Polistes metricus queens exhibit personality variation and behavioral syndromes

Polistes metricus queens exhibit personality variation and behavioral syndromes Consistent differences in behavior between individuals, otherwise known as animal personalities, have become a staple in behavioral ecology due to their ability to explain a wide range of phenom- ena. Social organisms are especially serviceable to animal personality techniques because they can be used to explore behavioral variation at both the individual and group level. Despite the suc- cess of personality research in social organisms generally, and social Hymenoptera in particular, social wasps (Vespidae) have received little to no attention in the personality literature. In the pre- sent study, we test Polistes metricus (Vespidae; Polistinae) paper wasp queens for the presence of repeatable variation in, and correlations (“behavioral syndromes”) between, several commonly used personality metrics: boldness, aggressiveness, exploration, and activity. Our results indicate that P. metricus queens exhibit personalities for all measured traits and correlations between differ- ent behavioral measures. Given that paper wasps have served as a model organism for a wide range of phenomena such as kin selection, dominance hierarchies, mate choice, facial recognition, social parasitism, and chemical recognition, we hope that our results will motivate researchers to explore whether, or to what degree, queen personality is important in their research programs. Key words: behavioral syndromes, personality, social insects, temperament, wasps. Any casual observer of animal behavior can attest that no 2 animals (Johnson and Sih 2005; Pruitt and Riechert 2009). Additional stud- behave precisely the same way. Behavioral differences within a spe- ies have shown that individual personality is often linked with key cies that persist across either time or context are known as animal life-history parameters (Wolf et al. 1999, 2007; Pruitt and Riechert personalities, and behavioral syndromes occur when 2 or more per- 2012; Wolf and Weissing 2012; Juette et al. 2014; Modlmeier et al. sonality traits appear linked (Sih et al. 2004; Dingemanse and Reale 2015; Canestrelli et al. 2016), further indicating the importance of 2005). For a long time, scientists had written off personality vari- personality in driving a variety of ecological outcomes. ation within a species as constituting merely noise around an adap- Social or group-living organisms provide particularly interesting tive mean, and instead focused largely on behavioral differences case studies for the animal personality research paradigm (Jandt between species. However, the past several decades have given rise et al. 2013; Bengston and Jandt 2014). This is due to the fact that to numerous studies highlighting the importance and predictive one can quantify personality at multiple levels: the individuals power of animal personality research that it can no longer be within the group, and the emergent behavior of the entire group it- ignored. The study of personality is alluring because many personal- self relative to other such groups. Social organisms exhibiting per- ity traits are important in accounting for seemingly maladaptive be- sonality variation span an ever-widening range of taxa such as birds havior within a population, such as superfluous prey killing (Schoepf and Schradin 2012; Aplin et al. 2013, 2014), fishes (Dyer (Maupin and Riechert 2001) and precopulatory cannibalism et al. 2009; Magnhagen 2012; Rasmussen and Belk 2012), mice V C The Author (2017). Published by Oxford University Press. 45 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/article-abstract/64/1/45/3063806 by Ed 'DeepDyve' Gillespie user on 16 March 2018 46 Current Zoology, 2018, Vol. 64, No. 1 (Schoepf and Schradin 2012), and various arthropod species Pennsylvania in the United States: the University of Pittsburgh’s 0 00 (Modlmeier et al. 2012; Holbrook et al. 2014; Shearer and Pruitt Pymatuning Laboratory of Ecology (PY; 41 37 22.80 N, 0 00 2014; Wright et al. 2015, 2016). The social Hymenoptera—ants, 80 27 16.62 W) and the Powdermill Nature Reserve (PM; 0 00  0 00 bees, and wasps—have been of great interest to early ethologists as 40 9 36.98 N, 79 16 17.30 W). The queens (n ¼ 59) were taken well as modern behavioral ecologists due to their stunning efficiency from their recently founded nests and transported back to the la- and complex division of labor along morphological and behavioral boratory at the University of Pittsburgh where we measured head castes (Oster and Wilson 1978). Our understanding of these insect width and wing length, both of which are highly correlated with societies has increased substantially under animal personality re- body size and mass (Eickwort 1969). The queens were given new search (Jandt et al. 2013) and, conversely, these taxa have been in- combs from the same site. Giving the queens new nests is somewhat of an artificial condition, but was required because the queens did strumental in their ability to test general personality theory not successfully build their own nests from scratch in the laboratory. (Bengston and Dornhaus 2014). For instance, in honeybees, colonies However, P. metricus queens commonly adopt new foreign or previ- exhibit strong differences in defensive, foraging, and undertaking ously used nests in the wild. Therefore, our results should be viewed behavior that also predict colony productivity and winter survival (Wray et al. 2011). In Temnothorax ants, colonies that harbored in the context of this limitation. Before queens were introduced to more intracolony variation in brood care and exploration were their new nests, we removed the eggs, and the queens and nests were more productive (Modlmeier et al. 2012). Taken together, consider- placed in a 30  30  30 cm nest box with an aluminum frame and ing intraspecific variation at both the individual and group level ap- chiffon siding on all walls, save for the front, which is covered with pears to enhance the predictability of a variety of behavioral and clear plastic for easy observations. This material allows light to per- ecological phenomena in social insects. meate throughout the entire container. Wasps were fed an ad lib- Despite the fervor surrounding personality research in social or- itum diet of greater wax moth larvae Galleria mellonella and sugar ganisms, personality studies in social wasps (Vespidae) remain con- cubes, and were given fresh water every week. The wasps were kept spicuously absent from the literature. We believe this is an oversight, on a 16:8 h light:dark cycle using incandescent halogen bulbs (Inger as social wasps have served as model organisms for the study of et al. 2014), and the temperature was maintained at approximately dominance hierarchies and social interactions (Pardi 1948; 25 C. All behavioral assays (boldness, aggressiveness, and explor- Turillazzi and Pardi 1977; Strassmann 1981; Cervo et al. 2008b; ation/activity) were performed under incandescent lighting between Zanette and Field 2009; Jandt et al. 2014), facial recognition 10 AM and 3 PM. Each behavioral assay trial, except for the first (Tibbetts 2002; Tibbetts and Lindsay 2008; Sheehan and Tibbetts boldness assay (approaching a rival), was performed one at a time 2010; Green et al. 2013; Cervo et al. 2015), kin selection and repro- over 4 consecutive days, with 1 trial per day. Therefore, each trial was performed 24 h apart, and no assays overlapped with another. ductive skew (Field et al. 1998, 2006; Gamboa 2004; Liebert and The first boldness assay was performed once every 72 h, as it took Starks 2006), social parasitism (Sledge et al. 2001; Cervo 2006; some time to collect new “rival” dummy wasps. Exploration/activity Cervo et al. 2008a), mate choice (Izzo and Tibbetts 2012; Beani assays were performed first, followed by boldness assays (approach- et al. 2014), and even chemical recognition (Dani 2006; Dapporto ing a rival), and then on-nest boldness and aggressiveness assays. et al. 2007; van Zweden and d’Ettorre 2010). Many if not all of The wasps were tested in random order for each trial. Wasps were these lines of research may be heavily influenced by, and could, given 24 h to acclimate to the laboratory prior to all trials, and all therefore, benefit from, incorporating an animal personality frame- experiments, from beginning to end, took a total of 21 days to work. Additionally, Vespid wasps evolved eusociality independently perform. from bees and ants (Johnson et al. 2013), and comparative studies The short time frame was chosen because we wanted to properly on personality variation may, therefore, spark novel insight into dis- assess queen personality early in the founding phase when all nests cussions surrounding the evolution of eusociality. are nearly equal in size and contain mostly eggs. Given that paper Polistes metricus (Vespidae; Polistinae) is a paper wasp native to wasp queens tend to become more aggressive as nests approach the North America, and can be found in the central and eastern United worker emergence phase, we wanted to take an early snapshot of States as well as Southern Canada. Unlike most paper wasp species queen personality before other factors such as nest contents have an that begin nests with multiple foundresses, P. metricus predomin- opportunity to significantly influence their behavior. antly founds nests solitarily (Bohm and Stockhammer 1977), and thus undergoes a transition from solitary to social living during its lifetime unlike many other paper wasps that are social throughout Exploration/activity assay their lives. Additionally, this species has been known to reutilize old To measure individual exploration and activity levels, single queens nests from the previous season (Starr 1976), as well as sharing and (n ¼ 52) were placed into a small plastic cylinder that was then maintaining multiple active nests (Gamboa 1981), sometimes even placed over the opening of a 29  16  4 cm exploration arena. This with other Polistes species. In the present study, we test for the pres- arena contains 10 compartments that the wasp can enter without ence of personality variation and behavioral syndromes in P. metri- hindrance (Figure 1). We allowed the wasps to enter an opening cus paper wasp queens using several commonly used personality located at the center of the exploration chamber. Once the wasp metrics: boldness, aggressiveness, exploration, and activity. These entered the arena, we started a timer and we allowed the wasp 10 personality metrics have proved useful for a wide variety of systems, min to freely explore the arena. While in the arena, we recorded the and it is our hope that this study may serve as a basis for future per- number of novel chambers entered (as a measure of exploration) sonality studies in social wasps. and the proportion of time the wasp remained active (activity). We define activity as walking or flying. These assays were performed 4 times on each queen, and the values from each trial were averaged Materials and Methods for our final measure of both exploration and activity. The arena All experimental P. metricus foundresses were collected on the same was cleaned with 70% ethanol and dried after every trial, and fumes day in the early Spring in May 2014 from 2 sites in Western were allowed to dissipate for 2 min between each trial. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/45/3063806 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Wright et al.  Personality variation and behavioral syndromes in Polistes metricus 47 especially because so many were used during the “approach a rival” boldness test. Boldness was calculated as the number of “attacks” required before the wasp fled her nest (Boldness II). Each attack con- sisted of prodding the wasp anteriorly with the brush and holding the brush in place for 2 s before removing it. Once removed, we waited an additional 2 s before initiating another prod. Queens that held their ground after frequent prods were considered bolder, and queens that readily abandoned their nests were considered shyer. Boldness was, therefore, scored on a 1–10 scale for each individual trial corresponding to the number of prods necessary before nest abandonment, which was then averaged over 4 trials. It should be noted that this assay might also be consistent with the proactive–re- active behavioral trait, and not boldness per se. Correlations with Figure 1. A 10-chambered exploration arena for wasps. Dimensions: this trait and between others such as exploration and activity would LWH ¼ 29  16  4 cm. potentially lend more support for the proactive–reactive interpret- ation. The brush was wiped down with a 70% ethanol-soaked paper Boldness assays towel and air-dried between each trial to remove any residual chem- Boldness—the propensity to engage in risky behavior—was assessed ical cues from previous trials. using 2 independent behavioral assays. The first boldness assay measured the latency for an individual queen to approach and feed Aggressiveness assay in the presence of a rival (Boldness I). Queens were starved for 48 h Aggressiveness was measured concurrently with the second boldness and then placed in a small circular arena (diameter ¼ 12 cm, assay (“prodding”). During each prod, it was noted whether or not height ¼ 4 cm) with a dead, previously frozen P. metricus “dummy” the queens responded aggressively toward the brush. Aggressive re- foundress mounted on a 1-cm sugar cube, forcing the hungry queen sponses included active biting and stinging. Aggressiveness was cal- to interact with the dummy or “rival” to feed. Dummy wasps were culated during each trial as the proportion of prods to which the taken from a population>150 km from the focal wasps to ensure queen responded aggressively. This proportion was averaged over 4 they were unrelated and never interacted previously. Dummy wasps trials to arrive at our summative measure of an individuals’ were frozen  24 h prior to all trials. Boldness was measured as the aggressiveness. latency to begin feeding after the first antennation of this “guarded” resource. It is important to note that clypeal or “face” pattern vari- Statistical methods ation is minimal or nonexistant in P. metricus, and seemingly does We tested for the repeatability across trials of individual queen per- not play a role in individual recognition or dominance such as in P. sonality using generalized linear mixed model (GLMM) (Poisson dominula and P. fuscatus (Sheehan and Tibbetts 2010, 2011), and distribution and log-link function) with head size as a fixed effect, so was not considered here. Antennation is defined as physically in- individual wasp ID nested within site ID, and dummy wasp ID (for specting, via direct contact with the antennae, the food source Boldness I test) as random effects, and starting nest size, egg num- guarded by the wasp dummy. Wasps that fed more quickly were bers, and trial number as fixed effects. Our predictor variables were considered bolder, and longer latencies were associated with shyer the latency to feed (Boldness I), the number of prods before fleeing individuals. Trials were terminated after 5 min. Dummy wasps were (Boldness II), proportion of observed aggressive encounters, explor- used on no more than 5 focal wasps before they were discarded to ation, and activity time. The proportion of total variation attribut- ensure a fresh hydrocarbon profile. Dummy wasps were assigned able to between individual differences provides an estimation of randomly and included as a random variable in our models. Dummy repeatability (Boake 1989; Falconer and Mackay 1996), which is a wasps did not vary greatly in size (wing length: mean ¼ 15.01, measure of how consistent individuals are in their behavior over r ¼ 0.85; head width: mean ¼ 3.94, r ¼ 0.30). We performed this multiple trials. Repeatability estimates and 95% CI were estimated boldness assay on each queen once every 72 h for a total of 4 trials. using maximum likelihood, and the significance of the repeatability Final boldness scores were calculated by averaging the boldness estimates was retained regardless of the error distribution modeled. scores from each of the 4 trials. Correlations between boldness, aggressiveness, activity, and explor- The second boldness assay was performed while queens were ation were analyzed using Spearman rank correlation tests using the perched on their nests. Only queens on nests containing only eggs average of each individual’s response for each behavioral metric. All (i.e., no larvae yet) were tested to control for behavioral variation statistics were performed using JMP version 10 (SAS Institute, Cary, (specifically boldness or aggressiveness) that may be associated with NC). having higher valued assets to defend (Clark 1994). For this assay, queens were prodded anteriorly to the clypeus with a small plastic brush up to 10 times, simulating molestation from a foreign rival or Results predator. A prod test was chosen as our prod represents a general antagonistic stimulus that is standardized for all queens. The use of Repeatability of behavior All behaviors tested showed high repeatability, indicating the pres- dummies was avoided because we would have to take into account ence of between-individual differences in behavior. Boldness, meas- many attributes of the dummy such as size and head width. ured as the latency to feed in a threatening environment (from a Additionally, the dummy’s hydrocarbon profile may erode or be contaminated with other chemicals from the focal wasp. This would sugar cube guarded by a dead queen), was highly repeatable require changing out the wasp dummy after several trials, and it is [r ¼ 0.93; n ¼ 53, 95% CI (0.62, 1.56)]. Similarly, boldness meas- difficult to acquire such a large number of dummies for this purpose, ured as the number of aggressive encounters before nest Downloaded from https://academic.oup.com/cz/article-abstract/64/1/45/3063806 by Ed 'DeepDyve' Gillespie user on 16 March 2018 48 Current Zoology, 2018, Vol. 64, No. 1 Figure 2. Relationship between both boldness assays: the number of encoun- ters before retreat (Boldness I), and latency to approach a rival (Boldness II) shows that both are significantly correlated, providing mutual corroboration that both boldness assays are measuring the same personality trait. Note that Boldness II latency scores have been subtracted from the maximum value to make higher values correspond to higher boldness. abandonment was also highly repeatable [r ¼ 0.81; n ¼ 38, 95% CI (0.49, 1.59)]. Most importantly, these boldness assays corroborate each other, because the wasps that fed without hesitation from a Figure 3. The behavioral syndrome between aggressiveness and (A) the guarded food source were also those that were less likely to abandon number of simulated attacks before retreat (Boldness I), and (B) the latency to their nests after repeated aversive stimuli (q¼0.23, P ¼ 0.0044) approach a rival (Boldness II). Note that Boldness II latency scores have been (Figure 2). Aggressiveness, measured as the proportion of predator subtracted from the maximum value to make higher values correspond to encounters (brush prods) the wasps acted aggressive toward (i.e., bit higher boldness. and stung the poker), was also highly repeatable [r ¼ 0.88; n ¼ 38, 95% CI (0.53, 1.75)]. Lastly, exploration and activity level showed State-dependent personality similarly high repeatability [exploration: r ¼ 0.88; n ¼ 52, 95% CI Wasp size (using head width as a proxy) was only significantly cor- (0.66, 1.66); activity: r ¼ 0.92; n ¼ 52, 95% CI (0.61, 1.56)]. related with activity and exploration, where larger wasps on average were less active and less explorative than smaller wasps (activity: F 1, ¼ 12.1, P ¼ 0.0011; exploration: F ¼ 5.18, P ¼ 0.027). Wasp 52 1, 52 Behavioral syndromes size was not correlated with boldness (latency to approach rival: We tested for correlations across all repeatable behaviors using non- n ¼ 52, P ¼ 0.65; encounters before retreat: n ¼ 38, P ¼ 0.21), or parametric Spearman rank correlation, and Bonferroni correction aggressiveness (n ¼ 38, P ¼ 0.32). Additionally, behavioral differ- for multiple comparisons (modified a ¼ 0.0055) and found that ences between queens were not correlated with the size of the nest aggressiveness and at least one of our 2 boldness measures (encoun- the queens adopted in the laboratory (latency to approach rival: ters before retreat) were correlated (latency to approach rival vs. n ¼ 52, P ¼ 0.98; encounters before retreat: n ¼ 38, P ¼ 0.62; aggres- aggressiveness: n ¼ 38, q ¼ 0.37, P ¼ 0.02; encounters before retreat siveness: n ¼ 38, P ¼ 0.72; exploration: n ¼ 52, P ¼ 0.56; activity: vs. aggressiveness: n ¼ 38, q ¼ 0.89, P< 0.0001) (Figure 3). This n ¼ 52, P ¼ 0.62). provides evidence for a behavioral syndrome between aggressiveness and at least 1 measure of boldness in P. metricus. However, we can- not rule out the possibility that Boldness II and aggressiveness lack Discussion independence, given that the assays were performed simultaneously. This study is the first to demonstrate that paper wasp queens (or Lastly, there existed a strong positive relationship between ex- wasps in general) exhibit consistent differences in behavior across ploration and activity time (q ¼ 0.93, P< 0.0001), though we are time and context (personality), and correlated personality metrics hesitant to call this a behavioural syndrome, as these measures are (behavioral syndrome). It must be noted, however, that behavioral likely not independent—wasps that are more active will, by random syndromes were only found between traits that were measured in chance alone, enter into more novel chambers than less-active the same trial, and thus future experiments using independent trials wasps. No syndromes were found between any other behavioral should be performed to verify whether the syndromes discovered in traits (aggressivness vs. activity: q ¼ 0.0035, P ¼ 0.98; aggressiveness our study hold. Additionally, future studies should be careful to re- vs. exploration: q ¼ 0.046, P ¼ 0.77; activity vs. Boldness I: move any traces of apolar compounds left in the arenas that, in this q ¼ 0.049, P ¼ 0.71; activity vs. Boldness II: q ¼ 0.12, P ¼ 0.45; ex- study, may have remained due to the use of a polar solvent. The ploration vs. Boldness I: q ¼ 0.086, P ¼ 0.52; exploration vs. presence of behavioral differences in Polistes wasps found in our Boldness II: q ¼ 0.097, P ¼ 0.54). study has many potentially important and interesting implications Downloaded from https://academic.oup.com/cz/article-abstract/64/1/45/3063806 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Wright et al.  Personality variation and behavioral syndromes in Polistes metricus 49 for their life history and fitness. Though P. metricus generally founds 2014). Given that paper wasps are only primitively eusocial, mean- nests solitarily, they do also form foundress associations on occa- ing that the reproductive division of labor is less discrete than in sion. Thus, it remains to be determined whether this personality more “advanced” eusocial taxa such as ants and honeybees (Wilson variation correlates with the tendency to form foundress associ- and Holldobler 2005), personality studies in paper wasps and other ations, the likelihood of becoming the dominant foundress (the Vespidae may prove particularly enlightening in these discussions. queen) in an association, the likelihood of being usurped by conspe- For instance, one may explore the extent to which individual differ- cifics, susceptibility to nest parasitism, and overall colony productiv- ences are associated with task participation, efficiency at various ity. Additionally, it may be intriguing to find out whether queen tasks, and propensity to switch tasks. At the colony level, examining personality is related to the differences between queens, foundresses, within-group behavioral composition may help us to predict inter- and workers in how much comb space they occupy as well as how colony differences in collective aggressiveness (Hui and Pinter- they distribute themselves spatially on the comb (Baracchi et al. Wollman 2014; Modlmeier et al. 2014a), brood care (Jandt et al. 2010). Each of these topics have been rigorously examined using 2013), or life-history attributes. By conducting such studies in paral- various Polistes models, however, we feel that the application of a lel across species with varying degrees of sociality (or eusociality), personality approach has the potential to integrate these topics into we may be able to retrace the role of individual behavioral differ- a shared explanatory framework. ences as precursors to morphologically based task differentiation. Polistes wasps have served as prominent model organisms for Indeed, such behavioral precursors have already been discovered in the study of dominance hierarchies and social interactions (Jandt ants (Dornhaus 2008; Pinter-Wollman et al. 2012; Lichtenstein et al. 2014). Many of these studies have focused on how intracolony et al. 2016) and even social spiders (Wright et al. 2014, 2016). aggression mediates dominant–subordinate, foundress–worker, and Our study also hints at the possibility for a more reductionist ap- worker–worker interactions (Eberhard 1969; Strassmann and proach regarding the mechanisms that lead to and help maintain in- Meyer 1983; Miyano 1986), yet do not focus on inherent differences ter- and intra-colony behavioral variation. Most studies have been in aggressiveness between wasps outside of a social context. A thor- content with explaining differences in behavior between colonies as ough examination of the prevalence of behavioral variation among resulting from intra-colony differences in behavior. Several mechan- queens, foundresses, and workers in Polistes and other Vespinae pre- isms have been proposed to explain inter-colony behavioral differ- sents researchers with an interesting opportunity to delve deeper ences, such as differences in the total average behavior of workers, into the role of intrinsic individual differences in mediating complex differences in the behavioral distribution of worker behavior, differ- social outcomes. Exploring behavioral variation among other social ences in behavioral response thresholds, or purely resulting from ex- arthropods have proved to be highly insightful, for example, ants ternal environmental factors (Bonabeau et al. 1996, 1998; (Modlmeier and Foitzik 2011; Hui and Pinter-Wollman 2014; Theraulaz et al. 1998; Pinter-Wollman 2012). Furthermore, the so- Modlmeier et al. 2014b), bees (Wray et al. 2011), water striders (Sih cial group, as opposed to the individual worker, is often regarded as and Watters 2005; Chang and Sih 2013), social spiders (Pruitt and being the object of selection in many social systems (Holldobler and Riechert 2011; Pruitt and Goodnight 2014; Wright et al. 2014). Wilson 1990; Mayr 1997; Korb and Heinze 2004). We suggest that Moreover, aggressive/bold syndromes, such as the one observed in in some systems, such as ours, where colony life histories are typified P. metricus here, have been identified in many nonsocial species by discrete solitary and social stages, the queen herself could be re- (Bell 2007), and are often associated with increased dispersal abil- garded as the object of selection, as her success during the founding ities (Clobert et al. 2009), different foraging strategies (Bell and Sih stage is necessary for there to even be a colony in the first place. And 2007; Chapman et al. 2011), vigilant anti-predator behavior her behavior may play a role in determining the behavioral compos- (Huntingford 1976), and even grouping behavior (Aplin et al. ition of her future colony. Once the social group exists, however, 2013). Given that Polistes wasps participate in all these behaviors to the object of selection may then be transferred to the social group as a great degree, further investigations in this system on how this syn- a whole. We feel it is an oversight to ignore the queen’s behavior drome and other personality traits influence life history and survival during the founding stage—the most vulnerable period of the col- should be rewarding. Notably, Polistes might be among the most ony’s life cycle—when considering the underlying mechanisms of promising future models for these lines of research, because the re- both inter- and intra-colony behavioral variation. peatability of individual differences in P. metricus (r ¼ 0.81–0.93) To conclude, we have documented a clear signature of personal- are among the very highest observed for any trait or any taxa meas- ity in P. metricus queens, including common traits such as aggres- ured in either in the lab or field (Bell et al. 2009), though personality siveness, boldness, exploration, and activity level. This species also traits were measured over a very short-time span in our study that exhibits a behavioral syndrome that bears resemblance to those may have inflated our repeatability estimates. Thus, there is compel- found in a variety of other social and solitary vertebrates ling evidence that queens exhibit substantial characteristic differ- (Huntingford 1976; Bell 2005; Dingemanse et al. 2007; ences in their behavioral tendencies, and that these individual Dochtermann and Jenkins 2007; Moretz et al. 2007) and inverte- differences may have consequences on a variety of behavioral and brates (Riechert and Hedrick 1993; Johnson and Sih 2005; Kortet ecological outcomes. and Hedrick 2007; Reaney and Backwell 2007). The short time Additionally, given that evidence suggests that paper wasps (and frame over which the queens were measured, however, means that other social Vespidae) evolved eusociality (or primitive eusociality) we cannot state with certainty that the personality differences independently from other eusocial Hymenoptera and Isoptera observed in our study are maintained throughout the queens’ tenure (Johnson et al. 2013), we feel that comparative personality studies on the nest. Both of these features bode well for Polistes’ promise as between these taxa could help contribute to the conversation sur- a generalizable model for behavioral syndrome research. This poten- rounding the evolution of eusociality and insect castes. Recent dis- tial is further augmented by the diversity of social structures ex- coveries in social spiders regarding the presence of “personality castes” suggest that behavioral variation could be an initial step on hibited within the Vespidae and the reservoir of seminal behavioral the path to complete reproductive division of labor (Wright et al. research that has already been conducted using these systems. Thus, Downloaded from https://academic.oup.com/cz/article-abstract/64/1/45/3063806 by Ed 'DeepDyve' Gillespie user on 16 March 2018 50 Current Zoology, 2018, Vol. 64, No. 1 Table 1. A summary table of repeatability values and a correlation matrix for each trait tested Correlations [P values and (Spearman’s q)] Trait Repeatability (r) Boldness I Boldness II Aggressiveness Exploration Boldness I 0.93 — — — — Boldness II 0.81 — — — — Aggressiveness 0.88 0.021 (0.37) <0.0001 (0.89) —— Exploration 0.88 0.52 (0.086) 0.54 (0.097) 0.77 (0.046) — Activity 0.92 0.71 (0.049) 0.45 (0.12) 0.98 (0.0035) <0.0001 (0.93) Notes: The first numbers in the matrix are the P values, and Spearman’s rho (q) is to the right in parentheses. Significant P-values are in bold. we encourage wasp researchers to further explore the potential im- Bonabeau E, Theraulaz G, Deneubourg JL, 1996. Quantitative study of the fixed threshold model for the regulation of division of labour in insect soci- portance of personality in their own research questions. eties. Proc R Soc B 263:1565–1569. Bonabeau E, Theraulaz G, Deneubourg JL, 1998. Fixed response thresholds and the regulation of division of labor in insect societies. Bull Math Biol Acknowledgments 60:753–807. We would like to acknowledge the many undergraduate researchers who Canestrelli D, Bisconti R, Carere C, 2016. Bolder takes all? The behavioral di- helped to keep the wasps fed and watered, as well as Kayla Hale for her assist- mension of biogeography. Trends Ecol Evol 31:35–43. ance in the lab. Additionally, we thank the Carson lab for their helpful com- Cervo R, 2006. Polistes wasps and their social parasites: an overview. Ann ments and criticisms on previous drafts of this manuscript, and Christine Rice Zool Fennici 43:531–549. for her commitment to twerking in the field, rain or shine. Cervo R, Cini A, Turillazzi S, 2015. Visual recognition in social wasps. In: Aquiloni L, Tricarico E, editors. Social Recognition in Invertebrates. Switzerland: Springer International Publishing, 125–145. Funding Cervo R, Dani FR, Cotoneschi C, Scala C, Lotti I et al., 2008a. Why are larvae of the social parasite wasp polistes sulcifer not removed from the host nest? This work was supported by an National Science Foundation Animal Behav Ecol Sociobiol 62:1319–1331. Behavior grant to J.N.P. (IOS 1352705 and 1455895), as well as G. Murray Cervo R, Dapporto L, Beani L, Strassmann JE, Turillazzi S, 2008b. On status McKinley Research Fund and the Arthur and Barbara Pape Endowment badges and quality signals in the paper wasp polistes dominulus: body size, Award research grants provided through the University of Pittsburgh’s facial colour patterns and hierarchical rank. Proc R Soc B 275:1189–1196. Pymatuning Laboratory of Ecology. Chang AT, Sih A, 2013. Multilevel selection and effects of keystone hyperag- gressive males on mating success and behavior in stream water striders. Behav Ecol 24:1166–1176. References Chapman BB, Thain H, Coughlin J, Hughes WHO, 2011. 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Polistes metricus queens exhibit personality variation and behavioral syndromes

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Abstract

Consistent differences in behavior between individuals, otherwise known as animal personalities, have become a staple in behavioral ecology due to their ability to explain a wide range of phenom- ena. Social organisms are especially serviceable to animal personality techniques because they can be used to explore behavioral variation at both the individual and group level. Despite the suc- cess of personality research in social organisms generally, and social Hymenoptera in particular, social wasps (Vespidae) have received little to no attention in the personality literature. In the pre- sent study, we test Polistes metricus (Vespidae; Polistinae) paper wasp queens for the presence of repeatable variation in, and correlations (“behavioral syndromes”) between, several commonly used personality metrics: boldness, aggressiveness, exploration, and activity. Our results indicate that P. metricus queens exhibit personalities for all measured traits and correlations between differ- ent behavioral measures. Given that paper wasps have served as a model organism for a wide range of phenomena such as kin selection, dominance hierarchies, mate choice, facial recognition, social parasitism, and chemical recognition, we hope that our results will motivate researchers to explore whether, or to what degree, queen personality is important in their research programs. Key words: behavioral syndromes, personality, social insects, temperament, wasps. Any casual observer of animal behavior can attest that no 2 animals (Johnson and Sih 2005; Pruitt and Riechert 2009). Additional stud- behave precisely the same way. Behavioral differences within a spe- ies have shown that individual personality is often linked with key cies that persist across either time or context are known as animal life-history parameters (Wolf et al. 1999, 2007; Pruitt and Riechert personalities, and behavioral syndromes occur when 2 or more per- 2012; Wolf and Weissing 2012; Juette et al. 2014; Modlmeier et al. sonality traits appear linked (Sih et al. 2004; Dingemanse and Reale 2015; Canestrelli et al. 2016), further indicating the importance of 2005). For a long time, scientists had written off personality vari- personality in driving a variety of ecological outcomes. ation within a species as constituting merely noise around an adap- Social or group-living organisms provide particularly interesting tive mean, and instead focused largely on behavioral differences case studies for the animal personality research paradigm (Jandt between species. However, the past several decades have given rise et al. 2013; Bengston and Jandt 2014). This is due to the fact that to numerous studies highlighting the importance and predictive one can quantify personality at multiple levels: the individuals power of animal personality research that it can no longer be within the group, and the emergent behavior of the entire group it- ignored. The study of personality is alluring because many personal- self relative to other such groups. Social organisms exhibiting per- ity traits are important in accounting for seemingly maladaptive be- sonality variation span an ever-widening range of taxa such as birds havior within a population, such as superfluous prey killing (Schoepf and Schradin 2012; Aplin et al. 2013, 2014), fishes (Dyer (Maupin and Riechert 2001) and precopulatory cannibalism et al. 2009; Magnhagen 2012; Rasmussen and Belk 2012), mice V C The Author (2017). Published by Oxford University Press. 45 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/article-abstract/64/1/45/3063806 by Ed 'DeepDyve' Gillespie user on 16 March 2018 46 Current Zoology, 2018, Vol. 64, No. 1 (Schoepf and Schradin 2012), and various arthropod species Pennsylvania in the United States: the University of Pittsburgh’s 0 00 (Modlmeier et al. 2012; Holbrook et al. 2014; Shearer and Pruitt Pymatuning Laboratory of Ecology (PY; 41 37 22.80 N, 0 00 2014; Wright et al. 2015, 2016). The social Hymenoptera—ants, 80 27 16.62 W) and the Powdermill Nature Reserve (PM; 0 00  0 00 bees, and wasps—have been of great interest to early ethologists as 40 9 36.98 N, 79 16 17.30 W). The queens (n ¼ 59) were taken well as modern behavioral ecologists due to their stunning efficiency from their recently founded nests and transported back to the la- and complex division of labor along morphological and behavioral boratory at the University of Pittsburgh where we measured head castes (Oster and Wilson 1978). Our understanding of these insect width and wing length, both of which are highly correlated with societies has increased substantially under animal personality re- body size and mass (Eickwort 1969). The queens were given new search (Jandt et al. 2013) and, conversely, these taxa have been in- combs from the same site. Giving the queens new nests is somewhat of an artificial condition, but was required because the queens did strumental in their ability to test general personality theory not successfully build their own nests from scratch in the laboratory. (Bengston and Dornhaus 2014). For instance, in honeybees, colonies However, P. metricus queens commonly adopt new foreign or previ- exhibit strong differences in defensive, foraging, and undertaking ously used nests in the wild. Therefore, our results should be viewed behavior that also predict colony productivity and winter survival (Wray et al. 2011). In Temnothorax ants, colonies that harbored in the context of this limitation. Before queens were introduced to more intracolony variation in brood care and exploration were their new nests, we removed the eggs, and the queens and nests were more productive (Modlmeier et al. 2012). Taken together, consider- placed in a 30  30  30 cm nest box with an aluminum frame and ing intraspecific variation at both the individual and group level ap- chiffon siding on all walls, save for the front, which is covered with pears to enhance the predictability of a variety of behavioral and clear plastic for easy observations. This material allows light to per- ecological phenomena in social insects. meate throughout the entire container. Wasps were fed an ad lib- Despite the fervor surrounding personality research in social or- itum diet of greater wax moth larvae Galleria mellonella and sugar ganisms, personality studies in social wasps (Vespidae) remain con- cubes, and were given fresh water every week. The wasps were kept spicuously absent from the literature. We believe this is an oversight, on a 16:8 h light:dark cycle using incandescent halogen bulbs (Inger as social wasps have served as model organisms for the study of et al. 2014), and the temperature was maintained at approximately dominance hierarchies and social interactions (Pardi 1948; 25 C. All behavioral assays (boldness, aggressiveness, and explor- Turillazzi and Pardi 1977; Strassmann 1981; Cervo et al. 2008b; ation/activity) were performed under incandescent lighting between Zanette and Field 2009; Jandt et al. 2014), facial recognition 10 AM and 3 PM. Each behavioral assay trial, except for the first (Tibbetts 2002; Tibbetts and Lindsay 2008; Sheehan and Tibbetts boldness assay (approaching a rival), was performed one at a time 2010; Green et al. 2013; Cervo et al. 2015), kin selection and repro- over 4 consecutive days, with 1 trial per day. Therefore, each trial was performed 24 h apart, and no assays overlapped with another. ductive skew (Field et al. 1998, 2006; Gamboa 2004; Liebert and The first boldness assay was performed once every 72 h, as it took Starks 2006), social parasitism (Sledge et al. 2001; Cervo 2006; some time to collect new “rival” dummy wasps. Exploration/activity Cervo et al. 2008a), mate choice (Izzo and Tibbetts 2012; Beani assays were performed first, followed by boldness assays (approach- et al. 2014), and even chemical recognition (Dani 2006; Dapporto ing a rival), and then on-nest boldness and aggressiveness assays. et al. 2007; van Zweden and d’Ettorre 2010). Many if not all of The wasps were tested in random order for each trial. Wasps were these lines of research may be heavily influenced by, and could, given 24 h to acclimate to the laboratory prior to all trials, and all therefore, benefit from, incorporating an animal personality frame- experiments, from beginning to end, took a total of 21 days to work. Additionally, Vespid wasps evolved eusociality independently perform. from bees and ants (Johnson et al. 2013), and comparative studies The short time frame was chosen because we wanted to properly on personality variation may, therefore, spark novel insight into dis- assess queen personality early in the founding phase when all nests cussions surrounding the evolution of eusociality. are nearly equal in size and contain mostly eggs. Given that paper Polistes metricus (Vespidae; Polistinae) is a paper wasp native to wasp queens tend to become more aggressive as nests approach the North America, and can be found in the central and eastern United worker emergence phase, we wanted to take an early snapshot of States as well as Southern Canada. Unlike most paper wasp species queen personality before other factors such as nest contents have an that begin nests with multiple foundresses, P. metricus predomin- opportunity to significantly influence their behavior. antly founds nests solitarily (Bohm and Stockhammer 1977), and thus undergoes a transition from solitary to social living during its lifetime unlike many other paper wasps that are social throughout Exploration/activity assay their lives. Additionally, this species has been known to reutilize old To measure individual exploration and activity levels, single queens nests from the previous season (Starr 1976), as well as sharing and (n ¼ 52) were placed into a small plastic cylinder that was then maintaining multiple active nests (Gamboa 1981), sometimes even placed over the opening of a 29  16  4 cm exploration arena. This with other Polistes species. In the present study, we test for the pres- arena contains 10 compartments that the wasp can enter without ence of personality variation and behavioral syndromes in P. metri- hindrance (Figure 1). We allowed the wasps to enter an opening cus paper wasp queens using several commonly used personality located at the center of the exploration chamber. Once the wasp metrics: boldness, aggressiveness, exploration, and activity. These entered the arena, we started a timer and we allowed the wasp 10 personality metrics have proved useful for a wide variety of systems, min to freely explore the arena. While in the arena, we recorded the and it is our hope that this study may serve as a basis for future per- number of novel chambers entered (as a measure of exploration) sonality studies in social wasps. and the proportion of time the wasp remained active (activity). We define activity as walking or flying. These assays were performed 4 times on each queen, and the values from each trial were averaged Materials and Methods for our final measure of both exploration and activity. The arena All experimental P. metricus foundresses were collected on the same was cleaned with 70% ethanol and dried after every trial, and fumes day in the early Spring in May 2014 from 2 sites in Western were allowed to dissipate for 2 min between each trial. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/45/3063806 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Wright et al.  Personality variation and behavioral syndromes in Polistes metricus 47 especially because so many were used during the “approach a rival” boldness test. Boldness was calculated as the number of “attacks” required before the wasp fled her nest (Boldness II). Each attack con- sisted of prodding the wasp anteriorly with the brush and holding the brush in place for 2 s before removing it. Once removed, we waited an additional 2 s before initiating another prod. Queens that held their ground after frequent prods were considered bolder, and queens that readily abandoned their nests were considered shyer. Boldness was, therefore, scored on a 1–10 scale for each individual trial corresponding to the number of prods necessary before nest abandonment, which was then averaged over 4 trials. It should be noted that this assay might also be consistent with the proactive–re- active behavioral trait, and not boldness per se. Correlations with Figure 1. A 10-chambered exploration arena for wasps. Dimensions: this trait and between others such as exploration and activity would LWH ¼ 29  16  4 cm. potentially lend more support for the proactive–reactive interpret- ation. The brush was wiped down with a 70% ethanol-soaked paper Boldness assays towel and air-dried between each trial to remove any residual chem- Boldness—the propensity to engage in risky behavior—was assessed ical cues from previous trials. using 2 independent behavioral assays. The first boldness assay measured the latency for an individual queen to approach and feed Aggressiveness assay in the presence of a rival (Boldness I). Queens were starved for 48 h Aggressiveness was measured concurrently with the second boldness and then placed in a small circular arena (diameter ¼ 12 cm, assay (“prodding”). During each prod, it was noted whether or not height ¼ 4 cm) with a dead, previously frozen P. metricus “dummy” the queens responded aggressively toward the brush. Aggressive re- foundress mounted on a 1-cm sugar cube, forcing the hungry queen sponses included active biting and stinging. Aggressiveness was cal- to interact with the dummy or “rival” to feed. Dummy wasps were culated during each trial as the proportion of prods to which the taken from a population>150 km from the focal wasps to ensure queen responded aggressively. This proportion was averaged over 4 they were unrelated and never interacted previously. Dummy wasps trials to arrive at our summative measure of an individuals’ were frozen  24 h prior to all trials. Boldness was measured as the aggressiveness. latency to begin feeding after the first antennation of this “guarded” resource. It is important to note that clypeal or “face” pattern vari- Statistical methods ation is minimal or nonexistant in P. metricus, and seemingly does We tested for the repeatability across trials of individual queen per- not play a role in individual recognition or dominance such as in P. sonality using generalized linear mixed model (GLMM) (Poisson dominula and P. fuscatus (Sheehan and Tibbetts 2010, 2011), and distribution and log-link function) with head size as a fixed effect, so was not considered here. Antennation is defined as physically in- individual wasp ID nested within site ID, and dummy wasp ID (for specting, via direct contact with the antennae, the food source Boldness I test) as random effects, and starting nest size, egg num- guarded by the wasp dummy. Wasps that fed more quickly were bers, and trial number as fixed effects. Our predictor variables were considered bolder, and longer latencies were associated with shyer the latency to feed (Boldness I), the number of prods before fleeing individuals. Trials were terminated after 5 min. Dummy wasps were (Boldness II), proportion of observed aggressive encounters, explor- used on no more than 5 focal wasps before they were discarded to ation, and activity time. The proportion of total variation attribut- ensure a fresh hydrocarbon profile. Dummy wasps were assigned able to between individual differences provides an estimation of randomly and included as a random variable in our models. Dummy repeatability (Boake 1989; Falconer and Mackay 1996), which is a wasps did not vary greatly in size (wing length: mean ¼ 15.01, measure of how consistent individuals are in their behavior over r ¼ 0.85; head width: mean ¼ 3.94, r ¼ 0.30). We performed this multiple trials. Repeatability estimates and 95% CI were estimated boldness assay on each queen once every 72 h for a total of 4 trials. using maximum likelihood, and the significance of the repeatability Final boldness scores were calculated by averaging the boldness estimates was retained regardless of the error distribution modeled. scores from each of the 4 trials. Correlations between boldness, aggressiveness, activity, and explor- The second boldness assay was performed while queens were ation were analyzed using Spearman rank correlation tests using the perched on their nests. Only queens on nests containing only eggs average of each individual’s response for each behavioral metric. All (i.e., no larvae yet) were tested to control for behavioral variation statistics were performed using JMP version 10 (SAS Institute, Cary, (specifically boldness or aggressiveness) that may be associated with NC). having higher valued assets to defend (Clark 1994). For this assay, queens were prodded anteriorly to the clypeus with a small plastic brush up to 10 times, simulating molestation from a foreign rival or Results predator. A prod test was chosen as our prod represents a general antagonistic stimulus that is standardized for all queens. The use of Repeatability of behavior All behaviors tested showed high repeatability, indicating the pres- dummies was avoided because we would have to take into account ence of between-individual differences in behavior. Boldness, meas- many attributes of the dummy such as size and head width. ured as the latency to feed in a threatening environment (from a Additionally, the dummy’s hydrocarbon profile may erode or be contaminated with other chemicals from the focal wasp. This would sugar cube guarded by a dead queen), was highly repeatable require changing out the wasp dummy after several trials, and it is [r ¼ 0.93; n ¼ 53, 95% CI (0.62, 1.56)]. Similarly, boldness meas- difficult to acquire such a large number of dummies for this purpose, ured as the number of aggressive encounters before nest Downloaded from https://academic.oup.com/cz/article-abstract/64/1/45/3063806 by Ed 'DeepDyve' Gillespie user on 16 March 2018 48 Current Zoology, 2018, Vol. 64, No. 1 Figure 2. Relationship between both boldness assays: the number of encoun- ters before retreat (Boldness I), and latency to approach a rival (Boldness II) shows that both are significantly correlated, providing mutual corroboration that both boldness assays are measuring the same personality trait. Note that Boldness II latency scores have been subtracted from the maximum value to make higher values correspond to higher boldness. abandonment was also highly repeatable [r ¼ 0.81; n ¼ 38, 95% CI (0.49, 1.59)]. Most importantly, these boldness assays corroborate each other, because the wasps that fed without hesitation from a Figure 3. The behavioral syndrome between aggressiveness and (A) the guarded food source were also those that were less likely to abandon number of simulated attacks before retreat (Boldness I), and (B) the latency to their nests after repeated aversive stimuli (q¼0.23, P ¼ 0.0044) approach a rival (Boldness II). Note that Boldness II latency scores have been (Figure 2). Aggressiveness, measured as the proportion of predator subtracted from the maximum value to make higher values correspond to encounters (brush prods) the wasps acted aggressive toward (i.e., bit higher boldness. and stung the poker), was also highly repeatable [r ¼ 0.88; n ¼ 38, 95% CI (0.53, 1.75)]. Lastly, exploration and activity level showed State-dependent personality similarly high repeatability [exploration: r ¼ 0.88; n ¼ 52, 95% CI Wasp size (using head width as a proxy) was only significantly cor- (0.66, 1.66); activity: r ¼ 0.92; n ¼ 52, 95% CI (0.61, 1.56)]. related with activity and exploration, where larger wasps on average were less active and less explorative than smaller wasps (activity: F 1, ¼ 12.1, P ¼ 0.0011; exploration: F ¼ 5.18, P ¼ 0.027). Wasp 52 1, 52 Behavioral syndromes size was not correlated with boldness (latency to approach rival: We tested for correlations across all repeatable behaviors using non- n ¼ 52, P ¼ 0.65; encounters before retreat: n ¼ 38, P ¼ 0.21), or parametric Spearman rank correlation, and Bonferroni correction aggressiveness (n ¼ 38, P ¼ 0.32). Additionally, behavioral differ- for multiple comparisons (modified a ¼ 0.0055) and found that ences between queens were not correlated with the size of the nest aggressiveness and at least one of our 2 boldness measures (encoun- the queens adopted in the laboratory (latency to approach rival: ters before retreat) were correlated (latency to approach rival vs. n ¼ 52, P ¼ 0.98; encounters before retreat: n ¼ 38, P ¼ 0.62; aggres- aggressiveness: n ¼ 38, q ¼ 0.37, P ¼ 0.02; encounters before retreat siveness: n ¼ 38, P ¼ 0.72; exploration: n ¼ 52, P ¼ 0.56; activity: vs. aggressiveness: n ¼ 38, q ¼ 0.89, P< 0.0001) (Figure 3). This n ¼ 52, P ¼ 0.62). provides evidence for a behavioral syndrome between aggressiveness and at least 1 measure of boldness in P. metricus. However, we can- not rule out the possibility that Boldness II and aggressiveness lack Discussion independence, given that the assays were performed simultaneously. This study is the first to demonstrate that paper wasp queens (or Lastly, there existed a strong positive relationship between ex- wasps in general) exhibit consistent differences in behavior across ploration and activity time (q ¼ 0.93, P< 0.0001), though we are time and context (personality), and correlated personality metrics hesitant to call this a behavioural syndrome, as these measures are (behavioral syndrome). It must be noted, however, that behavioral likely not independent—wasps that are more active will, by random syndromes were only found between traits that were measured in chance alone, enter into more novel chambers than less-active the same trial, and thus future experiments using independent trials wasps. No syndromes were found between any other behavioral should be performed to verify whether the syndromes discovered in traits (aggressivness vs. activity: q ¼ 0.0035, P ¼ 0.98; aggressiveness our study hold. Additionally, future studies should be careful to re- vs. exploration: q ¼ 0.046, P ¼ 0.77; activity vs. Boldness I: move any traces of apolar compounds left in the arenas that, in this q ¼ 0.049, P ¼ 0.71; activity vs. Boldness II: q ¼ 0.12, P ¼ 0.45; ex- study, may have remained due to the use of a polar solvent. The ploration vs. Boldness I: q ¼ 0.086, P ¼ 0.52; exploration vs. presence of behavioral differences in Polistes wasps found in our Boldness II: q ¼ 0.097, P ¼ 0.54). study has many potentially important and interesting implications Downloaded from https://academic.oup.com/cz/article-abstract/64/1/45/3063806 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Wright et al.  Personality variation and behavioral syndromes in Polistes metricus 49 for their life history and fitness. Though P. metricus generally founds 2014). Given that paper wasps are only primitively eusocial, mean- nests solitarily, they do also form foundress associations on occa- ing that the reproductive division of labor is less discrete than in sion. Thus, it remains to be determined whether this personality more “advanced” eusocial taxa such as ants and honeybees (Wilson variation correlates with the tendency to form foundress associ- and Holldobler 2005), personality studies in paper wasps and other ations, the likelihood of becoming the dominant foundress (the Vespidae may prove particularly enlightening in these discussions. queen) in an association, the likelihood of being usurped by conspe- For instance, one may explore the extent to which individual differ- cifics, susceptibility to nest parasitism, and overall colony productiv- ences are associated with task participation, efficiency at various ity. Additionally, it may be intriguing to find out whether queen tasks, and propensity to switch tasks. At the colony level, examining personality is related to the differences between queens, foundresses, within-group behavioral composition may help us to predict inter- and workers in how much comb space they occupy as well as how colony differences in collective aggressiveness (Hui and Pinter- they distribute themselves spatially on the comb (Baracchi et al. Wollman 2014; Modlmeier et al. 2014a), brood care (Jandt et al. 2010). Each of these topics have been rigorously examined using 2013), or life-history attributes. By conducting such studies in paral- various Polistes models, however, we feel that the application of a lel across species with varying degrees of sociality (or eusociality), personality approach has the potential to integrate these topics into we may be able to retrace the role of individual behavioral differ- a shared explanatory framework. ences as precursors to morphologically based task differentiation. Polistes wasps have served as prominent model organisms for Indeed, such behavioral precursors have already been discovered in the study of dominance hierarchies and social interactions (Jandt ants (Dornhaus 2008; Pinter-Wollman et al. 2012; Lichtenstein et al. 2014). Many of these studies have focused on how intracolony et al. 2016) and even social spiders (Wright et al. 2014, 2016). aggression mediates dominant–subordinate, foundress–worker, and Our study also hints at the possibility for a more reductionist ap- worker–worker interactions (Eberhard 1969; Strassmann and proach regarding the mechanisms that lead to and help maintain in- Meyer 1983; Miyano 1986), yet do not focus on inherent differences ter- and intra-colony behavioral variation. Most studies have been in aggressiveness between wasps outside of a social context. A thor- content with explaining differences in behavior between colonies as ough examination of the prevalence of behavioral variation among resulting from intra-colony differences in behavior. Several mechan- queens, foundresses, and workers in Polistes and other Vespinae pre- isms have been proposed to explain inter-colony behavioral differ- sents researchers with an interesting opportunity to delve deeper ences, such as differences in the total average behavior of workers, into the role of intrinsic individual differences in mediating complex differences in the behavioral distribution of worker behavior, differ- social outcomes. Exploring behavioral variation among other social ences in behavioral response thresholds, or purely resulting from ex- arthropods have proved to be highly insightful, for example, ants ternal environmental factors (Bonabeau et al. 1996, 1998; (Modlmeier and Foitzik 2011; Hui and Pinter-Wollman 2014; Theraulaz et al. 1998; Pinter-Wollman 2012). Furthermore, the so- Modlmeier et al. 2014b), bees (Wray et al. 2011), water striders (Sih cial group, as opposed to the individual worker, is often regarded as and Watters 2005; Chang and Sih 2013), social spiders (Pruitt and being the object of selection in many social systems (Holldobler and Riechert 2011; Pruitt and Goodnight 2014; Wright et al. 2014). Wilson 1990; Mayr 1997; Korb and Heinze 2004). We suggest that Moreover, aggressive/bold syndromes, such as the one observed in in some systems, such as ours, where colony life histories are typified P. metricus here, have been identified in many nonsocial species by discrete solitary and social stages, the queen herself could be re- (Bell 2007), and are often associated with increased dispersal abil- garded as the object of selection, as her success during the founding ities (Clobert et al. 2009), different foraging strategies (Bell and Sih stage is necessary for there to even be a colony in the first place. And 2007; Chapman et al. 2011), vigilant anti-predator behavior her behavior may play a role in determining the behavioral compos- (Huntingford 1976), and even grouping behavior (Aplin et al. ition of her future colony. Once the social group exists, however, 2013). Given that Polistes wasps participate in all these behaviors to the object of selection may then be transferred to the social group as a great degree, further investigations in this system on how this syn- a whole. We feel it is an oversight to ignore the queen’s behavior drome and other personality traits influence life history and survival during the founding stage—the most vulnerable period of the col- should be rewarding. Notably, Polistes might be among the most ony’s life cycle—when considering the underlying mechanisms of promising future models for these lines of research, because the re- both inter- and intra-colony behavioral variation. peatability of individual differences in P. metricus (r ¼ 0.81–0.93) To conclude, we have documented a clear signature of personal- are among the very highest observed for any trait or any taxa meas- ity in P. metricus queens, including common traits such as aggres- ured in either in the lab or field (Bell et al. 2009), though personality siveness, boldness, exploration, and activity level. This species also traits were measured over a very short-time span in our study that exhibits a behavioral syndrome that bears resemblance to those may have inflated our repeatability estimates. Thus, there is compel- found in a variety of other social and solitary vertebrates ling evidence that queens exhibit substantial characteristic differ- (Huntingford 1976; Bell 2005; Dingemanse et al. 2007; ences in their behavioral tendencies, and that these individual Dochtermann and Jenkins 2007; Moretz et al. 2007) and inverte- differences may have consequences on a variety of behavioral and brates (Riechert and Hedrick 1993; Johnson and Sih 2005; Kortet ecological outcomes. and Hedrick 2007; Reaney and Backwell 2007). The short time Additionally, given that evidence suggests that paper wasps (and frame over which the queens were measured, however, means that other social Vespidae) evolved eusociality (or primitive eusociality) we cannot state with certainty that the personality differences independently from other eusocial Hymenoptera and Isoptera observed in our study are maintained throughout the queens’ tenure (Johnson et al. 2013), we feel that comparative personality studies on the nest. Both of these features bode well for Polistes’ promise as between these taxa could help contribute to the conversation sur- a generalizable model for behavioral syndrome research. This poten- rounding the evolution of eusociality and insect castes. Recent dis- tial is further augmented by the diversity of social structures ex- coveries in social spiders regarding the presence of “personality castes” suggest that behavioral variation could be an initial step on hibited within the Vespidae and the reservoir of seminal behavioral the path to complete reproductive division of labor (Wright et al. research that has already been conducted using these systems. Thus, Downloaded from https://academic.oup.com/cz/article-abstract/64/1/45/3063806 by Ed 'DeepDyve' Gillespie user on 16 March 2018 50 Current Zoology, 2018, Vol. 64, No. 1 Table 1. A summary table of repeatability values and a correlation matrix for each trait tested Correlations [P values and (Spearman’s q)] Trait Repeatability (r) Boldness I Boldness II Aggressiveness Exploration Boldness I 0.93 — — — — Boldness II 0.81 — — — — Aggressiveness 0.88 0.021 (0.37) <0.0001 (0.89) —— Exploration 0.88 0.52 (0.086) 0.54 (0.097) 0.77 (0.046) — Activity 0.92 0.71 (0.049) 0.45 (0.12) 0.98 (0.0035) <0.0001 (0.93) Notes: The first numbers in the matrix are the P values, and Spearman’s rho (q) is to the right in parentheses. Significant P-values are in bold. we encourage wasp researchers to further explore the potential im- Bonabeau E, Theraulaz G, Deneubourg JL, 1996. Quantitative study of the fixed threshold model for the regulation of division of labour in insect soci- portance of personality in their own research questions. eties. Proc R Soc B 263:1565–1569. Bonabeau E, Theraulaz G, Deneubourg JL, 1998. Fixed response thresholds and the regulation of division of labor in insect societies. Bull Math Biol Acknowledgments 60:753–807. We would like to acknowledge the many undergraduate researchers who Canestrelli D, Bisconti R, Carere C, 2016. Bolder takes all? The behavioral di- helped to keep the wasps fed and watered, as well as Kayla Hale for her assist- mension of biogeography. Trends Ecol Evol 31:35–43. ance in the lab. Additionally, we thank the Carson lab for their helpful com- Cervo R, 2006. Polistes wasps and their social parasites: an overview. Ann ments and criticisms on previous drafts of this manuscript, and Christine Rice Zool Fennici 43:531–549. for her commitment to twerking in the field, rain or shine. Cervo R, Cini A, Turillazzi S, 2015. Visual recognition in social wasps. In: Aquiloni L, Tricarico E, editors. Social Recognition in Invertebrates. Switzerland: Springer International Publishing, 125–145. 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