Female house sparrows prefer big males with a large white wing bar and fewer feather holes caused by chewing lice

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1 Behavioral Ecology doi: /beheco/arr182 Advance Access publication 20 November 2011 Original Article Female house sparrows prefer big males with a large white wing bar and fewer feather holes caused by chewing lice Gregorio Moreno-Rueda a and Herbert Hoi b a Estación Experimental de Zonas Áridas (CSIC), La Cañada de San Urbano, Ctra. Sacramento s/n, E-04120, Almería, Spain and b Konrad-Lorenz-Institut für Vergleichende Verhaltensforschung, Department für Integrative Biologie und Evolution, Veterinörmedizinische Universitöt, Savoyenstraße 1a, A-1160, Wien, Austria Males frequently signal their resistance against parasites by elaborate ornaments. By mating with more ornamented males, females may choose less parasitized partners, and benefit by reducing the probability of contagion of parasites with direct transmission. Chewing lice (order Phthiraptera) are parasites of birds that considerably harm hosts, even decreasing survival. Previous studies showed that male house sparrows (Passer domesticus) can signal resistance against chewing lice by the size of the white wing bar, with more resistant birds having a larger bar. Here, in a mate-choice experiment, 16 female sparrows were presented to 16 dyads of males having similar initial wing bar sizes. In each dyad, the wing bar was experimentally reduced in a randomly selected male. Female house sparrows chose males with larger wing bars. Nevertheless, females also preferred males with less feather holes caused by chewing lice and larger males. By choosing males with larger wing bars, females choose males with larger uropygial glands, an organ involved in the resistance against chewing lice in this species. Therefore, white patches, which are widespread in birds, might be used by females in order to evaluate male resistance against chewing lice. Key words: chewing lice, mate choice, parasites, Passer domesticus, sexual selection. [Behav Ecol 23: (2012)] INTRODUCTION Parasites, by extracting resources from their hosts, decrease the host s fitness, becoming a strong evolutionary force for hosts (Gómez et al. 2010). To minimize the cost of parasitism, hosts must invest in antiparasitic strategies (Wakelin and Apanius 1997; Moyer and Clayton 2003; Møller and Saino 2004). However, antiparasitic strategies, such as the immune system, are usually costly and should be traded against other resource-demanding aspects of life history (review in Ardia and Schat 2008). Given that sexual ornaments are frequently costly to produce or bear (Andersson 1994), less parasitized individuals would have more resources to invest in the development of sexual ornaments (e.g., Hõrak et al. 2004; Hill et al. 2005; Mougeot et al. 2007), and therefore, such ornaments may indicate individual resistance to parasites (e.g., Roulin et al. 2001; Hill and Farmer 2005; Dawson and Bortolotti 2006). Thus, females (usually the choosing sex), by selecting moreornamented (therefore, less parasitized) males, may procure benefits by diminishing the probability of contagion of parasites transmitted by direct contact (Borgia and Collis 1989; Able 1996; Møller et al. 1999). By choosing less parasitized males, females also choose healthy males, which may be more proficient delivering parental care to offspring, although they may also be the ones that show polygamy (Hamilton 1990; Hill 1991; Price et al. 1993). Moreover, if sexual ornaments signal Address correspondence to G. Moreno-Rueda. gmr@eeza. csic.es. Received 19 January 2011; revised 10 October 2011; accepted 11 October Ó The Author Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please journals.permissions@oup.com heritable resistance against parasites, females choosing more ornamented males would acquire indirect (genetic) fitness benefits, as their offspring will inherit the resistance against parasites, increasing their fitness (Hamilton and Zuk 1982; Hillgarth and Wingfield 1997; Møller et al. 1999). In birds, many studies have shown a correlation among the load of different parasites and the magnitude of sexual signals such as song or plumage (reviews in Garamszegi 2005; Griffith and Pryke 2006). Among the main parasites in birds are chewing lice (also called feather lice; order Phthiraptera, formerly Mallophaga). Chewing lice are a group of ectoparasites that develop their complete cycle on birds, feeding on feather keratin, skin debris, and, in the case of suborder Amblycera, blood (Price et al. 2003). By feeding on feathers, these parasites deteriorate the quality of the plumage, provoking small holes on feathers (Møller 1991; Vas et al. 2008), which diminishes thermoregulatory capacity (Booth et al. 1993), and increases feather breakage (Kose and Møller 1999). Consequently, more infected individuals show delayed arrival dates (for migratory birds, Møller, de Lope, et al. 2004), delayed breeding commencement (Pap et al. 2005), reduced body condition (Potti and Merino 1995), and even lower survival (Brown et al. 1995; Clayton et al. 1999; Pap et al. 2005). Chewing lice are transmitted among hosts directly by contact (Marshall 1981), and resistance against these parasites may be heritable (Møller, Martinelli, et al. 2004). Therefore, females may achieve direct (lower risk of contagion) and indirect (more-resistant offspring) fitness benefits by choosing liceresistant males. Indeed, a number of studies have shown female preference for males less infected by lice (Hillgarth and Wingfield 1997). In the barn swallow (Hirundo rustica), resistance against chewing lice is reflected by the size of white spots present

2 272 Behavioral Ecology in the tail, and females prefer males with larger white spots (Kose and Møller 1999; Kose et al. 1999). These authors suggested that white spots honestly signal resistance against lice because chewing lice feed primarily on white feathers, which are softer (Kose et al. 1999; but see Bush et al. [2006] for a contrasting result). Consequently, only resistant males may develop large white spots, as spots would otherwise be chewed by lice, increasing the risk of tail breakage (Kose and Møller 1999). Although evidence of female preference for males with whiter or larger white patches has been found in other bird species (review in Pryke 2007; alsoseemontgomerie et al. 2001; Ferns and Hinsley 2004; Chaine and Lyon 2008; Galván and Sanz 2008; Bonato, Evans, and Cherry 2009; Griggio et al. 2011), we know only one other example where a white patch hasbeen shown to be indicative of resistance against chewing lice, namely the wing bars in house sparrow (Passer domesticus). As in barn swallows, wing bar size of male house sparrows is negatively correlated with the number of feather holes caused by chewing lice (Moreno-Rueda 2005). At the same time, wing bar size is positively correlated with the size of the uropygial gland, an organ with an antiparasitic function against chewing lice (Moreno-Rueda 2010). White wing bars are restricted to males, less apparent in winter, and conspicuously displayed during the courtship (Summers-Smith 1988; Cramp 1998; Anderson 2006). All this information suggests that this signal is used in female mate choice. Nevertheless, no available study has examined whether female house sparrows prefer males with larger wing bars. For this reason, in this study, we analyze female choice behavior according to experimentally modified wing-bar size in the house sparrow. MATERIALS AND METHODS Study subjects The house sparrow is a sexual dimorphic passerine distributed worldwide (Anderson 2006). Males show a black bib in the throat and a white wing bar, which are not present in females. The 2 traits intervene in agonistic encounters (Bókony et al. 2006), and the bib is under sexual selection, mainly intrasexual (review in Anderson 2006), although intersexual selection may operate under certain circumstances (Griggio and Hoi 2010). Wing-bar size is positively correlated with uropygial gland size, an organ related to resistance against chewing lice (Moreno-Rueda 2010). Consequently, wing-bar size is negatively correlated with the number of feather holes caused by chewing lice (Moreno-Rueda 2005). Therefore, wing-bar size offers information concerning resistance against chewing lice and could be used by females in mate choice. Both bib and wing bar are conspicuously displayed during courtship (Cramp 1998), suggesting that they intervene in mate choice. However, although several studies have analyzed mate choice on bib size (review in Anderson 2006), no study has examined the possibility of mate choice on wing-bar size. Ninety-six house sparrows (61 males and 35 females) were captured at a farm in Padul (SE Spain; lat 37 01#N, long 3 37#W) at the end of January Sparrows were housed in 8 outdoor aviaries of 12 m 3 each, located in Moraleda de Zafayona (lat 37 11#N, long 3 57#W). Six aviaries held females and males (4 6 pairs), whereas 2 aviaries held only males (14 and 15 individuals). Confinement was carried out with the permission of the Andalusian government, abiding by the European directive (P6_TA(2009)0343), and no bird showed symptoms of stress or died during this study. All birds were individually marked with color rings and were supplied with water and food (seed mixture, fruit, dipteran larvae, and different vitamins and minerals) without restriction, as well as diverse perches, and trays with water and dust for bathing. The aviary, especially the recipients for water and food, was regularly cleaned and disinfected. Figure 1 Sketch of the experimental cage of mate choice. Experimental design Between February 29 and March 8, we performed a matechoice experiment, when birds mate. For 24 h, 16 different females were placed in an experimental cage of cm. Food and water were available ad libitum. Females were offered 3 perches, one on each side of the cage and one in the center. On the left and right sides of the female cage, one male was offered in an adjacent cage ( cm; Figure 1). In each trial, males and females were taken from different aviaries, and they had no contact prior to the experiment. No individual was used in 2 trials, and the fact that males were in aviaries with or without females did not affect female rating (data not shown). Males were matched for their wing-bar size, which was measured by means of photography on gridded paper with a digital camera (Nikon Coolpix 4300; following Figuerola and Senar 2000). The camera was mounted on a tripod, consistently at the same distance from birds. Afterward, patch surface areas were measured with the program Image J (Rasband 2008). In each dyad of males, one male, randomly selected, was designed as the experimental male, and we reduced its wing bar by coloring the outermost feathers of the bar with a black marker. In the other male (control male), we painted with the black marker a similar portion of the brown covert feathers closest to the wing bar, therefore showing coloration similar to that in experimental males (measured with a spectrophotometer Konica Minolta CM-2600d). The position (left/right) of the experimental male cage was alternated for each trial. Given that environmental light may affect female perception (Théry 2006), the experiment was performed outside, under the same natural light conditions and regime as for wild sparrows. During the experiment, weather was constant, consistently sunny, with no rain or wind. During the 24 h of acclimation to the experimental cage, males and females could not see each other due to plastic barriers. The experiment started 15 min after the plastic barriers were removed and the sparrows became accustomed to the new situation. Throughout the experiment the female could see both males, but physical contact was prevented via a wire mesh. Cardboard barriers prevented the males from seeing each other, without limiting female movements. One researcher (G.M.-R) recorded the behavior of females, by scans at intervals of 1 min for 1 h, from a hiding place 15 m from the cage. We recorded whether females were resting, eating, drinking, moving, or showing interest for any male (paying attention to the male and standing close to him) and recorded their position (left or right side or in the center of the cage). We also checked whether males behaved with normality and showed interest in the female. In neither trial did individuals show obvious signs of stress, such as nervous and repetitive movements from one side of the cage to the other or prolonged immobility at the bottom of the cage. Any show of interest for a particular male, termed female rating, was considered as the number of times that a female was sighted

3 Moreno-Rueda and Hoi Mate choice for white wing bar in house sparrows 273 in front (on the perch) of that male. The most highly rated male by the female was considered the preferred male. We measured body mass with an electronic balance to the nearest of 0.1 g, wing length with a ruler to the nearest of 0.5 mm, and tarsus length with a digital caliper to the nearest of 0.01 mm, of males used in this study. Body mass of a male was lost in a dyad, reducing the sample size to 15 in analyses involving body mass. Bib size was determined by photographs (similar to wing bars, see above). As the wing bar is negatively related to louse load, we estimated relative louse load by counting feather holes in the primaries and secondaries of the right wing of males. Descriptive studies suggest that these marks in feathers are caused by chewing lice, as the density of some louse species and feather holes are correlated (Møller 1991; Vas et al. 2008). Therefore, the number of feather holes may be used as an indicator of louse load in birds (Clayton and Walther 1997). Statistical analyses Variables were close to a normal distribution, and therefore, we used parametric statistics. Motivation for mating might have varied among females, and poorly motivated females would have diminished the statistical power. Less motivated females would have been detected less frequently rating a male (i.e., showing interest for males). Therefore, we repeated the analyses weighing by the whole rating value (as indicative of motivation) of females. In general, when weighing was performed by whole rating, the analyses provided very similar results, and therefore, these results are not presented, except when findings significantly differed between the 2 analyses. In statistical models, we checked for homoscedasticity as well as for normality of the residuals (Quinn and Keough 2002). The analyses were performed with a repeated measures analysis of variance (RM-ANOVA). This test was used to analyze the difference in female rating between control and experimental males (treatment; within-dyads component), as well as the interactions with the differences in male traits. Moreover, in the between-dyads component, we analyzed whether the effect of male traits differed between treatments (von Ende 2001). When multiple tests were performed, we applied Bonferroni correction (Quinn and Keough 2002). Means are given with the standard error. RESULTS In the whole sample of males, unmanipulated wing-bar size was negatively correlated with the number of feather holes (Pearson correlation, r ¼ 20.33, P ¼ 0.03, n ¼ 61; Figure 2). Wing-bar size was not significantly correlated with tarsus length (r ¼ 20.03, P ¼ 0.82) or body condition (r ¼ 0.17, P ¼ 0.19) but was correlated with bib size (r ¼ 0.32, P ¼ 0.01). In the mate-choice experiment, the manipulation significantly diminished the size of the wing bar in the experimental birds (paired t-test, t 15 ¼ 9.20; P, 0.001; see original and final size in Table 1). In experimental birds, wing bar was decreased by an average of 0.40 cm 2 (range: cm 2 ), implying a reduction of 36% (range: 21 55%). The final size ranged between 0.35 and 1.35 cm 2, which is practically within the normal size range of wing bars in male house sparrows (mean: 1.38 cm 2 ; range: cm 2 ; n ¼ 61 males). In control birds, the manipulation did not significantly alter bar size (t 15 ¼ 0.14; P ¼ 0.89; Table 1). There were no significant differences between control and experimental males for the traits measured (morphological traits, feather holes, bib size, and original wing bar size), the only significant difference being manipulated wing bar (Table 1). We found no difference in female rating according to the position of the experimental Figure 2 Correlation between wing-bar size (cm 2 ) and chewing-louse load (number of feather holes). The line indicates the regression fit. male cage (left side: ; right side: ; t 15 ¼ 0.25; P ¼ 0.81). Eleven females preferred (rated more times) the control male (with larger wing bar), whereas 4 females preferred the experimental male and one female showed no clear preference. A two-sample proportions test revealed significant differences in preference for experimental and control males (z ¼ 2.48; P ¼ 0.01). Female rating tended to be higher for control males ( ) than for experimental males ( ), but the difference was not significant (paired t-test; t 15 ¼ 1.47; P ¼ 0.16), although statistical power was low (1 2 b ¼ 0.39). We investigated whether differences between males in any measured trait, apart from manipulated wing bar, affected female decision. Difference between preferred and nonpreferred males in tarsus length significantly correlated with the difference in female rating of preferred and nonpreferred males (Table 2; Figure 3). Controlling for differences in tarsus length between control and experimental males, we found a significant difference in rating of experimental and control males, with females preferring control males (RM-ANOVA; treatment effect: F 1,14 ¼ 10.01; P, 0.01; treatment 3 difference in tarsus length: F 1,14 ¼ 12.85; P, 0.01; Figure 4). The remaining morphological traits did not show a significant interaction with treatment, suggesting that only tarsus length Table 1 Difference in measured traits between experimental and control house sparrow males Experimental Control t 15 P Body mass (g) (1.70) (2.06) 0.51* 0.62 Tail length (mm) (2.52) (2.33) Wing length (mm) (1.73) (3.06) Tarsus length (mm) (0.73) (0.53) Louse load (feather holes) 2.31 (0.46) 2.25 (0.56) Bib size (cm 2 ) 5.08 (0.45) 5.15 (0.47) Initial wing bar (cm 2 ) 1.09 (0.09) 1.17 (0.08) Manipulated wing bar (cm 2 ) 0.69 (0.06) 1.18 (0.08) 6.69,0.001 Comparisons performed with Student s t-test. The standard error is in brackets. *For body mass, sample size was 15. The results were unchanged when applying Bonferroni correction (critical a ¼ ).

4 274 Behavioral Ecology Table 2 Correlations of the difference in measured traits between preferred and nonpreferred males, with the difference in rating for preferred and nonpreferred males Nonweighed Weighed r P r w P w n Difference in body mass Difference in tail length Difference in wing length Difference in tarsus length Difference in louse load Difference in bib size W indicates that correlations were performed with data weighed by whole rating value of females, as indicative of female motivation for mating. Correlations that were significant after applying Bonferroni correction appear in bold (critical a ¼ ). affected the results (data not shown). The effect of the treatment on female rating remained significant in a full model including all the traits measured, which revealed a significant interaction between the difference in louse load (control minus experimental males) and the female rating in each treatment (Table 3; Figure 5). This latter result suggests that females preferred males with low louse loads, and they seem to be able to detect louse load, to a degree, independently of wing-bar size. DISCUSSION The results of this study show wing-bar size to be negatively correlated with the number of feather holes, supporting previous findings (Moreno-Rueda 2005). Moreover, female house sparrows chose males with larger white wing bars. Given that males with larger uropygial gland show larger wing bars, by choosing males with larger wing bars, females appear to be concomitantly choosing males with larger uropygial glands, and thus, higher resistance against chewing lice (Moreno-Rueda 2010). Females benefit, because they diminish the probability of contagion, and, if the resistance against chewing lice is heritable Figure 3 Correlation of the difference in tarsus length between preferred and nonpreferred males, with the difference in rating between preferred and nonpreferred males. The line indicates the regression fit. Figure 4 Relationship between female rating of control (open circles) and experimental (filled circles) males, with the difference in tarsus length between control and experimental males, indicated by the lines of regression. in the house sparrow, as suggested for the barn swallow (Møller, Martinelli, et al. 2004), female house sparrows may also raise more resistant offspring, which would increase their fitness. Nevertheless, females seem to have some capacity to use other (unknown) traits in addition to wing bar to determine male louse load, given that, when the male with the largest wing bar (due to experimental manipulation) was heavily parasitized, females preferred the less parasitized male, despite a smaller wing bar. Nonetheless, this result should be considered with caution, as it is correlative and the sample size was low. For example, in the rock dove (Columba livia), females evaluated male louse load according to male display behavior, with more parasitized males offering less elaborate displays (Clayton 1990). White patches might honestly signal resistance against chewing lice because these parasites prefer to feed on white feathers (Kose et al. 1999). Moreover, several strains of the Table 3 Results of a RM-ANOVA for female rating according to manipulated wing-bar size, controlling for the differences in morphological traits and louse load between control and experimental males Between-dyads component Degrees of freedom F P Intercept ,0.001 Difference in body mass Difference in wing length Difference in tarsus length Difference in louse load Difference in bib size Error 9 Within-dyads component Effect of manipulated wing-bar size Rating 3 Difference in body mass Rating 3 Difference in wing length Rating 3 Difference in tarsus length ,0.001 Rating 3 Difference in louse load ,0.01 Rating 3 Difference in bib size Error 9

5 Moreno-Rueda and Hoi Mate choice for white wing bar in house sparrows 275 Figure 5 Relationship between female rating of control (open circles) and experimental (filled circles) males, with the difference in louse load (number of feather holes) between control and experimental males, indicated by the lines of regression. feather-degrading bacterium Bacillus licheniformis also show more degrading activity on white feathers (Burtt and Ichida 2004; Goldstein et al. 2004; Gunderson et al. 2008), suggesting that white patches are also more susceptible to damage of feather-degrading bacteria. Thus, the ability to have bigger wing bars may indicate a higher resistance against chewing lice as well as feather-degrading bacteria. There is evidence that uropygial gland secretion has properties against chewing lice (Moyer et al. 2003; Moreno-Rueda 2010) as well as against feather-degrading bacteria (Shawkey et al. 2003; Møller et al. 2009; Ruiz-Rodríguez et al. 2009). Therefore, to maintain white plumage in good condition, individuals bearing white patches should invest more time in preening (Roulin 2007), implying a maintenance cost (Walther and Clayton 2005). Individuals with larger white patches should have a welldeveloped uropygial gland (larger uropygial gland usually implies more secretion; Pap et al. 2010). In fact, at least 2 studies have shown that individuals with more extensive white plumage have larger uropygial glands, in the barn owl (Tyto alba; Roulin 2007) and with respect to the wing bar in the house sparrow (Moreno-Rueda 2010). However, the development of the uropygial gland is costly in terms of reduced immunocompetence (Piault et al. 2008), and only individuals in good condition can afford it in order to maintain the white plumage. In this scenario, a cheater male with a large white wing bar would lose a large proportion of covert feathers degraded by lice and/or bacteria. Cheaters with large white patches might also be precluded by a number of costs. For example, white patches may increase the risk of being detected by predators (Montgomerie et al. 2001), but there is no evidence for this cost in the house sparrow (Bókony et al. 2008). The size of the white wing bar might be maintained honestly due to the social environment, as shown for the white forehead in the collared flycatcher (Ficedula albicollis; Qvarnström 1997); but the size of the wing bar does not influence the result of agonistic encounters (Bókony et al. 2006). White coloration is produced in feathers without pigments by means of the incoherent scattering of the reflected light (Prum 2006). For this reason, it has usually been considered that there is no cost of development for plumage with this color. Recent studies, by contrast, have shown that the development of white plumage is not cost free, and birds reared on protein-poor diets develop white patches of smaller sizes than do well-fed birds (McGlothlin et al. 2007; also see Gustafsson et al. 1995), which has been shown also for the white wing bar of the house sparrow (Poston et al. 2005). Therefore, white patches may also be indicative of the nutritional state of their bearers, which could explain why some studies have found a relationship between white patch size and survival (Török et al. 2003; Hanssen et al. 2009), breeding quality (Ruusila et al. 2001; Hanssen et al. 2006), immune system (Hanssen et al. 2006; Bonato, Evans, Hasselquist, et al. 2009), and the degree of infection by Trypanosoma (Potti and Merino 1996). Moreover, molt speed affects wing-bar size and whiteness, as house sparrows molting relatively faster tend to grow smaller wing bars (Vágási et al. 2010). And recent results suggest that sparrows with larger uropygial glands, and thus with fewer feather holes, molt slower (Moreno-Rueda, submitted), thereby allowing them to develop a larger and whiter wing bar (Vágási et al. 2010). Therefore, despite the apparent simplicity of white plumage, it seems to be costly to produce and maintain. Even white patches may simultaneously signal different aspects of the bird (Grether et al. 2004; Hanssen et al. 2009). This might be the case of the white wing bar, the size of which has been related to resistance against chewing lice (Moreno- Rueda 2005, 2010; this study), its whiteness has been related to an adequate molt (Poston et al. 2005; Vágási et al. 2010), and the contrast in color with the surrounding feathers, but not wing bar size, is related to the dominance ranking (Bókony et al. 2006). In this work, we also found a preference of females for bigger males. Female preference for bigger males is quite general in birds, given that bigger males usually have competitive advantages in contests (review in Andersson 1994, p. 129). However, in the house sparrow, bib size, but not body size, determines dominance ranking (Møller 1987; Liker and Barta 2001; Gonzalez et al. 2002). On the other hand, there was no evidence of mate choice for males with larger bibs, this result being consistent with other studies in this species (review in Anderson 2006). Bib and wing-bar color are not significantly correlated (Václav 2006), suggesting that these 2 sexually selected traits signal different aspects of the phenotype of the house sparrows. Bib size may signal dominance (Anderson 2006), whereas wing bar signals resistance against chewing lice (this study). In conclusion, female house sparrows prefer to mate with males that are less parasitized by chewing lice, and those that have larger white wing bars. By doing so, females may choose males with a larger uropygial gland (positively correlated with wing-bar size), and thus more resistant against lice. By choosing these males, females presumably diminish the risk of direct contagion and raise offspring more resistant against lice. Consequently, wing-bar size seems to be under intersexual selection in the house sparrow. FUNDING G.M.-R. was funded by a postdoctoral fellowship from the University of Granada (Perfeccionamiento de doctores). The aviary was provided by G.M.-R s family. José M. Rivas kindly helped capture sparrows. Manuel Pizarro kindly designed Figure 1. Inés Álvarez, Carlos Castillo, Antonio López, and Maribel P. Moreno contributed to the care of the animals. David Nesbitt improved the English. All work was performed with the permissions of the Andalusian government. Comments by 4 anonymous referees greatly improve the manuscript.

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