fold at the base of the ovipositor, to lock in his cerci. Pairs remain in this coupled position for up to two hours. During this period, abdominal movements were observed in the coupled mates. If the pair separates without transfers of the spermatophore, I classified the interaction as ending in copula. Alternatively, the male transfers the sperm-containing ampulla, which becomes attached directly to the female genital opening, with its associated sperm-free spermatophylax attached proximal to the ampulla. This I called successful spermatophore transfer. After transfer of the nuptial gift, females use the spermatophore as a food resource. Sperm and seminal fluids pass from the ampulla to the female’s spermatheca while the female consumes the spermatophylax.

To identify possible parameters used by females to choose a male I measured body dimensions. For measurements of body size I used the length of the pronotum and the length of the right hind femur. Measurements were obtained with a pair of Mitutoyo callipers (accuracy 0.01 mm). Five days after the end of the experiments I determined the wet mass of the males and then killed them, measured body dimensions and dissected and weighed the wet weight of the spermatophylax producing accessory glands on a Mettler Toledo AG 245 scale (± 0.01 mg). It is well known, that mating history influences male investment into the spermatophore. Males of X. charactus remated in the course of the experiment after one to two days. Feeding for five additional days post end of experiment was used to compensate for different mating history during the course of the experiment. Therefore differences in the weight of the glands five days post experiment reflect the condition of the males, as males with a better condition will be able to invest more into the glands. Measurements of body mass were also made at this time. Males assigned randomly to the three cages did not differ in hind femur, pronotum length, body weight or glandular weight (ANOVA: df=2: p= ns).

Statistical analysis using WinSTAT^® für Excel Vers. 2001.1 (Beneke and Schwippert 2001) were two-tailed in all cases. Multiple regression analysis was used to test for sexual selection on male body dimensions.

Results

Number of Matings

Matings were observed between 2100 and 0300 hours. Within this time horizon of six hours the number of observed matings followed a Gaussian curve regardless of population density, with most matings occurring around midnight (Fig. 1). No significant differences in the mating frequency between the cages could be found (Chi-square test for each time interval: ²₂, df=2, p<0.05).

Figure 1

Mate Choice

Finite Time Horizon

Multiple regressions of different body parameters revealed a significant correlation with male mating success in the high but not in the low-density populations (Table 1). A positive relationship between male glandular mass and mating number in males was found for the high-density population only. Another significant relationship existed between pronotum length and the number of matings. The other three measured dimensions had no influence on mating success.

Males were scattered within the 2m² cages, so females had to choose sequentially between them. Females sampled up to three males under low-density conditions and up to five males under high-density conditions (compare Fig. 3). Any comparison tactic requires at least the sampling of two males by females during the search process. However, over fifty percent of females chose the first encountered mate (compare Fig. 3), suggesting that females were not using a “best-of-n” tactic for choosing mates. Any comparison tactic of mate choice also requires that females revisit previous encountered males in the same night. Such a pooling sampling tactic could be rejected, as females revisited previous encountered males in the same night only in 2.17 percent of the cases (n=227).

While females of X. charactus mated, on average, the same number of times over seven nights, females in the higher density cage tended to reject more males before copulating. Active mate choice is evident from the observations that X. charactus females visit several prospective mates, but choose only one of them per night. This active choice also included the rejection of undesired partners. Although female bushcrickets are initially attracted by song characteristics (Bailey 1991; Forrest and Raspet 1994) they might narrow down their choice among visited males using additional cues (Gwynne 2001), reflecting the potential for sexual selection during copulation. There is amble evidence not only for female sequential mate choice, but for male sequential mate choice as well (Wong et al. 2004; Bateman and Fleming 2005; Byrne and Rice 2006). However, females had control over matings in my study, therefore I restrict my discussion to the female perspective.

Mate rejection during physical engagement occurred at high rates in X. charactus; one third of the partners split off during antennae contact, with identical rates in both mate densities. By contrast, rejection during copulation varied with density; one third of all coupled pairs separated before spermatophore transfer in high density population, compared to eight percent in low density population. Thus, females with a higher potential encounter rate were more discriminating during copulation. Females in the high-density population tended to choose males with a larger glandular mass: sexual selection acting on males was evident only under these high-density conditions.

During the search process of a single night up to five different males were visited in succession, indicating a sequential mate choice tactic. The number of visits during male assessment was affected by population density (see Fig. 3), albeit the absolute number of visits was relatively low in comparison to other animals (Gibson and Langen 1996). Two factors might explain this restrictive search behaviour: (1) X. charactus is a flightless species, so that travelling between mates can be assumed to be costly (see Heller 1992 for the results in the similar sized and flightless Greek bushcricket P. veluchianus). (2) If the process of choice itself is time-consuming, as in the bushcrickets, searching for other partners might be time constrained (Reid and Stamps 1997).

Choosiness varies due to the differing availability of partners in X. charactus. In the high density population the probability of meeting more partners was higher and therefore the acceptance probability for an actual mate was reduced. The ultimate factor behind this finding might be the implicit risk of a prolonged search, even if predators were prevented from entering the experimental cages in this study. The evolution of the mating system might be largely imposed by natural selection due to predation, as shown in the bushcricket P. mariannae (Lehmann and Lehmann 2006). It also might be a response to the necessary search time. A reduced density therefore implies, that a longer and more risky search must be conducted. In the Greek bushcricket P. veluchianus, travel distance of females is negatively correlated with the survival rate (Heller 1992), due to predation by spiders and other predators (Heller and Helversen 1990).

In theory, choosiness is influenced by ecological constraints at the time of mating. Models predict that individuals should become less choosy as the season progresses (Real 1990; Collins and McNamara 1993; Johnstone 1997). Choosiness tends to be strongest at the beginning of the mating period (Crowley et al. 1991). As the end of the season approaches, fewer opportunities for sampling remain, and the expected future fitness gains from continuing to search for a mate are consequently lower (Johnstone 1997). In X. charactus the acceptance rate of mates increases linearly with the time of the night (Fig. 4), which can be interpreted as a reaction to the time constraints of a finite nightly mating period.

Analyses of body dimensions showed that at high mate densities the weight of the glandular mass was positively correlated with the number of matings obtained by males. I propose that females are able to deduce the amount of transferable glandular mass during copulation. How females achieve this is unclear, but the extended time of copulation might give females the opportunity to measure the hydraulic pressure of a males’ abdomen and use this as a criterion of male quality. Measurements from the bushcricket species P. veluchianus shows a correlation between glandular mass and the amount of spermatophylax transferred at mating (Heller and Reinhold 1994). Females obtain reproductive benefits by spermatophylax donation. For example, an increased size of this paternal investment positively influences the number/size of subsequently laid eggs (Gwynne 1997; Arnqvist and Nilsson 2000) and additionally increases egg (Gwynne 1988) and larval survival (Reinhold 1998). In contrast to the reproductive benefit, mating per se incurs costs in regard to longevity in other bushcricket species (e.g. in K. nartee: Simmons and Kvarnemo 2006). At present, it is not clear, whether this mortality costs outweigh the benefits of nuptial feeding for females.

While a more or less direct comparison of the qualities of potential mates is possible in lekking species, even when challenging (Gibson 1996), it is prevented in nonlekking cases: potential mates have to be examined sequentially (Mazalov et al. 1996). In the present study the majority of partners choose the first encountered mate, rejecting the possibility for “best-of-n” mate choice tactics. Females also very rarely revisited a male in the same night, rejecting the pooling sampling tactic. The data are consistent with threshold tactics of mate acceptance as females accepted in most cases the first male they encountered and revisited males only by chance. Bushcrickets appeared to adjust their acceptance threshold in response to mate density and time constraints. These results suggest that females do not use a fixed-threshold search rule in which they mate with any male with a phenotype that exceeds a given threshold. Instead, females appear to use a more complex search rule in which they adjust their searching behaviour based on the local distribution of male phenotypes (see Wagner et al. 2001).

But under which conditions might such an adjustable threshold function be the best strategy? With a short time horizon, it is more effective to rely on an innate image. The same is true if searching individuals must make repeated samplings within the same deme during successive breeding cycles (Mazalov et al. 1996). These predictions are met in X. charactus bushcrickets, where mates are sampled during the night and successive matings occur within the same deme over subsequent nights (nonetheless mating occurred only once in a single night).

Overall, research on sexual selection has largely concentrated on which mates are chosen and why, ignoring the processes by which prospective mates are evaluated (Gibson and Langen 1996; Reid and Stamps 1997; Kokko and Rankin 2006). The present study reveals that the tactic of sequential mate sampling is adjusted in response to mate density. This threshold is also balanced against the finite time horizon. As the night proceeds discrimination is successively lowered. These results support the theoretical notion (reviewed in Kokko and Rankin 2006) that mate choice can be altered by population density.

This study would not have been possible without the help of Winston J. Bailey who invited me to the University of Western Australia, Zoology Department, and provided office and research space during my stay. Arne Lehmann helped with the field experiments. I thank Gregory Voigt (Conservation and land management, CALM, Busselton) for his help and the opportunity to work inside the national park. Brenton Knott generously loaned me camping equipment for the field experiments. Darryl Gwynne, Klaus-Gerhard Heller, Robert Hickson, Arne Lehmann and two anonymous referees gave helpful criticism on the manuscript and Robert Hickson improved the English. The research was funded by a postdoctoral grant from the DAAD.

Alatalo, R. V., Carlson, A., and Lundberg, A. (1988). The search cost in mate choice of the pied flycatcher. Animal Behaviour 36, 289-291.

Allen, G. R., and Bailey, W. J. (1994). Female encounter rate and the calling behavior and mating propensity of male Requena verticalis (Orthoptera: Tettigoniidae). Behavioral Ecology and Sociobiology 34, 63-69.

Andersson, M. B. (1994). ‘Sexual selection’. Princeton. (Princeton University Press: Princeton.)

Arnqvist, G., and Nilsson, T. (2000). The evolution of polyandry: multiple mating and female fitness in insects. Animal Behaviour 60, 145-164.

Backwell, P. R. Y., and Passmore, N. I. (1996). Time constraints and multiple choice criteria in the sampling behaviour and mate choice of the fiddler crab, Uca annulipes. Behavioral Ecology and Sociobiology 38, 407-416.

Bailey, W. J. (1991). ‘Acoustic behaviour of insects’. (Chapman and Hall: London.)

Bakker, T. C. M., and Milinski, M. (1991). Sequential female choice and the previous male effect in sticklebacks. Behavioral Ecology and Sociobiology 29, 205-210.

Bateman, P. W., and Fleming, P. A. (2005). Males are selective too: mating, but not courtship, with sequential females influences choosiness in male field crickets (Gryllus bimaculatus). Behavioral Ecology and Sociobiology, 59, 577-581.

Bateman, P. W., Gilson, L. N., and Ferguson, J. W. H. (2001). Male size and sequential mate preferences in the cricket Gryllus bimaculatus. Animal Behaviour 61, 631-637.

Bateman, P. W., Ferguson, J. W. H., and Ferreira, M. (2004). The influence of physical and acoustic experience on sequential mate preference in the cricket Gryllus bimaculatus. Is song important? Journal of Insect Behavior 17, 843-855.

Beneke, T., and Schwippert, W. (2001). ‘WinSTAT für Excel Vers. 2001.1’. (Fitch Software: Germany).

Bonduriansky, R. (2001). The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biological Reviews 76, 305-339.

Briscoe, A. D., and Chittka, L. (2001). The evolution of color vision in insects. Annual Review of Entomology 46, 471-510.

Byrne, P. G., and Rice, W. R. (2006). Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster. Proceedings of the Royal Society of London B 273, 917-922.

Collins, E. J. (1995). The effect of recent experience on female choice in zebra finches. Animal Behaviour 49, 479-486.

Collins, E. J., and McNamara, J. M. (1993). The job-search problem with competition: an evolutionary stable dynamic strategy. Advanced Applied Probability 25, 314-333.

Cotton, S., Small, J., and Pomiankowski, A. (2006). Sexual selection and condition-dependent mate preferences. Current Biology 16, R755-R765.

Crowley, P. H., Travers, S. E., Linton, M. C., Cohn, S.L., Sih, A., and Sargent, R. C. (1991). Mate density, predation risk, and the seasonal consequence of mate choice: a dynamic game. American Naturalist 137, 567-596.

deRiviera, C. E., Backwell, P. R. Y., Christy, J. H., and Vehrencamp, S. L. (2003). Density affects female and male mate searching in the fiddler crab, Uca beebei. Behavioral Ecology and Sociobiology 53, 72–83.

Dombrovsky, Y., and Perrin, N. (1994). On adaptive search and optimal stopping in sequential mate choice. American Naturalist 144, 355-361.

Downhower, J. F., and Lank, D. B. (1994). Effects of previous experience on mate choice by female mottled sculpins. Animal Behaviour 47, 369–372.

Forrest, T. G., and Raspet, R. (1994). Models of female choice in acoustic communication. Behavioral Ecology 5, 293-303.

Forsgren, E. (1992). Predation risk affects mate choice in a gobiid fish. American Naturalist 140, 1041-1049.

Getty, T. (1995). Search, discrimination and selection: mate choice by pied flycatchers. American Naturalist 145, 146-154.

Gibson, R. M. (1996). Female choice in sage grouse: the roles of attraction and active comparison. Behavioral Ecology and Sociobiology 39, 55-59.

Gibson, R. M., and Langen, T. A. (1996). How do animals choose their mates? Trends in Ecology and Evolution 11, 468-470.

Godin, J.-G. J., and Briggs, S. E. (1996). Female mate choice under predation risk in the guppy. Animal Behaviour 51, 117-130.

Grafe, T. U. (1997). Costs and benefits of mate choice in the lek-breeding reed frog, Hyperolius marmoratus. Animal Behaviour 53, 1103-1117.

Gwynne, D. T. (1988). Courtship feeding and the fitness of female katydids (Orthoptera: Tettigoniidae). Evolution 42, 545-555.

Gwynne, D. T. (1997). The evolution of edible ‘sperm sacs’ and other forms of courtship feeding in crickets, katydids and their kin (Orthoptera: Ensifera). In: ‘The evolution of mating systems in insects and arachnids’ (Eds J. C. Choe and B. Crespi.). pp. 110-129. (Cambridge University Press: Cambridge.)

Gwynne, D. T. (2001). ‘Katydids and bush-crickets: reproductive behavior and the evolution of the Tettigoniidae’. (Cornell University Press, Ithaka.)

Gwynne, D. T., and Simmons, L. W. (1990). Experimental reversal of courtship roles in an insect. Nature 346, 172-174.

Härdling, R., and Kaitala, A. (2005). The evolution of repeated mating under sexual conflict. Journal of Evolutionary Biology 18, 106–115.

Hedrick, A. V., and Dill, L. M. (1993). Mate choice by female crickets is influenced by predation risk. Animal Behaviour 46, 193-196.

Heller, K.-G. (1992). Risk shift between males and females in pair forming behavior of bushcrickets. Naturwissenschaften 79, 89-91.

Heller, K.-G., and von Helversen, O. (1990). Survival of a phaneropterid bush cricket studied by a new marking technique (Orthoptera: Phaneropteridae). Entomologia Generalis 15, 203-208.

Heller, K.-G., and Reinhold, K. (1994). Mating effort function of the spermatophore in the bushcricket P. veluchianus (Orthoptera, Phaneropteridae): support from a comparison of the mating behaviour of two subspecies. Biological Journal of the Linnean Society 53, 153-163.

Johnstone, R. A. (1995). Sexual selection, honest advertisement and the handicap principle: Reviewing the evidence. Biological Reviews 70, 1-65.

Johnstone, R. A. (1997). The tactics of mutual mate choice and competitive search. Behavioral Ecology and Sociobiology 40, 51-59.

Kokko, H., and Rankin, D. J. (2006). Lonely hearts or sex in the city? Density-dependent effects in mating systems? Philosophical Transactions of the Royal Society of London B 361, 319-334.

Kokko, H., Brooks, R., Jennions, M. D., and Morley, J. (2003). The evolution of mate choice and mating biases. Proceedings of the Royal Society of London B 270, 653-664.

Lehmann G.U.C., and Lehmann, A.W. (2000). Female bushcrickets mated with parasitized males show rapid remating and reduced fecundity (Orthoptera: Phaneropteridae: Poecilimon mariannae). Naturwissenschaften 87, 404-407.

Lehmann G.U.C., and Lehmann, A.W. (2006). Potential lifetime reproductive success for male bushcrickets following parasitism by a phonotactic fly. Animal Behaviour 71, 1103-1110.

Lehmann, G. U. C., and Lehmann, A. W. (2007). Sex differences in "time out" from reproductive activity and sexual selection in male bushcrickets (Orthoptera: Zaprochilinae: Kawanaphila mirla). Journal of Insect Behavior DOI: 10.1007/s10905-007-9076-1

Lehmann, G. U. C., and Lehmann, A. W. (in press). Bushcrickets song is essential for female mate choice of heavier males, who provide larger direct (material) benefits. Behavioral Ecology and Sociobiology

Luttbeg, B. (2004). Female mate assessment and choice behaviour affect the frequency of alternative male mating tactics. Behavioral Ecology 15, 239-247.

Magnhagen, C. (1991). Predation risk as a cost of reproduction. Trends in Ecology and Evolution 6, 183-186.

Mazalov, V., Perrin, N., and Dombrovsky, Y. (1996). Adaptive search and information updating in sequential mate choice. American Naturalist 148, 123-137.

Milinski, M. (2001). The economics of sequential mate choice in sticklebacks. In: ‘Model systems in behavioural ecology: integrating conceptual, theoretical and empirical approaches’ (Ed. L. A. Dugatkin). pp. 245-264. (Princeton University Press: Princeton.)

Milinski, M., and Bakker, T. C. M. (1992). Costs influence sequential mate choice in sticklebacks, Gasterosteus aculeatus. Proceedings of the Royal Society of London B 250, 229-233.

Møller, A. P., and Jennions, M. D. (2001). How important are direct fitness benefits of sexual selection? Naturwissenschaften 88, 401-415.

Real, L. (1990). Search theory and mate choice I. Models of single-sex discrimination. American Naturalist 136, 376-404.

Reid, M. L., and Stamps, J. A. (1997). Female mate choice tactics in a resource-based mating system: field tests of alternative models. American Naturalist 150, 98-121.

Reinhold, K. (1998). Paternal investment in Poecilimon veluchianus bushcrickets: beneficial effects of nuptial feeding on offspring viability. Behavioral Ecology and Sociobiology 45, 293-299.

Shelly, T. E., and Bailey, W. J. (1992). Experimental manipulation of mate choice by male katydids: the effect of female encounter rate. Behavioral Ecology and Sociobiology 30, 277-282.

Simmons, L. W. (1992). Quantification of role reversal in relative parental investment in a bush cricket. Nature 358, 61-63.

Simmons, L. W., and Bailey, W. J. (1990). Resource influenced sex roles of zaprochiline tettigoniids (Orthoptera: Tettigoniidae). Evolution 44, 1853-1868.

Simmons, L. W., and Kvarnemo, C. (2006). Costs of breeding and their effects on the direction of sexual selection. Proceedings of the Royal Society of London B 273, 465-470.

Thomas, F., Liautard, C., Cézilly, F., and Renaud F. (1998). A finite time horizon influences sequential mate choice in male Gammarus aequicauda (Amphipoda). Canadian Journal of Zoology 76, 401-405.

Thornhill, R. (1984). Alternative female choice tactics in the scorpion-fly Hylobittacus apicalis (Mecoptera) and their implications. American Zoologist 24, 367-383.

Vahed, K. (2007). All that glisters is not gold: sensory bias, sexual conflict and nuptial feeding in insects and spiders. Ethology 113, 105-127.

Valone, T. J. (2006). Are animals capable of Bayesian updating? An empirical review. Oikos 112, 252-259.

Voigt, C. C., Lehmann, G. U. C., Michener, R. H., and Joachimski, M. M. (2006). Nuptial feeding is reflected in tissue nitrogen isotope ratios of female katydids. Functional Ecology 20, 656-661.

Wagner, W. E. jr (1998). Measuring female preferences. Animal Behaviour 55, 1029-1042.

Wagner, W. E. Jr, Smeds, M. R., and Wiegmann, D. D. (2001). Experience affects female responses to male song in the variable field cricket Gryllus lineaticeps (Orthoptera, Gryllidae). Ethology 107, 769-776.

Wiegmann, D. D., Real, L. A., Capone, T. A., and Ellner, S. (1996). Some distinguishing features of models of search behavior and mate choice. The American Naturalist 147, 188-204.

Wong, B. B. M., Jennions, M. D., and Keogh, J. S. (2004). Sequential male mate choice in a fish, the Pacific blue-eye Pseudomugil signifier. Behavioral Ecology and Sociobiology 56, 253–256.

Table 1: Lehmann

Figure 1: Lehmann

High density (n = 143)
29 %

Antennae Split up

contact

21 %

Copula Separation



50 %

Spermatophore

transfer

Low densities (n = 39 and 45)

26-29 %

Antennae Split up

contact

4-5 %

Copula Separation



67-69 %

Spermatophore

transfer

Figure 2: Lehmann

Figure 3: Lehmann

Figure 4: Lehmann

Figure 5: Lehmann