TY - JOUR
AU - Herberstein, Marie E.
AB - Abstract Courtship signals are expected to be consistent within but vary between males of different qualities. Such traits are, therefore, predicted to exhibit high repeatability. However, studies have shown that courtship behaviors vary greatly in their within-individual repeatability, resulting in substantial variation in their ability to reflect male quality. This has implications for the evolution of female mate choice and courtship communication, as low levels of repeatability may reflect courtship signals that do not provide accurate quality information to females. In this article, we tested whether male courtship shuddering in the tropical orb-web spider, Argiope radon , influences female mate choice. We also tested whether male shudder performance reflects male phenotypic condition and is repeatable. We found that male shudder performance and condition predicted female latency to move onto the mating thread, a measure of mate preference. Aspects of male shudder performance were positively correlated with male body condition. Further, we found surprisingly high levels of repeatability in male courtship shuddering, ranking among the highest levels recorded to date for courtship behavior. We suggest that male courtship shuddering functions as an important indicator of male quality, with strong potential to respond to selection. INTRODUCTION Females are expected to base mate choice decisions on traits that vary consistently between males of different qualities, such as courtship performance ( Zahavi 1975 ; Alatalo et al. 1998 ; Hoefler et al. 2009 ). However, it is becoming increasingly apparent that courtship traits vary considerably in their capacity to indicate male condition or quality ( Kokko et al. 2002 ; Lehtonen 2012 ). This is reflected in substantial variation across studies in measurements of male courtship consistency, or “repeatability,” which may be defined as the behavioral variation between but not within individuals of a given species ( Lessells and Boag 1987 ; Boake 1989 ; Bell et al. 2009 ). High repeatability in courtship behavior may help identify traits that are informative for females when the differences in male performance vary consistently with quality. In turn, low repeatability may indicate courtship behaviors that do not reflect individual quality or traits that exhibit little genetic variation between individuals and are also less likely to represent traits that influence female mate preferences ( Potti and Merino 1997 ; Rivero et al. 2000 ; Hoefler et al. 2009 ; Reinhold 2011 ). Highly repeatability of a behavioral trait will generally increase its evolutionary potential (assuming an underlying additive genetic basis to the trait), because selection can then more accurately and consistently distinguish among individuals, that is, the within-individual component of trait variation is relatively low ( Boake 1989 ; Aragaki and Meffert 1998 ; Sattman and Cocroft 2003 ; Nakagawa et al. 2007 ; Hoefler et al. 2009 ; Fowler-Finn and Rodríguez 2013 ). Repeatability may also help to indicate traits that have a strongly heritable basis. Indeed, repeatability is often used to provide a useful estimate of the upper bounds of broad-sense heritability ( Brooks and Endler 2001 ; Bell et al. 2009 ; Hoefler et al. 2009 ; but see Dohm 2002 ). Sexually selected traits that provide information about mate quality are expected to have both high repeatability and high heritability ( Boake 1989 ; Rowe and Houle 1996 ; Hoefler et al. 2009 ) and often show condition-dependent expression ( Rowe and Houle 1996 ; Kemp and Rutowski 2007 ; Kemp 2008 ; Hoefler et al. 2009 ). Repeatability is also an important measure in animal personality research, which can drive individual mate choice decisions ( Sih et al. 2004 ; Dingemanse et al. 2010 ; Schuett et al. 2010 ; Jandt et al. 2014 ). Studies that explore the repeatability of courtship behaviors can, therefore, increase our understanding of both the evolution of courtship and the possible historic and future selective responses of constituent behavioral traits ( Nakagawa et al. 2007 ; Fowler-Finn and Rodríguez 2013 ). Here, we test which courtship behaviors are used by female web-building spiders as indicators of male quality, and whether those behaviors exhibit high repeatability, as predicted for sexual signals (sensu Zahavi 1975 ). Web-building spiders are particularly useful models for examining the theoretical predictions of repeatability and female choice. These systems are amenable to both field and laboratory studies, exhibit a diverse array of courtship behaviors, and results can be interpreted against established postcopulatory mechanisms and behaviors ( Herberstein, Schneider, Uhl, et al. 2011 ; Herberstein and Hebets 2013 ). Argiope is a genus of orb-web spiders in which courtship proceeds primarily via vibrations that travel through the web and includes elements such as shuddering, which comprises multiple anteroposterior rocks ( Table 1 ; see also Robinson and Robinson 1980 ; Wignall and Herberstein 2013a ). Shuddering behaviors in this genus appear to be particularly significant, given that they influence female aggression (and hence cannibalism risk), and correlate with female mate choice behaviors ( Wignall and Herberstein 2013a , 2013b ). However, to date, the repeatability of shuddering behavior has not been explored, and we know little about its potential to signal individual quality. Table 1 Details of the traits of male courtship behavior measured from each repeatability trial Behavior . Details of the analysis . Time travel Time for the male to travel across the silk dragline, beginning with the male’s first touch of the silk thread to the male’s first touch of the wooden frame Shudder number Number of shudders per trial Number of rocks Beginning with the start of the male’s first rock to the end of the male’s last rock that was deliberately driven by his legs (not including the time the male spent passively moving on the silk thread after a shudder due to momentum) Shudder duration Time for the male to complete a shudder, beginning with the start of the male’s first rock, to the end of the male’s last rock that was deliberately driven by his legs Shudder interval Duration between shudders within a trial Shudder ratio Shudder duration divided by number of rocks Behavior . Details of the analysis . Time travel Time for the male to travel across the silk dragline, beginning with the male’s first touch of the silk thread to the male’s first touch of the wooden frame Shudder number Number of shudders per trial Number of rocks Beginning with the start of the male’s first rock to the end of the male’s last rock that was deliberately driven by his legs (not including the time the male spent passively moving on the silk thread after a shudder due to momentum) Shudder duration Time for the male to complete a shudder, beginning with the start of the male’s first rock, to the end of the male’s last rock that was deliberately driven by his legs Shudder interval Duration between shudders within a trial Shudder ratio Shudder duration divided by number of rocks Open in new tab Table 1 Details of the traits of male courtship behavior measured from each repeatability trial Behavior . Details of the analysis . Time travel Time for the male to travel across the silk dragline, beginning with the male’s first touch of the silk thread to the male’s first touch of the wooden frame Shudder number Number of shudders per trial Number of rocks Beginning with the start of the male’s first rock to the end of the male’s last rock that was deliberately driven by his legs (not including the time the male spent passively moving on the silk thread after a shudder due to momentum) Shudder duration Time for the male to complete a shudder, beginning with the start of the male’s first rock, to the end of the male’s last rock that was deliberately driven by his legs Shudder interval Duration between shudders within a trial Shudder ratio Shudder duration divided by number of rocks Behavior . Details of the analysis . Time travel Time for the male to travel across the silk dragline, beginning with the male’s first touch of the silk thread to the male’s first touch of the wooden frame Shudder number Number of shudders per trial Number of rocks Beginning with the start of the male’s first rock to the end of the male’s last rock that was deliberately driven by his legs (not including the time the male spent passively moving on the silk thread after a shudder due to momentum) Shudder duration Time for the male to complete a shudder, beginning with the start of the male’s first rock, to the end of the male’s last rock that was deliberately driven by his legs Shudder interval Duration between shudders within a trial Shudder ratio Shudder duration divided by number of rocks Open in new tab The orb-web spider Argiope radon ( Levi 1983 ) is a tropical spider that builds webs over the edges of riverbanks in northern Australia ( Rao et al. 2009 ). To examine whether shuddering behavior may be used as an indicator of male quality, we tested whether male A. radon courtship shudder performance influences female mate choice behaviors during mating trials. We predicted that females would select mates based on their performance in traits with high repeatability as an honest indicator of male quality. We also assessed whether there is a relationship between male courtship behavior and phenotypic condition (sensu Schulte-Hostedde et al. 2005 ), as predicted for mate quality indicator traits ( Rowe and Houle 1996 ). We also tested whether male courtship shudder performance is repeatable using controlled courtship assays. Given the reliance of females on vibratory courtship for information, we predicted high levels of repeatability in male courtship behavior. MATERIALS AND METHODS Study animals We collected 15 male and 15 female A. radon from the banks of the Katherine River (Northern Territory, Australia). Males were collected as adults, and females were collected as subadults. Male spiders were maintained in individual plastic cups (300mL), upturned with mesh lids for ventilation. Female spiders were maintained in individual Perspex frames (50×50×10cm) in which they could build orb-webs. The laboratory was maintained at 25–27 °C and 50–60% humidity on a 12:12h light:dark cycle. Spiders were provided with water daily and fed twice weekly on flies or crickets ( Drosophila melanogaster , Musca domestica , and Acheta domesticus ). Courtship progresses stereotypically in A. radon , similar to other species of Argiope ( Robinson and Robinson 1980 ; Wignall and Herberstein 2013a ). Males enter the female’s web on a frame thread and approach the hub where the female is located, shuddering periodically as soon as he comes into contact with silk. Once at the hub, the male spends some time tapping the female and “tasting” her, continuing to shudder sporadically. During this time, he also performs sporadic bouts of abdominal wags (comprising multiple dorsoventral abdominal pumps). The male then cuts out a section of the female’s web and builds a silk line across the gap called a mating thread ( Robinson and Robinson 1980 ; Wignall and Herberstein 2013a ). The male then hangs from the mating thread and begins to bounce and pluck the thread. A female that decides to mate with the male will move up to the thread and hang from it in a characteristic “acceptance” or “copulatory” posture that allows the male to approach and copulate ( Robinson and Robinson 1980 ; Herberstein et al. 2002 ). Experimental procedure: male courtship performance and female choice We concentrated on male courtship shuddering due to its apparent significance in mediating mate cannibalism and female preference in related Argiope species ( Wignall and Herberstein 2013a , 2013b ). We tested whether male courtship performance correlates with known behavioral signatures of female choice. Note that due to the high risk of cannibalism during courtship and copulation, we tested the repeatability of shuddering behavior (see methods below) prior to running the female choice tests. Female preference in orb-web spiders may be assayed via latency to move onto the mating thread and copulation duration ( Elgar et al. 2000 ; Herberstein et al. 2002 ; Wignall and Herberstein 2013a ). To measure latency, we paired each male with a novel virgin female (i.e., a female that was not previously used as a stimulus for one of his 5 repeatability trials). All spiders had at least 1 week between being used in repeatability assays and mating trials. Males were weighed prior to the beginning of a mating trial. A male was released at the base of a female’s web and allowed to make his own way into the web. Male courtship performance during his approach to the hub is highly correlated with his performance in the repeatability assays in related species of Argiope (Magris M, Wignall A, Herberstein M, unpublished data). Courtship was recorded until the end of copulation ( n = 12), with latency for the female to move onto the mating thread recorded to the nearest 0.1 s and copula duration recorded to the nearest 1 s. After copulation ended, the spiders were collected and photographed using a Canon 600D SLR (Canon Inc., Tokyo, Japan) attached to a Motic SMZ-168 microscope (Motic, China). Femur–patella length of the first leg was measured to the nearest 0.001mm using ImageJ ( http://rsb.info.nih.gov/ij/ ) ( Herberstein et al. 2002 ). Male and female body condition was calculated as the residual value from a least-squares regression of body weight against leg length ( Jakob et al. 1996 ; Schulte-Hostedde et al. 2005 ; Shamble et al. 2011 ; Yip and Rayor 2013 ). Experimental procedure: male courtship repeatability To assay male courtship repeatability, we simulated the scenario of a male making his first approach across the web to the female. We achieved this by pulling a dragline from a virgin adult female’s spinnerets and stretching it across a 300-mm frame, angled at ~45° ( Figure 1 ). The female, still in her web, was placed beside the wooden frame to allow passive flow of her pheromones across the experimental arena but prevent her any opportunity to respond to the male’s courtship. To begin a trial, male subjects were held in a vial (25mL) attached to the lower left side of the wooden frame ( Figure 1 ) to acclimate for 2min. The vial lid was then removed, and subjects were allowed to make their own way out of the vial and onto the wooden frame. Subjects were rested for an hour by returning them to their home cups that they were maintained in, then reassayed. This relatively short interval between trials is analogous to the natural situation as male spiders often encounter multiple females within short spaces of time due to female’s tendencies to form aggregations ( Rao et al. 2009 ). Figure 1 Open in new tabDownload slide The repeatability assay test apparatus. Spiders were acclimatized in the vial before being released to run along the silk thread toward the female in her web at the other end of the wooden frame. Figure 1 Open in new tabDownload slide The repeatability assay test apparatus. Spiders were acclimatized in the vial before being released to run along the silk thread toward the female in her web at the other end of the wooden frame. During a typical trial, males would exit the vial, move onto the silk dragline and up toward the female, shuddering at intervals until they reached the end of the silk thread. We recorded each trial using high-speed video at 300 frames per second (Casio Ex-F1 digital camera; Casio America, Inc.). Each male ( n = 14) was assayed 5 times, using silk pulled from a different female each time. Males were weighed after they had completed the 5 assays. Each female was used for either 4 or 5 males, and her ID was controlled for in subsequent analyses (see below). For each repeatability trial, we measured a suite of behaviors that characterize male courtship, with particular emphasis on shuddering behavior (see Table 1 for list of behaviors and details of the scoring). Videos of male courtship were scored blind with respect to male identity by observing and measuring behaviors played back in slow motion in Adobe Soundbooth CS4 v2.01 (Adobe Systems Incorporated). Some measurements were not obtained because not all males shuddered during a trial, and some shuddered only once ( Supplementary Table 1 ). Within each male’s 5 courtship trials, we averaged shudder duration, number of rocks, shudder ratio, and shudder interval ( Table 1 ). This generated 5 series of scores for each male, with each series of scores representing his behavior in an individual courtship trial. Statistical analyses Several courtship traits that we measured represented different aspects of 1 courtship behavior (e.g., shudder duration and number of rocks within each shudder). As a result, several of our courtship variables were autocorrelated. To solve this, we ran non-linear iterative partial least squares (NIPALS) principal component analysis (PCA) in R using ade4 package (“nipals” function) to identify the principal axes of variation and to generate variables that are more holistic representations of individual courtship behaviors (specifically, courtship shuddering). This technique reduced the variables into principal components that represent orthogonal axes of variation in male courtship ability and that also reduced the probability of Type I errors in subsequent hypothesis testing. From the NIPALS PCA, we extracted the principal component scores for each male. These principal component scores were then used in subsequent analyses as measures of male courtship performance. We used the information theoretic approach ( Burnham and Andersson 2002 ) to assess which courtship behaviors influenced female choice behaviors (latency to move onto the mating thread and copulation duration). We used the R package “AICcmodavg” for model selection among candidate generalized linear models (Gaussian family). Candidate models to explain female choice included the independent variables principal component 1 (PC1), principal component 2 (PC2), male condition, female condition, cannibalism, and interactions between these variables. We chose the model with the lowest Akaike’s information criterion value (highest AICcWt) as the best model, using AICc for small sample sizes. To further assess the potential influence of individual behavioral traits on female choice behaviors, we generated individual models for each male courtship trait. Models included the male courtship trait, male condition, and the interaction between the trait and male condition. This post hoc exploratory approach allows the generation of specific hypotheses for experimental tests. We tested whether male courtship was repeatable using the principal component scores. Repeatability was calculated from intraclass correlation coefficients ( Lessells and Boag 1987 ) in the R package “irr,” with the function “icc,” using a 2-way Anova (to account for having random factors of both the male identity and female stimulus identity) and unit “average.” Including the unit “average” in the Anova test acknowledges that our behavioral scores for each of the 5 repeatability assays were means. For example, if a male shuddered multiple times in an assay, we calculated the mean shudder duration and used that mean as his duration score for that particular assay. This method of calculating repeatability is very strong for behavioral data. However, the function “icc” has only limited scope for testing for the effects of trial order (the sequence of repeatability trials). Therefore, we also tested for trial order effects separately. We also calculated the coefficient of variation to measure natural variation present in individual courtship behaviors that females may use as a source of information about male quality ( Gabor and Aspbury 2008 ; Fowler-Finn and Rodríguez 2013 ). All analyses were conducted using R version 2.15.0 ( R Foundation for Statistical Computing 2010 ). RESULTS Two principal components were extracted from the NIPALS PCA of male shudder behavior assays ( Table 2 ). Based on the loadings matrix for each principal component, high values of PC1 represent long shudder durations and long intervals between shudders ( Table 2 ). In turn, high values of PC2 represent long time to travel across the silk dragline and low shudder ratios ( Table 2 ). Female latency to move onto the mating thread was best predicted by the model PC1 + PC2 + Male condition ( Table 3 ). Copula duration was not influenced by male shuddering behavior ( Table 4 , all P > 0.50). Male condition positively correlated with PC1 (Spearman’s ρ = 0.70, P < 0.01; Figure 2a ) but did not correlate with PC2 (Spearman’s ρ = −0.41, P = 0.15; Figure 2b ). Shudder number was the only individual behavior to show an individual effect on female latency to move onto the mating thread ( Table 3 ). No other individual model effects were discerned for female latency to move onto the mating thread or copula duration. Table 2 NIPALS PCA for male courtship behavior and coefficients of variation (CV) for each courtship trait . PC1, shudder timing . PC2, time ratio . CV . Time travel 0.32 0.55 148.15 Shudder number 0.32 0.03 74.33 Shudder duration 0.57 −0.40 18.67 Number of rocks 0.40 −0.09 18.59 Shudder interval 0.54 0.34 154.87 Shudder ratio 0.12 − 0.65 13.55 Eigenvalue 4.61 1.72 Variance explained (%) 72.9 27.1 Repeatability 0.82 0.72 . PC1, shudder timing . PC2, time ratio . CV . Time travel 0.32 0.55 148.15 Shudder number 0.32 0.03 74.33 Shudder duration 0.57 −0.40 18.67 Number of rocks 0.40 −0.09 18.59 Shudder interval 0.54 0.34 154.87 Shudder ratio 0.12 − 0.65 13.55 Eigenvalue 4.61 1.72 Variance explained (%) 72.9 27.1 Repeatability 0.82 0.72 Principal component loadings >0.5 and <−0.5 are shown in bold. Open in new tab Table 2 NIPALS PCA for male courtship behavior and coefficients of variation (CV) for each courtship trait . PC1, shudder timing . PC2, time ratio . CV . Time travel 0.32 0.55 148.15 Shudder number 0.32 0.03 74.33 Shudder duration 0.57 −0.40 18.67 Number of rocks 0.40 −0.09 18.59 Shudder interval 0.54 0.34 154.87 Shudder ratio 0.12 − 0.65 13.55 Eigenvalue 4.61 1.72 Variance explained (%) 72.9 27.1 Repeatability 0.82 0.72 . PC1, shudder timing . PC2, time ratio . CV . Time travel 0.32 0.55 148.15 Shudder number 0.32 0.03 74.33 Shudder duration 0.57 −0.40 18.67 Number of rocks 0.40 −0.09 18.59 Shudder interval 0.54 0.34 154.87 Shudder ratio 0.12 − 0.65 13.55 Eigenvalue 4.61 1.72 Variance explained (%) 72.9 27.1 Repeatability 0.82 0.72 Principal component loadings >0.5 and <−0.5 are shown in bold. Open in new tab Table 3 Predictors for female Argiope radon latency to move onto the mating thread . t . P value . Effect size (semi-partial R ) . Best overall model (AICc = 146.86)  PC1 −2.43 0.04 −0.55  PC2 1.21 0.26 0.28  Male condition 3.10 0.01 0.71 Individual effects  Shudder number −2.31 0.05  Male condition 1.61 0.15  Shudder number × Male condition −0.23 0.82 . t . P value . Effect size (semi-partial R ) . Best overall model (AICc = 146.86)  PC1 −2.43 0.04 −0.55  PC2 1.21 0.26 0.28  Male condition 3.10 0.01 0.71 Individual effects  Shudder number −2.31 0.05  Male condition 1.61 0.15  Shudder number × Male condition −0.23 0.82 Significant P values (∞ = 0.05) are shown in bold. Open in new tab Table 3 Predictors for female Argiope radon latency to move onto the mating thread . t . P value . Effect size (semi-partial R ) . Best overall model (AICc = 146.86)  PC1 −2.43 0.04 −0.55  PC2 1.21 0.26 0.28  Male condition 3.10 0.01 0.71 Individual effects  Shudder number −2.31 0.05  Male condition 1.61 0.15  Shudder number × Male condition −0.23 0.82 . t . P value . Effect size (semi-partial R ) . Best overall model (AICc = 146.86)  PC1 −2.43 0.04 −0.55  PC2 1.21 0.26 0.28  Male condition 3.10 0.01 0.71 Individual effects  Shudder number −2.31 0.05  Male condition 1.61 0.15  Shudder number × Male condition −0.23 0.82 Significant P values (∞ = 0.05) are shown in bold. Open in new tab Table 4 Parameters included in the best model predicting copula duration . t . P value . Effect sizes (semi-partial R ) . Best overall model (AICc = 167.16)  PC1 −0.06 0.96 −0.02  PC2 −0.16 0.88 −0.05  Male condition −0.63 0.55 0.19 . t . P value . Effect sizes (semi-partial R ) . Best overall model (AICc = 167.16)  PC1 −0.06 0.96 −0.02  PC2 −0.16 0.88 −0.05  Male condition −0.63 0.55 0.19 Open in new tab Table 4 Parameters included in the best model predicting copula duration . t . P value . Effect sizes (semi-partial R ) . Best overall model (AICc = 167.16)  PC1 −0.06 0.96 −0.02  PC2 −0.16 0.88 −0.05  Male condition −0.63 0.55 0.19 . t . P value . Effect sizes (semi-partial R ) . Best overall model (AICc = 167.16)  PC1 −0.06 0.96 −0.02  PC2 −0.16 0.88 −0.05  Male condition −0.63 0.55 0.19 Open in new tab Figure 2 Open in new tabDownload slide Correlation between male condition and (a) PC1 and (b) PC2. Figure 2 Open in new tabDownload slide Correlation between male condition and (a) PC1 and (b) PC2. The repeatability of each principal component was extremely high (PC1 = 0.82, PC2 = 0.72; both P < 0.01). There was no effect of test order on male courtship performance (PC1, F1,68 = 0.24, P = 0.62 and PC2, F1,68 = 0.02, P = 0.88). DISCUSSION In A. radon , female mate choice behavior, specifically latency to move onto the mating thread, was influenced by male courtship behaviors that show extremely high repeatability. Male courtship behaviors show significant variation between individuals and some degree of condition dependence. These behaviors, therefore, show strong potential to indicate male quality, and females appear to base mate choice decisions on male performance, as we predicted. The individual consistency of courtship among males of different conditions (quality) suggests a heritable basis to courtship behavior and is consistent with strong potential to respond to selection. However, we still know very little about how female choice behavior translates into male paternity success in this species or indeed many other species. Although we expected to find repeatability in shuddering behavior, the observed level of repeatability was surprisingly high compared with a mean repeatability of 0.37 in a recent meta-analysis of behavioral repeatability across vertebrates and invertebrates ( Bell et al. 2009 ). Courtship studies generally observe higher levels of repeatability than mate preference studies ( Bell et al. 2009 ), but our estimates still reside at the upper extreme of those previously reported. To date, relatively few studies have examined repeatability in spiders ( Bonte et al. 2009 ; Rodríguez and Gloudeman 2011 ; Pruitt and Riechert 2012 ; McGinley et al. 2013 ). To our knowledge, only 2 studies have assessed the repeatability of male courtship components. Both of these studies tested male wolf spider courtship and found marked differences in the levels of courtship repeatability ( Hygrolycosa rubrofasciata , signal shape, r = 0.09, pulse rate, r = 0.84, Rivero et al. 2000 ; Pardosa milvina , leg raises/minute, r = 0.03–0.46 depending on male condition, Hoefler et al. 2009 ). The repeatability reported for pulse rate in H. rubrofasciata compares with that observed in PC1 for A. radon here. Both values appear high in relation to estimates for other courtship traits in wolf spiders and species across other taxa ( Bell et al. 2009 ). These are both vibratory courtship signals, which may lend themselves to higher repeatabilities more than the visual leg raises in P. milvina , perhaps due to differences in sensory sensitivity and processing abilities. Female web-building spiders are often highly aggressive and also exhibit high levels of sexual cannibalism ( Elgar 1991 ; Wilder et al. 2009 ). Males thus often risk injury, or death, when approaching a female. The high levels of danger inherent to courtship behavior in spiders may generate strong selection for high repeatability in male courtship signals to increase the information available to females about male identity (i.e., not prey), intent, and/or quality ( Wignall and Herberstein 2013a , 2013b ). This is also particularly evident given recent work that indicates that one signal in web-building spiders may serve multiple functions (e.g., delay female aggression and signal male quality; Wignall and Herberstein 2013a , 2013b ). Female web-building spiders are extremely sensitive to web vibrations but have very poor vision ( Herberstein and Wignall 2011 ). As a result, females cannot identify males visually but rely on vibratory discrimination of males from prey. Prey-generated vibrations are characterized by an initial impact vibration ( Wignall and Taylor 2011 ) and quick changes in amplitude ( Barth 1982 ). Our experiments indicate that male courtship shudders are, in contrast, characterized by a high degree of temporal repetitiveness. In presenting females with a repeatable vibratory signature in the webs during the initial stages of courtship, male spiders may reduce the risk that a female will respond aggressively toward the vibrations he generates in the web. Male body condition appears to be linked to shuddering performance in A. radon . This is in contrast to Argiope keyserlingi males, who do not exhibit any correlation between body condition and courtship performance ( Wignall and Herberstein 2013a ). However, there is some indication that shuddering behavior is energetically costly, as male A. keyserlingi reduce their shuddering effort once having completed the risky, initial approach to the female at the hub ( Wignall and Herberstein 2013a ). Shudders may require short, powerful bursts of energy (per individual shudder) or sustained energy (for maintenance of shudder duration and rate). These 2 alternate forms of energy (short bursts and endurance) appear subject to performance trade-offs in some spiders ( McGinley et al. 2013 ). The energy requirements of shudder performance may hence provide insights into the male performance abilities that are preferred by females. Interestingly, copula duration is not correlated with male courtship performance, either in A. radon or A. keyserlingi ( Wignall and Herberstein 2013a ). Copula duration is often positively correlated with either the amount of sperm transferred or male paternity success ( Simmons 2002 ). However, in spiders, the general pattern remains unclear. Male spiders appear to transfer the bulk of their sperm relatively early in copulation ( Snow and Andrade 2004 ; Schneider et al. 2005 ). A long copulation is only associated with an increase in sperm storage when the male is cannibalized in A. keyserlingi ( Herberstein, Schneider, Harmer, et al. 2011 ). Long copulations also increase the effectiveness of male genital plugging ( Herberstein et al. 2012 ). Given that females appear to exert some control over copula duration within related Argiope ( Elgar et al. 2000 ; Herberstein et al. 2012 ), it would make sense that female A. radon would end copulation with lower quality males earlier. However, the prevalence of plugging behavior and the association with sperm transfer and copula duration have yet to be investigated in this species. Present evidence supports cryptic female choice in this species, with copula duration playing only a minor, if any, role in male paternity success. Our study illustrates a potentially significant model system with which to study the evolution of courtship behavior. The high individual repeatability of male courtship shuddering, coupled with its potential to indicate male phenotypic condition and its role in male attractiveness, all point to an intriguing role for this trait as a sexually selected quality indicator. More generally, we propose that web-based courtship in spiders presents unique opportunities to examine courtship evolution, heritability, and the trade-offs inherent in a system that imposes considerable constraints on signal design. SUPPLEMENTARY MATERIAL Supplementary material can be found at Supplementary Data FUNDING This work was supported by The Australia & Pacific Science Foundation (APSF 11/05) and a Macquarie University Research Fellowship Grant (A.E.W.). We would like to thank A. Harmer for assistance in the field. A. Harmer, M. Magris, H. Gow, and P. Taylor provided useful discussions, and 2 anonymous referees provided comments that greatly improved the manuscript. REFERENCES Alatalo RV Kotiaho JS Mappes J Parri S . 1998 . Mate choice for offspring performance: major benefits or minor costs? Proc Biol Sci . 265 : 2297 – 2301 . Google Scholar Crossref Search ADS WorldCat Aragaki DlR Meffert LM . 1998 . A test of how well the repeatability of courtship predicts its heritability . Anim Behav . 55 : 1141 – 1150 . Google Scholar Crossref Search ADS PubMed WorldCat Barth FG . 1982 . The vibrational sense of spiders . In: Hoy RR Popper AN Fay RR , editors. Comparative hearing: insects . 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TI - Extreme short-term repeatability of male courtship performance in a tropical orb-web spider
JF - Behavioral Ecology
DO - 10.1093/beheco/aru083
DA - 2014-09-01
UR - https://www.deepdyve.com/lp/oxford-university-press/extreme-short-term-repeatability-of-male-courtship-performance-in-a-G0qL2qaL0T
SP - 1083
EP - 1088
VL - 25
IS - 5
DP - DeepDyve
ER -