Despite growing interest in female ornament evolution, we still have a rudimentary understanding of female display traits relative to similar traits in males. Under one popular adaptive scenario, fe- male ornaments are hypothesized to function in female–female competition and serve as badges of status, such that their expression is linked with elevated aggression in some cases. In this study, we investigated the relationship between 2 female ornaments—male-like red throat color and red spine coloration—and female aggression in 2 independently derived stream-resident populations of three-spined stickleback Gasterosteus aculeatus. Using simulated intrusions, we tested whether females with redder ornaments were generally more aggressive, and for variation in aggressive and social behaviors between the 2 populations. We found that the red intensity of the throat and spine did not predict aggression levels in either population, suggesting a limited role for both fe- male ornaments during female–female interaction. The 2 populations exhibited different levels of aggressive behaviors, unrelated to the color patches. Our results suggest that variation in selective pressures between populations may promote interpopulation variance in aggressive behavior but not the correlation between female ornamentation and aggression, and raise the possibility that red coloration may have evolved through different mechanisms or processes in the 2 populations. Key words: aggression, animal coloration, female ornaments, Gasterosteus aculeatus, stickleback. Within the last decade, work on sexual selection has demonstrated female ornament evolution remains one of the central goals of stud- that female ornaments are more common than previously thought, ies of female ornament evolution. and can be as conspicuous as those found in males (Kraaijeveld et al. The evolution of such ornaments is in some systems associated 2007; Clutton-Brock 2009; Tobias et al. 2012; Dale et al. 2015; with aggressive behaviors in the context of female–female competition Charmantier et al. 2017). A long-held hypothesis for female orna- (Pryke 2007, 2009; Clutton-Brock 2009; Midamegbe et al. 2011; ments views them as correlated by-products of selection on males, Tobias et al. 2012). Despite some potential costs, female aggressive- and some recent studies support this perspective (Lande 1980; Dale ness may be advantageous in a number of intrasexual contexts, et al. 2015; Yong et al. 2015; Charmantier et al. 2017). However, including competition for rank and territories, and for access to mates investigations of possible functions of display traits in females have (Bakker 1986; Rosvall 2011; Stockley and Campbell 2013). often yielded evidence that they benefit females directly (Clutton- Moreover, agonistic behaviors are often accompanied and correlated Brock 2009; Tobias et al. 2012; Flanagan et al. 2014). Resolving the with badges of status, that is, colorful traits whose functions include relative importance of by-product and direct selection processes in advertising competitive ability. Females bearing such conspicuous V C The Author(s) (2018). Published by Oxford University Press. 345 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 firstname.lastname@example.org Downloaded from https://academic.oup.com/cz/article-abstract/64/3/345/4924237 by Ed 'DeepDyve' Gillespie user on 21 June 2018 346 Current Zoology, 2018, Vol. 64, No. 3 badges tend to be more aggressive (Clutton-Brock 2009; Pryke 2009; male spine color intensity predicts attack behavior aimed at females dur- Midamegbe et al. 2011), and badges are commonly found in mating ing courtship trials (Wright et al. 2016). Spine color intensity is often systems with intense female–female competition and extra-pair mat- positively correlated with that of the throat, with which it shares to ing (Rubenstein and Lovette 2009; Stockley and Bro-Jørgensen 2011). some extent a genetic basis (Yong et al. 2013, 2016). Relationships between color variation and a variety of traits, Our goals in the present study were to 1) examine the relation- including aggression, have been studied extensively in the three- ship between variation in female throat color, spine color, and ag- spine stickleback Gasterosteus aculeatus, in which replicated adap- gressive response to a standardized stimulus between and within tive radiations have facilitated extensive and wide-ranging studies of populations, and 2) evaluate possible differences in aggressive and the evolution of male secondary sexual traits (e.g., Bakker and social behavior between our 2 study populations, which are Milinski 1993; Rowland 1994; McKinnon 1996; Boughman 2001, hypothesized to have independently evolved red female throat color- 2007; Malek et al. 2012). The ancestral marine (or anadromous) ation (Yong et al. 2013). Regarding the latter goal, the prediction stickleback form, which is hypothesized to have given rise to was that if the female color patches generally evolved in the context derived-freshwater populations, is known to be conventionally sexu- of intrasexual competition and aggression, females from the popula- ally dichromatic for the male-typical nuptial throat ornament (i.e., tion with the most intense throat and spine coloration should behave red throats are present almost exclusively in males). In a few more aggressively. freshwater-resident North American stream populations, however, females too have been found to exhibit red nuptial throat coloration at high frequencies (von Hippel 1999; McKinnon et al. 2000; Yong Materials and Methods et al. 2013). Two such populations, which are the focus of this Stickleback collection and maintenance study, are found in different drainages in southern British Columbia Three-spined sticklebacks were collected during the breeding season (Little Campbell River, BC, Canada, hereafter LC) and Northern in 2 years and stream locations: LC in April 2010 (49.012 N, California (Matadero Creek, CA, USA, hereafter MAT). Given the 122.624 E) and MAT in June 2012 (37.393 N, 122.162 E). Fish distance between them and the likely postglacial origin of at least were shipped to our laboratory at East Carolina University (ECU), the British Columbia population, these populations have likely where they were housed in conditioned community tanks, as de- arisen from independent colonizations of freshwater by marine or tailed in Yong et al. (2015). All fish were maintained on a 16 L:8 D anadromous ancestors in which females lacked red throats. To date, photoperiod at 16 C. All fish were fed twice daily with brine shrimp formal documentation of stickleback red female coloration is con- and bloodworm (chironomid larvae), and allowed to acclimate to la- fined to stream-resident ecotypes from just these localities and one boratory conditions for at least 1 month before any behavioral trials more (von Hippel 1999) although we have observed the trait at add- were conducted. All experimental procedures were approved by the itional sites (McKinnon, unpublished data). ECU IACUC (Protocol #AUP 224a). The intensity of male stickleback red coloration has repeatedly been found to be positively correlated with male aggressiveness to a standardized stimulus (such as a dummy or a conspecific in a small Aggression experiment: simulated territorial intrusion container: Rowland 1984; McLennan and McPhail 1989; Wright To test for variation in female aggression, we used a simulated terri- et al. 2016) as well as with dominance in pairwise interactions torial intrusion previously validated in stickleback (Bakker 1986; (Bakker and Sevenster 1983; Baube 1997; McKinnon 1996). In our Sanogo et al. 2012). Behavioral experiments for each population investigations till date, we have not found a relationship between fe- were conducted during the breeding season (April–July), and within male red intensity and dominance (Yong et al. 2015), but we have not the same year in which they were collected. Resident females (LC: tested for a relationship with aggressiveness toward a standardized n¼ 23; MAT: n¼ 20), varying in throat color intensity from each stimulus; the latter tests are important because they may be more sen- population were haphazardly selected from community tanks, and sitive than experiments in which fish fully interact, because domin- individually isolated for 42 h in an experimental 21-L tank (41 20 ance and aggression are not always correlated (e.g., Rowland 1989; 1/4 25 1/2 cm) containing a UV transparent chamber Baube 1997) and because the negative dominance result is surprising (15 7 7 cm) hung inside and on the back of the tank. As the focus in light of findings for males. In addition, our behavioral studies so far was on the resident’s response to the visual presence of the intruder, have been confined to one population and drawing definitive conclu- the chamber was sealed, eliminating the potential transmission of sions from studies of single populations is problematic in a species water and chemical cues. The designated isolation period was previ- that shows as much geographic variation as the three-spined stickle- ously validated to promote territorial behavior and enhanced aggres- back (Bell and Foster 1994). Inclusion of additional populations also sion in females (Yong et al. 2015). All females were nongravid. enables the initiation of potentially informative comparative investi- After the isolation period and at the start of the behavioral trial, an gations. It is additionally important to note that some field observa- intruding female of the same population with duller throat color- tions of sticklebacks suggest that aggression and dominance may ation was introduced into the chamber. Dull-throated females were sometimes be beneficial to females, to facilitate access to nesting primarily used as natural and standardized stimuli. The chamber males, or maintain feeding territories (MacLean 1980). prevented physical contact between the females, and allowed us to Another orange-red color patch is gaining increasing attention in focus mainly on the resident’s behavioral response. Resident and in- stickleback research, on the posterior portion of pelvic spines and asso- truder females were size-matched (up to 5% difference in standard ciated membranes (Nordeide 2002; Hodgson et al. 2013; Amundsen length). The behavioral trial was video-recorded (Sony Handycam et al. 2015). The spine color patch seems almost ubiquitous (Amundsen Digital Camcorder-HDR-XR 500), and the behaviors of the resident et al. 2015; Yong et al. 2015), andearlierworksuggeststhat erected female directed at the intruder were scored using Noldus Observer pelvic spines might function during social displays as indication of eli- v7 (Noldus Information Technology, Leesburg, VA). We quantified cited aggression; males with erected spines have been observed to often latency to respond to the intruder (in seconds), number of charge at conspecifics (van Iersel 1953). In addition, we have found that approaches (within one body length of the intruder’s chamber), Downloaded from https://academic.oup.com/cz/article-abstract/64/3/345/4924237 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Yong et al. Aggression in red-throated female sticklebacks 347 proportion of time spent inspecting the intruder (duration of time Results spent within one body length of the intruder’s chamber/total trial Females generally responded to the intruders within 5 min by orient- duration), number of bites, bites while in proximity (bite number/ ing toward or approaching them, with no significant differences approach duration). Behavioral trials generally lasted about 30 min, between the populations (W¼ 245, latency: P ¼ 0.541, Mann– but up to 35 min in a few trials, that is, 5 trials, for the LC popula- Whitney U test). One LC female showed no behavioral response tion. To control for the variation in trial time duration across trials, during the trial, and was removed from further analyses. As previ- we calculated behavioral rates per minute. ously documented, MAT females had more intense red throat color- ation than LC females (W¼ 2, P ¼ 9.48 x 10 , Mann–Whitney U test, Figure 1), but spine color intensity did not differ between popu- Throat color measurement lations (W¼ 189.5, P ¼ 0.449, Mann–Whitney U test). Immediately after the behavioral trial, females were measured for While there is a negative trend for the relationship between red throat intensity or “red throat chroma” as detailed in Yong throat color and bite rate, the linear models revealed that the inten- et al. (2013, 2015). Throat coloration was only sampled once and sity of red throat and spine coloration were not significantly associ- after the trial, as it was previously found that color intensity does ated with the resident’s bite rate during the territorial intrusion in not significantly change before or after a social interaction (Yong either population (throat chroma: F ¼ 0.127, P ¼ 0.127, popula- 1,38 et al. 2015). The reflectance of the throat was measured using an tion: F ¼ 10.05, P ¼ 0.003, interaction: F ¼ 4.27, P ¼ 0.045, 1,38 1,38 Ocean Optics Maya spectrometer (Ocean Optics Inc., Dunedin, FL), Figure 2A; spine chroma: F ¼ 0.039, P ¼ 0.84, population: 1,38 where measurement was taken from 2 to 3 spots (0.8 mm in diam- F ¼ 8.56, P ¼ 0.005, interaction; F ¼ 0.023, P ¼ 0.881, 1,38 1,38 eter) along the midline of the throat, deliberately selected to yield Figure 2B). Both linear models explained 42% and 44% of the vari- maximum red throat. Then, we incorporated the spectrometry data ation, respectively. Although a significant interaction term was pre- into a physiological model of stickleback vision to estimate stickle- sent for throat color, further within population analyses revealed no back visual perception of red throat coloration. The relative quan- significant association between bite rate and throat color (LC: tum catches for each cone (UV, SWS, MWS, LWS) were calculated P ¼ 0.071; MAT: P ¼ 0.323), or spine color (LC: P ¼ 0.93; MAT: and used to calculate Cartesian coordinates (x, y, z) to obtain the P ¼ 0.82). Similarly, we found no relationships between either maximum (red) throat chroma, based on the Euclidean distance throat or spine chroma with bite rate whereas in proximity (throat from the achromatic center in a tetrahedral space; this measure was chroma: F ¼ 0.024, P ¼ 0.878, population: F ¼ 16.97, 1,38 1,38 used for subsequent analyses. P ¼ 0.0002, interaction: F ¼ 0.05, P ¼ 0.826; spine chroma: 1,38 F ¼ 0.17, P¼ 0.682, population: F ¼ 17.01, P ¼ 0.0002, inter- 1,38 1,38 action: F ¼ 0.004, P ¼ 0.947). Relationships between throat 1,38 color and other behaviors, that is, latency to respond, approaches, Spine color measurement and proportion of time spent, were also nonsignificant (P> 0.22). Spine color was quantified from standardized digital photographs, As there was a significant effect of population on bite rate, we each including a gray card, taken after the behavioral trial and using conducted further tests between populations, revealing other consid- methods detailed in Yong et al. (2013) and Wright et al. (2016).In erable behavioral differences. Although MAT females had more in- brief, we divided a digital image of the left spine into 8 equal sec- tense throat color, they did not generally exhibit higher levels of tions and calculated the red chroma of each, using Adobe Photoshop agonistic behaviors. LC females made more frequent approaches to CS3, as standardized R divided by the sum of standardized R, G, the intruder, but spent shorter periods of time close to them, and B. We used the maximum among these 8 initial chroma in sub- whereas MAT females spent more time in proximity overall sequent analyses, as “red spine chroma.” (W¼ 307.5, approach: P ¼ 0.0284; W¼ 59, proportion of time spent with intruder: P ¼ 5.294 10 Mann–Whitney U test, Figure 3A, B). While LC and MAT females did not differ statistically Statistical analyses Assumptions of residual normality were checked by visually inspect- ing the residuals for all models. If residual normality was met, we used linear models to examine the relationship between color patches and bites between populations, where either red throat or spine chroma and population (LC vs. MAT) were treated as fixed ef- fects, and bite rate [log(nþ 1) transformed] as the response variable. Standard length was first included in the model as a continuous vari- able, but was removed as it did not approach significance. In some cases, model residuals did not conform with normality and data transformation did not improve the situation; in such instances, nonparametric univariate tests were used to test for differences in color and behaviors (e.g., bites, approaches, approach duration, and bites while in proximity) between the 2 populations. We acknow- ledge that the year, in which the trials were conducted, and popula- tion are statistically confounded (i.e., each population was tested in separate years), and thus cannot tease apart the separate effects of year and population. In light of this, our comparisons between populations are interpreted with caution. All statistical analyses Figure 1. Boxplots showing differences in red throat color between popula- th th were performed in the R environment v. 3.3.2 (R Core Team 2016). tions. Plots show median and 25 –75 percentiles. Downloaded from https://academic.oup.com/cz/article-abstract/64/3/345/4924237 by Ed 'DeepDyve' Gillespie user on 21 June 2018 348 Current Zoology, 2018, Vol. 64, No. 3 Figure 2. Differences in the relationship between aggressive behavior and (A) red throat color and (B) spine color. The black and gray lines represent the Little Campbell and Matadero populations, respectively, in (B). Gray areas represent 95% conﬁdence intervals. Figure 3. Behavioral differences between stickleback populations. Boxplots show median and 25th–75th percentiles. * denotes signiﬁcance at P< 0.05 level. in bite rates (W¼ 284, P ¼ 0.108, Mann–Whitney U test, variation. In our study populations, in which females often possess Figure 3C), LC females engaged in more biting per unit time than the red throats typical of males of most populations, females re- MAT females when in close proximity to the intruder (W ¼ 312, sponded aggressively toward the intruder but the color intensities of P ¼ 0.0078, Mann–Whitney U test, Figure 3D), suggesting that LC the throat and spine were not significantly correlated with aggres- females mainly approach intruders to attack them, relative to MAT sion, and the trend (though nonsignificant) was for females with red- females. der throats generally to exhibit reduced aggression. These results complement and corroborate our earlier findings, in which red-throated females were not more aggressive or dominant during a Discussion dyadic social interaction (Yong et al. 2015). Also, we observed be- havioral differences in aggression between the 2 populations, but Ornamental traits often evolve in the context of social competition, these too failed to indicate a positive relationship between red including aggression and dominance, and are linked with behavioral Downloaded from https://academic.oup.com/cz/article-abstract/64/3/345/4924237 by Ed 'DeepDyve' Gillespie user on 21 June 2018 Yong et al. Aggression in red-throated female sticklebacks 349 coloration and aggression. In fact, LC females, whose red throats these color traits, it appears that color and behavior might not were the less intense of the 2 populations, exhibited more frequent covary consistently between the sexes, being less coupled in females. aggression when in close proximity to the intruder whereas MAT in- Whether these differences in correlations between traits might have dividuals spent more time close to the intruder, much as LC females an adaptive aspect is an open question. dominated, and differed from, anadromous females in an earlier We acknowledge potential limitations. First, the effects of popu- study (Yong et al. 2015). lation and year are confounded, which might partly influence some Our results are also unexpected in light of studies of male stickle- of the behavioral differences observed between the 2 populations. back that used the territorial intrusion paradigm. When confronted The year of collection could have included unaccounted variation in with an intruder, males with brighter red throats typically display environmental conditions, in which, for instance, interspecific com- more aggression, especially in freshwater stream ecotypes (Bakker petition or density were variable. However, it is worth noting that and Milinski 1993; Bakker 1994; Rowland 1994). Even in marine all fish from both populations were sampled at approximately the ecotypes, Rowland (1984) and McLennan and McPhail (1989) have same time of the year and during the breeding season, and tested shown that more intensely colored males can exhibit higher levels of within the same timeframe as to minimize variation in the experi- attack. Because both MAT and LC populations are from stream habi- mental design. Also, given the known documented variation in ag- tats, males would be predicted to behave in a similar way. Our labora- gression and other behaviors among stickleback populations tory has previously found that throat color intensity in LC males is a (Bakker 1994; Rowland 1994), it is likely the observed behavioral positive predictor of courtship intensity during mating trials (Wright variation is primarily owing to population differences. Nevertheless, et al. 2016). In the same study, Wright et al. (2016) reported that we advise some caution as we cannot definitely rule out the possibil- males with more intense spine coloration bit females more often dur- ity of a year effect in the absence of replicated behavioral data across ing mating trials, but we did not detect any associations between spine years. Concerning a different aspect of our study, it is possible that coloration and female aggressive behaviors in the present investiga- other results could have been obtained if different female stimuli tion. It is possible that color patches do not covary with behaviors were used. For instance, intruders with redder throats might have consistently across the sexes and populations, and that the different elicited attacks from the resident fish, as the trait is often considered social contexts (intra vs. intersexual) can affect these relationships. a releaser of aggression in territorial individuals (Rowland 1982). Although rates of female agonistic behaviors were not readily However, Rowland (1982) found the opposite effect, with red lead- predicted by color intensity in the throat or spine within our study ing to reduced attacks (also see Wright et al. 2015), whereas in other populations, we did find notable interpopulation differences in ag- studies, the intruder’s coloration had no effect on the resident’s ag- gressive and other social behaviors. We also observed that the throat gressive response (Peeke et al. 1969; McKinnon and McPhail 1996). color difference between female populations in this study was In conclusion, our study reveals substantial differences in aggres- greater than observed by Yong et al. (2013), which may be ex- sive behavior between female stickleback from 2 populations in plained by the time of the breeding season, or the year, during which which female possess red throats and spines, and provides comple- fish were collected. Whereas LC females were collected earlier in the mentary evidence that the female traits are not associated with ag- season (April), MAT females were collected later (June). Regardless, gressive behavior and thus unlikely serve as badges of status. Our MAT females typically express the brightest throat color of the 2 study populations provide an example of how female ornaments populations, yet generally bit less once in proximity to intruders, may not necessarily evolve through adaptive processes, and could which suggests that MAT females are less aggressive. Conversely, arise as byproducts of a shared genetic architecture with, and selec- LC females, whose throat intensity was on average lower, tended to tion on, males. bite more, especially when in close proximity to the intruder. We also observed differences in the amount of behavioral variability ex- hibited, where LC females exhibited greater variation. Taken to- Acknowledgments gether, the inconsistent trend between the 2 populations suggests We thank members of the McKinnon lab for assistance with ﬁsh husbandry that among population color differences are unlikely to be mediated and maintenance; K. Peichel and D. Schluter and their labs who provided lo- principally via agonistic social behaviors. Rather, differences in ag- gistical help; the Semiahmoo First Nation, California Department of Fish and onistic behaviors and color may evolve somewhat independently at Game (Permit #: SC-11861), BC Ministry of Natural Resources (Permit #: least in some cases. Consistent with patterns in this study, stream fe- SU11-68627, 76724), and Little Campbell Regional Park for granting us ac- males from the LC population also engage in more agonistic encoun- cess to their lands and permits for ﬁsh collection; I. Schlupp and 3 anonymous ters than do LC anadromous females (Yong et al. 2015), which are reviewers for valuable comments on the manuscript. thought to possess ancestral character states relative to the stream LC females. This supports our earlier supposition that selection for female aggressiveness may be relatively favored in the LC stream Funding habitat. Such differences in behavior among stickleback populations The work was supported in part by grants from the Animal Behaviour are not uncommon and often have been attributed to ecological vari- Society, the American Museum of Natural History, the American Society of ation (Bell 2005; Bell and Sih 2007). Ichthyologists and Herpetologists, and the Society for the Study of Evolution Based on the findings of this study together with previous work, [to L.Y.]; an ECU Undergraduate Research and Creative Activities Award [to nonadaptive mechanisms may play the major role in male-typical B.L.]. throat color evolution in female stickleback. Indeed, quantitative loci mapping of the red throat and spine in the MAT population confirms that coloration in both sexes is due to a similar, possibly Authors’ contributions shared genetic architecture and potential pleiotropy between traits (Yong et al. 2016), consistent with a byproduct process. 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Experimental investigations of the evolu- tionary signiﬁcance of sexually dimorphic nuptial coloration in Downloaded from https://academic.oup.com/cz/article-abstract/64/3/345/4924237 by Ed 'DeepDyve' Gillespie user on 21 June 2018
Current Zoology – Oxford University Press
Published: Mar 7, 2018
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