Multiple color patches and parasites in Sceloporus occidentalis: differential relationships by sex and infection

Multiple color patches and parasites in Sceloporus occidentalis: differential relationships by... Parasites generally have a negative influence on the color expression of their hosts. Sexual selec- tion theory predicts resistant high-quality individuals should show intense coloration, whereas sus- ceptible low-quality individuals would show poor coloration. However, intensely colored males of different species of Old and New World lizards were more often infected by hemoparasites. These results suggest that high-quality males, with intense coloration, would suffer higher susceptibility to hemoparasites. This hypothesis remains poorly understood and contradicts general theories on sexual selection. We surveyed a population of Sceloporus occidentalis for parasites and found infections by the parasite genera Lankesterella and Acroeimeria. In this population, both males and females express ventral blue and yellow color patches. Lankesterella was almost exclusively infect- ing males. The body size of the males significantly predicted the coloration of both blue and yellow patches. Larger males showed darker (lower lightness) blue ventral patches and more saturated yellow patches that were also orange-skewed. Moreover, these males were more often infected by Lankesterella than smaller males. The intestinal parasite Acroeimeria infected both males and females. The infection by intestinal parasites of the genus Acroeimeria was the best predictor for the chroma in the blue patch of the males and for hue in the yellow patch of the females. Those males infected by Acroeimeria expressed blue patches with significantly lower chroma than the uninfected males. However, the hue of the yellow patch was not significantly different between infected and uninfected females. These results suggest a different effect of Lankesterella and Acroeimeria on the lizards. On the one hand, the intense coloration of male lizards infected by Lankesterella suggested high-quality male lizards may tolerate it. On the other hand, the low chroma of the blue coloration of the infected males suggested that this coloration could honestly express the infection by Acroeimeria. Key words: animal communication, coloration, Hamilton and Zuk, parasites, sexual selection. V C The Author(s) (2018). Published by Oxford University Press. 1 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/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 2 Current Zoology, 2018, Vol. 0, No. 0 In 1982, Hamilton and Zuk proposed a co-evolutionary mechanism yellow coloration of lizards in the genus Sceloporus in relation to to explain how sexual selection favors resistance against parasitic the infection by 2 closely related hematic and intestinal parasites in diseases in nature: The parasite hypothesis (Hamilton and Zuk a population where both males and females express color patches. 1982). This Hamilton–Zuk (H–Z) hypothesis predicts a negative The aim of the study was to test whether the different color patches relationship between the expression of the host’s secondary sexual in males and females reflect information on these parasitic infections characters and the degree of its parasitic infections (Balenger and and also whether the observed relationships have a negative sign as Zuk 2014). Thus, sexual selection favors resistance against parasites expected by the H–Z hypothesis. Considering previous results of the because individuals would mate with highly ornamented individuals parasite hypothesis from studies of lizards, we predicted that males (Hamilton and Zuk 1982). Evidence supporting the parasites with more intense coloration will be infected by hemoparasites. hypothesis (Hamilton and Zuk 1982) exists for insects (Zuk 1988; However, we might expect a negative relationship between the Worden et al. 2000), fish (Ward 1988; Houde and Torio 1992), and male’s color expression and the infection by intestinal parasites. In birds (Merila ¨ et al. 1999; Ho ¨ rak et al. 2001; del Cerro et al. 2010). addition, we expect different relationships of parasitic infections, In all these host–parasite systems, the infected individuals usually with color expression depending on the sex of the host. show poor breeding coloration (Thompson et al. 1997; Martı ´nez- Padilla et al. 2007, but see also Skarstein and Folstad 1996) and suf- Material and Methods fer reduced survival (Merino et al. 2000; Martı ´nez-de la Puente et al. 2010). However, studies of both Old and New World lizards The host model have produced mixed results. On the one hand, studies investigating Sceloporus occidentalis (Squamata: Phrynosomatidae) is usually the relationships between the expression of the breeding coloration described as sexually dimorphic. Adult males express blue ventral and the infection by ticks or nematodes in lizards suggest that these patches, whereas females typically show gray bellies (e.g., Stebbins parasites negatively affect the expression of breeding coloration in and McGinnis 2012). However, in some populations of this lizard male lizards (Va ´ clav et al. 2007; Megı ´a-Palma et al. 2016a, 2017a; species, both sexes present ventral blue patches (Bell and Price Llanos-Garrido et al. 2017). On the other hand, studies considering 1996). In a closely related species, S. jarrovi, patches of males had chronic infections produced by hematic parasites contradict pre- reduced lightness, greater saturation and a higher angular hue (i.e., vious results and, therefore, the parasite hypothesis. In these studies, were more bluish) than ventral patches of females (Cox et al. 2008). male lizard hosts with more hematic parasites usually have more In addition to the blue coloration, S. occidentalis has yellow patches intense colorations (Ressel and Schall 1989; Megı ´a-Palma et al. on their forelimbs that are fundamentally based on pterins in lizards 2016a, 2016b). Similarly as it occurs in birds, coloration in New of the family Phrynosomatidae (Morrison et al. 1995; Weiss et al. and Old World lizards reflect individual quality, and males with 2012; Haisten et al. 2015). The function of pterine-based coloration more intense colors may be of better quality because they are usually as a potential intraspecific signal has been documented in female liz- bigger, keep larger home ranges, and have better mating success ards of the genus Sceloporus (Weiss 2002; Weiss et al. 2012). than paler individuals (Dı ´az 1993; Salvador and Veiga 2001; However, there is little evidence for its function in male lizards of Langkilde and Boronow 2010). Thus, the importance of the parasite this genus where, on the contrary, blue coloration seems to have hypothesis to sexually dimorphic coloration remains poorly under- received a major attention (e.g., Cooper and Burns 1987; Martins stood in lizards. 1993; Smith and John-Alder 1999). The presence of multiple color Visual communication is important in lizards and plays a key patches in males and females in some populations of S. occidentalis role in male intrasexual selection (Bajer et al. 2010; Abalos et al. makes this species a good model to test whether variation in social 2016). Dominant males have intense colors (Martı ´n and Lo ´ pez coloration in lizards of both sexes could reflect chronic parasitic 2009), and females might also prefer these intensely colored males infections as expected by the H–Z hypothesis. Several intestinal and (Salvador and Veiga 2001). However, costs and benefits of colora- hematic parasite genera were described as infecting S. occidentalis tion may differ between sexes (Svensson et al. 2009; Swierk (Bonorris and Ball 1955; Clark 1970; Ressel and Schall 1989). and Langkilde 2013). In New World lizards of the family Recently, we molecularly characterized the blood and the intestinal Phrynosomatidae, males use the coloration of conspecifics for sex parasites found in the population of S. occidentalis that we will discrimination (Cooper and Burns 1987). Indeed, in some popula- study here and we classified them, respectively, in the genera tions where males and some females show similar colorations, those Lankesterella (Eimeriorina: Lankesterellidae) and Acroeimeria females that have male-like coloration suffer reduced fitness because (Eimeriorina: Eimeriidae) (Megı ´a-Palma et al. 2015, 2017b). The males invest more time courting females with female-like pheno- intestinal parasites, genus Acroeimeria, that infect S. occidentalis types (Swierk and Langkilde 2013). That said, selection may also act undergo direct horizontal transmission among hosts without the on female coloration if it varies with reproductive status and may intervention of a vector. In contrast, hemoparasites of the genus serve to either attract or dissuade potential mates (Cooper and Lankesterella are transmitted by hematophagous arthropods. All of Crews 1988). these endoparasites undergo reproduction in internal organs of the Parasites can affect males and females differently owing to sexual host and break down the host’s tissues with every reproductive differences in behavior or hormone levels (Duneau and Ebert 2006). cycle, causing negative effects (Telford 2008). Thus, given these or other sexual differences in life-history traits, we might also expect sexual differences in the level or the sign of the Sampling methods relationship between the degree of infection and the color expres- We collected 68 S. occidentalis bocourtii (45 males and 23 females) sion, even in cases where both sexes show similar ornaments (e.g., in May 2014, corresponding to the breeding season of this species. Megı ´a-Palma et al. 2016 b). Thus, studying species where both sexes show color patches offers a good opportunity to investigate sexual Lizards were captured in a linear transect of 400 m (from differences in the expression of shared traits in relation to parasitic 36.985270, 122.061440 to 36.985287, 122.056934) on the infections. Here, we analyzed the spectral reflectance of blue and campus of the University of California, Santa Cruz, CA (UCSC). Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Megı´a-Palma et al.  Sexual coloration and parasites 3 Each lizard was individually identified using a xylene-free marker with a blue number that was written in the gray area of the belly out of the color patches as examples in the Appendix. The lizards were transported in a cooler to the lab in the UCSC facilities to perform all the color measurement under standardized light conditions (see below). Snout-to-vent length (SVL) for each lizard was measured with a ruler to the nearest millimeter and the individuals were weighed to the nearest centigram with a digital balance (Scout Pro SP202, Ohaus Corp., NJ, USA). A body condition index (BCI) was calculated as the residuals of the regression of log mass on log SVL (Dunlap and Mathies 1993). The sex of the individuals was deter- mined by the presence of enlarged post-anal scales (Cox et al. 2005; Langkilde and Boronow 2012). No lizard died during the study, and all were released at their site of capture following data collection. Screening of blood smears for parasites Blood samples were collected from the base of the tail of each lizard using sterilized needles (Megı ´a-Palma et al. 2013, 2014). In the case of male lizards, blood was collected by carefully avoiding the area of the hemipenis (by bleeding the tail at least 2 cm from the cloaca). The drop of blood obtained by this method was collected with a heparinized microcapillary tube (BRAND, 75 1.1 mm, Na- heparinized). These blood samples were used to make thin-layer blood smears. The dried blood smears were fixed with methanol Figure 1. (A) Comparison of the mean6 SE spectra of the blue patches of and stained for 40 min with Giemsa 1:10 at pH 7.2. The same per- males taking in consideration infection by parasites of the genus son (RMP) screened 15,000 red blood cells of each individual lizard Acroeimeria. (B) Comparison of mean6 SE spectra of the yellow patches of females considering infection by the same parasite. at 1,000 magnification (Megı ´a-Palma et al. 2017b) for diagnosing the presence of parasites in the blood of the lizards. (Ocean Optics Inc., Dunedin, FL, USA). The light source used was a deuterium–tungsten light (MINI DT1000A-112; Analytical Screening of fecal samples Instruments System, Inc., Ringoes, NJ, USA). We used an integra- Fecal samples were collected directly into 1.5-mL micro-centrifuge tion time of 10 ms, a boxcar width of 5, and 10 averaged readings tubes by briefly massaging the belly of the lizards (e.g., Megı ´a- per spectrum. In a darkened room, we measured the reflectance Palma et al. 2016a). These fecal samples were stored in 1 mL potas- from the color patches with a probe at 45 of inclination and a con- sium dichromate (Duszynski and Wilber 1997). We applied stant distance of 3 mm from the skin surface. We recorded 3 spectra Sheather’s sugar flotation technique (Megı ´a-Palma et al. 2015)to per patch. Ventral blue coloration shifts from blue to green depend- concentrate intestinal parasites. Each sample was screened at 600 ing on the body temperature in the closely related species, magnification. S. undulatus (Langkilde and Boronow 2012). To account for this, all individuals remained at room temperature (24 C) for 20 min Measuring reflectance of color patches before we measured coloration. All measurements were relative to a We measured the reflectance from the blue patch on the right side of 99% WS-1 white reflectance standard. the belly; and the yellow patch located on the anterior part of the right forelimb (Appendix). We avoided the blue markings that we Statistical analyses used to identify the individuals during the color measurements. All The mean reflectance spectra of each color patch and lizard were spectral measurements of the colorful patches were obtained by summarized in 1-nm bin-size spectra using the CLR v1.1 software spectrophotometry from 400 to 700 nm. Unfortunately, we could for analyzing reflectance spectra (Montgomerie 2009). Thereafter, not measure ultraviolet (UV) reflectance due to a problem with the the data of the 3 spectral measurements were averaged in Microsoft UV lamp in the spectrophotometer and, thus, it remained off during Excel (2010) per patch and lizard. Spectral data of color reflectance the measurements (the UV lamp is independent of the deuterium– can be broken down into 3 variables for its analysis: that is, light- tungsten light used for the visible range). Thus, our analyses are cen- ness, chroma, and hue (Montgomerie 2006). The total lightness for tered exclusively in the reflection of the visible range of the spec- trum. It is known that blue ventral coloration of Sceloporus lizards each spectrum was calculated as RQ , with Q being the per- 400-700 peaks in the blue–green spectral area and the reflectance is residual centage of reflectance for a given wavelength (k). Lightness is the total amount of light reflected by a surface and it is interpreted as in the near-UV range (see Figures 1a and 1b in Stoehr and McGraw how dark or light a surface is (Montgomerie 2006). Hue can be 2001). Pterins—and not carotenoids—are known to be the main pig- ment that produce the yellow or orange-based coloration of phryno- interpreted as a categorical variable of color describing a surface somatids (Morrison et al. 1995; Weiss et al. 2012; Haisten et al. (blue, green, yellow, red, etc). The hue variable for the blue and the 2015) and, apparently, no significant biological information is con- yellow patches was defined as the value of k for the Q (i.e., k ; max max Montgomerie 2006). Thus, lower values of hue in the blue patch tained in the near-UV region of color patches based on this pigment (Haisten et al. 2015; Cuervo et al. 2016). The spectrophotometer, define more bluish coloration, whereas higher values of hue in the an USB2000 Ocean Optics, was connected to a fiber-optic probe yellow patch define orange-like patches. For chroma calculation of Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 4 Current Zoology, 2018, Vol. 0, No. 0 each color patch, we selected the defined range of blue and yellow in Sexual dimorphism and dichromatism Males and females did not significantly differ in SVL (males mean the visible range (Endler 1990; Grill and Rush 2000), which assigns SVL6 SE¼ 59.46 0.9 mm, range¼ 41.0–69.0; females mean wavelength ranges of 75 nm to each color (i.e., blue, green, yellow, SVL6 SE¼ 56.46 1.0 mm, range¼ 48.0–68.0; F ¼ 3.78, and red) and we calculated RQ /RQ . Thus, we obtained 1, 66 segment 400-700 P¼ 0.05). Our model-selection procedure produced a set of models a relative reflectance, or saturation, of the segment of interest (Table 1) that included the sex of the individuals as the best predic- for each color patch (i.e., 400–475 nm in the blue patch and tor for the chromatic variables in the blue patch (best models for the 550–625 nm in the yellow patch). blue patch: lightness  sexþ SVL, AICc¼ 927.04, weight¼ 0.49; We analyzed the relationships among the chromatic variables, chroma  Acroeimeriaþ sexþ SVL, AICc¼186.55, weight¼ the morphological variables, and the presence of parasites using 0.28; hue  Acroeimeriaþ sexþ Acroeimeria*sex, AICc¼ 179.62, Akaike’s information criterion (AIC) to select the model with the weight¼ 0.22). The coefficients in our model-averaging procedure best fit (¼ with the lowest AIC, Burnham and Anderson 2004). suggested that the sex of the individuals was a significant predictor Furthermore, we performed model averaging using MuMIn (Barton for the lightness (relative importance ¼ 1.0, P< 0.001) and the hue 2013) and calculated the relative importance of each predictor sum- of the blue patch (relative importance ¼ 1.0, P< 0.001), whereas it ming the weights of all the models where the term appears. For that, was nearly significant in relation to the blue chroma (relative we considered sufficiently informative all the models with D AIC 2 importance¼ 0.68, P¼ 0.05). The blue patches of the males were (Burnham and Anderson 2004). In addition, we calculated the sig- significantly darker (the mean6 SE lightness for the blue patch was nificance of the coefficients for each predictor in the final models. 494.66 27.9 for the males and 1,154.66 61.6 for the females; For those predictors that were significant (<0.05), we calculated the F ¼ 126.09, P< 0.0001) and significantly more bluish (the 1, 66 maximum likelihood estimate and its standard error. Each chro- mean6 SE hue for the blue patch was 494.76 3.0 for the males and matic variable was independently tested in 2 sets of tests. First, we 535.86 9.3 for the females; F ¼ 27.41, P< 0.0001) compared 1, 66 ran the analyses for both males and females together. The sex and with those of females (Table 1). Thus, the blue patch was sexually the presence of Acroeimeria were fixed as factors. The SVL, BCI, dichromatic. In addition, the SVL was a significant predictor for and interaction sex*Acroeimeria were the independent predictors. lightness in the blue patch of males (relative importance ¼ 1.0, Second, we tested the relationships among the chromatic variables, P< 0.001; Pearson’s correlation: P< 0.0001, R ¼ 0.39). Larger the morphological variables, and the presence of parasites in males males had darker blue patches than smaller individuals (Table 2). and females separately. As we found Lankesterella in only 2 females, Among the females, none of the predictors explored here signifi- cantly explained the chromatic variables of the blue coloration. we tested for the effects of infection of the hemoparasite on males Although the sex of the individuals was included in the best models only. We tested differences in SVL and BCI between individuals of for all the chromatic variables in the yellow patch (best models for the both sexes with absence/presence of Acroeimeria with one-way yellow patch: lightness  Acroeimeriaþ BCIþ sexþ Acroeimeria*sex, ANOVA. AICc¼ 982.59, weight¼ 0.31; chroma  sexþ SVL, AICc¼289.62, weight¼ 0.27; hue  Acroeimeriaþ BCIþ sexþ Acroeimeria*sex, BCIc¼151.46, weight¼ 0.55), our model-averaging procedure sug- Results gested that neither sex nor the infection by Acroeimeria were impor- Parasites detected tant predictors for the chromatic variables of the yellow patch when We found parasites of the genus Acroeimeria in the feces and para- males and females are analyzed together because their coefficients were sites of the genus Lankesterella in the blood of the lizards (Megı ´a- not significant in the resulting averaged models (Table 1). Palma et al. 2015, 2017). No infection by malarial parasites was Nevertheless, the SVL of the lizards significantly predicted the chroma detected. We found a similar prevalence of Acroeimeria (33.8%) in (relative importance¼ 1.0, P< 0.001) and the hue (relative the sample (v ¼ 0.71). There were no differences between sexes importance¼ 1.0, P< 0.001) of the yellow patch in both sexes with 1, 68 in the prevalence of Acroeimeria: 31% (14/45) of the males and thesamesign (Table 2). Larger individuals had higher yellow chroma 39% (9/23) of the females were infected (v ¼ 0.3, P¼ 0.6). We and higher values of hue (i.e., orange) than smaller individuals 1, 68 found 30.8% (21/68) prevalence of Lankesterella in the sample. (Pearson’s correlation for chroma: P< 0.0001, R ¼ 0.27; and hue: P¼ 0.002, R ¼ 0.12; Figure 2). Furthermore, SVL was a significant However, only 2 females were infected and, therefore, the preva- predictor of the yellow lightness in males (relative importance¼ 0.78, lence was significantly higher in males (42.2%) than in females P< 0.01; Pearson’s correlation: P¼ 0.04, R ¼ 0.09). Larger males had (8%; v ¼ 7.7, P¼ 0.005). 1, 68 darker yellow patches (Figure 2). In addition, BCI was a significant predictor of the hue in the yellow patch of males (relative Parasites, body size, and body condition importance¼ 0.96, P< 0.01; Pearson’s correlation: P¼ 0.02, There were no differences in SVL among males or females with respect R ¼ 0.11). Males with better body condition had higher values of hue. to the presence/absence of Acroeimeria (differences of SVL in males: F ¼ 0.23, P¼ 0.63; difference of SVL in females: F ¼ 0.35, 1, 43 1, 21 Parasite infection and coloration P¼ 0.55. In contrast, the males infected by Lankesterella were signifi- Our model-selection procedure suggested that the infection by the cantly larger (mean SVL6 SE¼ 61.76 1.0 mm) than the uninfected intestinal parasites of the genus Acroeimeria was a good predictor for ones (mean SVL6 SE¼ 57.76 1.4 mm; F ¼ 4.78, P¼ 0.03). 1, 43 coloration when males and females were analyzed separated. The indi- Significant differences were present neither in BCI between infected vidual models for the chromatic variables of both sexes (Table 2)sug- and uninfected males with respect to Acroeimeria, nor in males (F 1, 42 gested that infection by Acroeimeria was a significant predictor of the ¼ 0.09, P¼ 0.75) or in females (F ¼ 0.18, P¼ 0.66). Neither were 1, 20 chroma in the blue patches of the males (best models for the blue patch the differences in BCI significant with respect to Lankesterella (F of the males: blue chroma  Acroeimeria,AICc¼116.58, 1, ¼ 1.55, P¼ 0.21). weight¼ 0.42, coefficient for Acroeimeria ¼ 0.96) and the hue in the Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Megı´a-Palma et al.  Sexual coloration and parasites 5 Table 1. Akaike analyses of the chromatic variables for males and females together and summarized by model-averaging procedure Blue: L SE Blue: C SE Blue: H SE Yellow: L SE Yellow: C SE Yellow: H SE n (D AIC 2) 32 42 5 2 N 43 45 5 5 TOTAL_V Importance Sex ***1.00 *0.68 ***1.00 0.93 *1.00 0.57 SVL ***1.00 0.25 0.48 **0.82 ***1.00 ***1.00 BCI 0.19 0.22 0.18 **0.79 0.40 ***1.00 Acroeimeria 0.32 **0.90 0.43 0.56 0.51 0.56 Sex*Acroeimeria 0.09 **0.50 *0.29 **0.44 *0.38 ***0.46 Estimates Sex 619.65 58.52 43.27 10.27 SVL 215.01 4.33 214.33 6.53 <0.01 <0.001 1.25 0.36 BCI 21363.65 634.72 112.47 35.89 Acroeimeria 20.04 0.02 Sex*Acroeimeria 0.06 0.03 371.94 168.45 225.72 9.47 Notes: n (D AIC 2)¼ number of probable models with D AIC 2. N ¼ total number of variables included in the models with D AIC 2. TOTAL_V Importance ¼ relative weight of the variables in the resulting averaged model. In the row “importance,” values shown in bold indicate the coefficients of the maxi- mum likelihood estimates that are significant with level of significance: *P¼ 0.05, **P< 0.01, ***P< 0.001. In the row “estimates,” we show the slope of the coefficients and their standard error. L, C, and H are lightness, chroma, and hue, respectively. Table 2. Akaike analyses of the chromatic variables for males and females separated and summarized by model-averaging procedure Males Blue: L SE Blue: C SE Blue: H SE Yellow: L SE Yellow: C SE Yellow: H SE n (D AIC 2) 226 7 4 4 N 223 4 4 3 TOTAL_V Importance SVL ***1.00 0.21 0.22 **0.78 ***1.00 **0.68 BCI 0.19 0.21 0.64 0.38 *0.66 **0.96 Acroeimeria 0.19 ***0.96 0.58 *0.67 *0.66 0.53 Lankesterella *0.57 0.25 0.30 0.43 0.29 0.25 Estimates SVL 217.25 3.72 215.13 7.23 <0.01 <0.001 0.92 0.45 BCI 130.01 49.51 Acroeimeria 20.05 0.02 Lankesterella Females Blue: L SE Blue: C SE Blue: H Yellow: L SE Yellow: C SE Yellow: H SE n (D AIC 2) 334 3 1 2 N 223 2 1 3 TOTAL_V Importance SVL 0.16 0.50 0.39 0.15 **0.81 ***1.00 BCI 0.30 0.24 0.20 *0.63 0.20 0.19 Acroeimeria 0.24 0.17 0.24 0.30 0.16 **1.00 Estimates SVL <0.01 0.001 2.99 0.58 BCI Acroeimeria 216.15 6.02 Notes: n (D AIC 2)¼ number of probable models with D AIC 2. N ¼ total number of variables included in the models with D AIC 2. TOTAL_V Importance ¼ relative weight of the variables in the resulting averaged model. In the row “importance,” values shown in bold indicate the coefficients of the maxi- mum likelihood estimates that are significant with level of significance: *P¼ 0.05, **P< 0.01, ***P< 0.001. In the row “estimates,” we show the slope of the coefficients and their standard error. L, C, and H are lightness, chroma, and hue, respectively. yellow patches of the females (yellow hue  Acroeimeriaþ SVL, Males and females infected by intestinal parasites of the genus AICc¼40.57, weight¼ 0.47, coefficient for Acroeimeria¼ 1.00). Acroeimeria expressed lower coloration as predicted by the H–Z The males infected with parasites of the genus Acroeimeria had blue hypothesis, although the differences observed in the females were patches with significantly less chroma (mean6 SE¼ 23.26 0.01) than not significant. The infected males expressed blue patches with a the uninfected males (mean6 SE¼ 28.76 0.01; F ¼ 7.31, mean 5.5% less chroma than the blue patch of the uninfected males. 1, 43 P¼ 0.009; Figure 1A); meanwhile, the females that were infected by Hormonal differences between infected and uninfected males might Acroeimeria expressed yellow patches that had lower values of hue explain the chromatic differences observed in the blue patch. In this (yellow-like patches: mean6 SE¼ 629.46 7.5) than the uninfected sense, reduction of testosterone level by castration of male S. jarrovi females (orange-like patches: mean6 SE¼ 641.46 6.6), but this differ- induced a significant reduction in chroma in the blue coloration ence was not significant (F ¼ 1.77, P¼ 0.19; Figure 1B). 1, 21 (Cox et al. 2008). Similarly to the castrated males in the study of Cox et al. (2008), male S. occidentalis that were infected by Acroeimeria expressed blue patches with low chroma. Castrated Discussion male S. jarrovi reduced their territorial and sexual behavior (Moore We found partial evidence supporting the parasite hypothesis 1987), and malarial parasites have similar effects in S. occidentalis (Hamilton and Zuk 1982) in this population of S. occidentalis. (Dunlap and Schall 1995) because they hinder their ability to Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 6 Current Zoology, 2018, Vol. 0, No. 0 Figure 2. Relationship between the SVL and the chromatic variables of the blue (A) and the yellow (B, C, and D) patches. In each of the analyses, the sex analyzed is shown in the bottom-left corner. compete for females or to actively patrol their home ranges (Schall in the blue patch could be related to sexual differences in testoster- and Dearing 1987; Schall and Houle 1992). Eimeriid parasites of one secretion because this hormone influences dimorphism in immu- strict intestinal life cycle, such as the genus Acroeimeria, are largely nocompetence in lizards (e.g., Mondal and Rai 1999) and, further, known to cause multiple diseases—and even death—in livestock and is responsible for sexual dichromatism in Sceloporus (Cox et al. wild fauna (Coudert et al. 1993; Blake and Tomley 2014). Similarly 2005, 2008; Calisi and Hews 2007). Testosterone increases the to males infected by malarial parasites, the presence of low chroma expression of the blue coloration in males of Sceloporus that may be in the blue patches of the males infected by Acroeimeria suggested important in S. occidentalis because this coloration is displayed that the infection might have a negative effect on the fitness of the toward competitors at short distance, reduces aggressive escalation male lizards in this population. during fights, and is used by conspecific for sex discrimination Besides the relationships found between the blue coloration of (Cooper and Burns 1987; Sheldahl and Martins 2000). However, the males with respect to the infection by Acroeimeria, we found the production of testosterone reduces both macrophage production low statistical evidence that supports any relationship of the infec- and the inflammatory response in male lizards (Mondal and Rai tion by Lankesterella with the expression of the color patches meas- 1999; Belliure et al. 2004). In addition, it may augment the meta- ured. Interestingly, hemoparasites of the genus Lankesterella bolic rate (e.g., Feuerbacher and Prinzinger 1981), increasing the infected almost exclusively males that, additionally, were larger oxidative stress and the cellular damage in the individuals (von than the uninfected ones. Larger males expressed darker blue Schantz et al. 1999). At the same time, oxidative stress can impair patches (i.e., less lightness) than uninfected males and, moreover, as immune functions (Alonso-Alvarez et al. 2007), and renders males previously commented, had darker yellow patches, with high more susceptible to parasitic infections (Mondal and Rai 1999). chroma and high hue. Langkilde and Boronow (2010) found that In addition to the relationships achieved between the parasitic larger males of the closely related species, S. undulatus, had darker infections and the coloration and morphology of the male lizards, blue patches than smaller males, suggesting that the coloration we found a strong effect of SVL on the chromatic variables of the might shift ontogenetically and, thus, larger males of S. occidentalis yellow coloration, with the same sign in both males and females. with intense coloration might be older. There are few reported cases Large males expressed orange-like (high values of hue) yellow of Lankesterella parasites in reptiles (Telford 2008), although its patches (also explained by BCI), which had more chroma and were presence may be more common than previously thought (e.g., Maia darker than those of smaller males. Similarly, large females et al. 2016; Megı ´a-Palma et al. 2017b). To our knowledge, only 1 expressed orange-like yellow patches with more chroma than study describes a negative effect of Lankesterella parasites causing smaller females. Thus, it seems to be a non-dichromatic patch that pneumonia in avian hosts (Speer et al. 1997). In S. occidentalis,we might have similar signaling function irrespective of the sex of the found low intensities of infection (i.e., mean parasite load/15,000 bearer. The Western Fence Lizard is considered a territorial lizard cells6 SE ¼ 4.66 1.1, max¼ 40) in comparison to other studies of species because both sexes show high site fidelity and defend their Old World lizards (e.g., Megı ´a-Palma et al. 2014 found a mean load home ranges (Sheldahl and Martins 2000). One of its most frequent of Lankesterella in 10,000 cells¼ 27.8, with max¼ 115 in behaviors is a series of short push-ups that they display to potential Acanthodactylus erythrurus). This might mean that, in this popula- mates or rivals from the distance (e.g., Schall and Houle 1992; tion it is important to maintain infections by Lankesterella under Sheldhal and Martins 2000). During this display, individuals may low thresholds because only high-quality individuals can tolerate it increase the visibility of the yellow patches of the forelimbs that or, alternatively, it might suggest a low virulence of this hemopara- might inform to conspecifics on their body size. The body size of the site (sensu Svensson and Ra ˚ berg 2010). In addition, the sexual dif- ferences in infection by Lankesterella and the sexual dichromatism individuals correlates with the female’s fecundity in the genus Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Megı´a-Palma et al.  Sexual coloration and parasites 7 Belliure J, Smith L, Sorci G, 2004. Effect of testosterone on T cell-mediated Sceloporus (Jime ´ nez-Arcos et al. 2017) and with fighting ability in immunity in two species of Mediterranean lacertid lizards. J Exp Zool Part lizards in general (Carpenter 1995; Molina-Borja et al. 1998). A 301:411–418. Based on the current knowledge of the high visual sensitivity of Blake DP, Tomley FM, 2014. Securing poultry production from the the visual system in closely related lizards of the family Iguanidae ever-present Eimeria challenge. Trends Parasitol 30:12–19. (i.e., Loew et al. 2002), we may speculate on the perceptual capacity Bonorris JS, Ball GH, 1955. Schellackia occidentalis n. sp., a blood-inhabiting of S. occidentalis to discriminate the chromatic characteristics of coccidian found in lizards in Southern California. J Protozool 2:31–34. conspecifics. Unfortunately, our spectral data did not include the Burnham KP, Anderson DR, 2004. Multimodel inference, understanding AIC UV range, although probably not being relevant in the color patches and BIC in model selection. Soc Methods Res 33:261–304. of Sceloporus (Stoehr and McGraw 2001), it precludes the applica- Calisi RM, Hews D, 2007. Steroid correlates of multiple color traits in the tion of tetrachromatic visual models in this study and, therefore, the spiny lizard Sceloporus pyrocephalus. J Comp Physiol B 177:641–654. consecution of stronger conclusions. We can only speculate whether Carpenter GC, 1995. Modeling dominance: the influence of size, coloration, these differences could be discriminated by conspecifics. It seems and experience on dominance relations in tree lizards Urosaurus ornatus. Herpetol Monogr 9:88–101. reasonable that the visual system of lizards co-evolves with the Clark GW, 1970. Eimeria ahtanumensis n. sp. from the northwestern fence liz- subtle variation of the coloration of conspecifics (Stoehr and ard Sceloporus occidentalis in central Washington. J Protozool 17:526–530. McGraw 2001), especially if those could transmit Acroeimeria.A Cooper WE, Jr, Burns N, 1987. Social significance of ventrolateral coloration proper discrimination between infected and uninfected potential in the fence lizard Sceloporus undulatus. Anim Behav 35:526–532. mates may be important for these lizards to decrease the probability Cooper WE, Jr, Crews D, 1987. Sexual coloration, plasma concentration of of infection whereas increasing the resistance to this parasite in the sex steroid hormones, and responses to courtship in the female keeled earless population. lizard Holbrookia propinqua. Horm Behav 22:12–25. In conclusion, we found partial support for the parasite hypothe- Coudert P, Licois D, Provot F, Drouet-Viard F, 1993. Eimeria sp. from the sis (Hamilton and Zuk 1982)in S. occidentalis because lizards rabbit Oryctolagus cuniculus: pathogenicity and immunogenicity of infected with parasites of the genus Acroeimeria expressed duller Eimeria intestinalis. Parasitol Res 79:186–190. colorations than the uninfected individuals. Although parasites Cox RM, Skelly SL, Leo A, John-Alder HB, 2005. Testosterone regulates sexu- ally dimorphic coloration in the Eastern Fence Lizard, Sceloporus undula- might mediate the sexual selection of this species (e.g., Schall and tus. Copeia 2005:597–608. Dearing 1987; Schall and Houle 1992), the Lankesterella–lizard Cox RM, Zilberman V, John-Alder HB, 2008. Testosterone stimulates the host system studied here did not support the H–Z hypothesis expression of a social color signal in the Yarrows Spiny Lizard, Sceloporus because infected males were bigger and more intensely colored than jarrovii. J Exp Zool 309A:505–514. the uninfected ones. Cuervo JJ, Belliure J, Negro JJ, 2016. Coloration reflects skin pterin concentra- tion in a red-tailed lizard. Comp Biochem Phys B 193:17–24. del Cerro S, Merino S, Martı´nez-de la Puente J, Lobato E, Ruiz-de-Castaneda ~ Acknowledgments et al., 2010. Carotenoid-based plumage colouration is associated with blood We want to thank the staff in the Arboretum of the Campus of Santa Cruz, parasite richness and stress protein levels in blue tits Cyanistes caeruleus. CA, for providing logistic support and K. Paulling, N. Bunn, and C. Wertin Oecologia 162:825–835. who contributed to collecting the lizards and doing the color measurements. Dı ´az JA, 1993. Breeding coloration, mating opportunities, activity, and survival in the lacertid lizard Psammodromus algirus. Can J Zool 71:1104–1110. Duneau D, Ebert D, 2006. Host sexual dimorphism and parasite adaptation. Funding PLoS Biol 10:e1001271. Financial support was provided by Spanish Ministerio de Economı´a y Dunlap KD, Mathies T, 1993. Effects of nymphal ticks and their interactions Competitividad (projects CGL2012-40026-C02-01 and CGL2015-67789- with malaria on the physiology of male fence lizards. Copeia 4:1045–1048. C2-1-P (MINECO/FEDER) to SM, and CGL2012-40026-C02-02 to JM, and Dunlap KD, Schall JJ, 1995. Hormonal alterations and reproductive inhibition grant numbers BES-2010-038427 and EEBB-I-14-08326 to RM-P). in male fence lizards Sceloporus occidentalis infected with the malarial para- Ministerio de Educacio ´ n funded SR with FPU grant number AP-2009-1325 site Plasmodium mexicanum. Physiol Zool 68:608–621. and EST13/00196. Permits for carrying out this investigation and collecting Duszynski DW, Wilber PG, 1997. A guideline for the preparation of species lizards were provided by the UCSC ethics committee (IACUC) and CDFG to descriptions in the Eimeriidae. J Parasitol 83:333–336. RDC. Research at the UCSC was supported by an NSF grant to BS (EF- Endler JA, 1990. On the measurement and classification of colour in studies of 1241848). animal colour patterns. Biol J Linn Soc 41:315–352. Feuerbacher I, Prinzinger R, 1981. The effects of the male sex-hormone testos- terone on body temperature and energy metabolism in male Japanese quail References Coturnix coturnix japonica. Comp Biochem Physiol 70A:247–250. ´ Grill CP, Rush VN, 2000. Analysing spectral data: comparison and applica- Abalos J, Pe ´ rez I de Lanuza G, Carazo P, Font E, 2016. The role of male colo- tion of two techniques. Biol J Linn Soc 69:121–138. ration in the outcome of staged contests in the European common wall liz- Haisten DC, Paranjpe D, Loveridge S, Sinervo B, 2015. The cellular basis of ard Podarcis muralis. Behaviour. doi: 10.1163/1568539X–00003366. polymorphic coloration in common side-blotched lizards Uta stansburiana. Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G, 2007. Herpetologica 71:125–135. Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc Hamilton WD, Zuk M, 1982. Heritable true fitness and bright birds: a role for R Soc B 274:819–825. parasites? Science 218:384–387. Barton K, 2013. MuMIn: Multi-model inference. R package, version1.40.0. Ho ¨ rak P, Ots I, Vellau H, Spottiswoo C, Møller AP, 2001. Carotenoid-based Bajer K, Molna ´ r O, To¨ro ¨ k J, Herczeg G, 2010. Female European green lizards plumage coloration reflects hemoparasite infection and local survival in Lacerta viridis prefer males with high ultraviolet throat reflectance. Behav breeding great tits. Oecologia 126:166–173. Ecol Sociobiol 64:2007–2014. Houde AE, Torio AJ, 1992. Effect of parasitic infection on male color pattern Balenger SL, Zuk M, 2014. Testing the Hamilton-Zuk hypothesis: past, present, and future. Int Comp Biol 54:601–613. and female choice in guppies. Behav Ecol 3:346–351. Bell EL, Price AH, 1996. Sceloporus occidentalis. Catalogue of American Jime ´ nez-Arcos VH, Sanabria-Urba ´ n S, Cueva del Castillo R, 2017. The inter- Amphibians and Reptiles (CAAR) 631:1–17. play between natural and sexual selection in the evolution of sexual size Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 8 Current Zoology, 2018, Vol. 0, No. 0 dimorphism in Sceloporus lizards (Squamata: phrynosomatidae). Ecol Evol Montgomerie R, 2009. CLR, version 1.1. Queen’s University, 7:905–917. Kingston, Canada. Available from http://post.queensu.ca/mont/color/ana Langkilde T, Boronow KE, 2010. Color as a signal: the relationship between lyze.html. coloration and morphology in male Eastern fence lizards, Sceloporus undu- Moore MC, 1987. Castration affects territorial and sexual behaviour of latus. J Herpetol 44:261–271. free-living lizards Sceloporus jarrovi. Anim Behav 35:1193–1199. Langkilde T, Boronow KE, 2012. Hot boys are blue: temperature-dependent Morrison RL, Rand MS, Frost-Mason SK, 1995. Cellular basis of color differ- color change in male Eastern Fence Lizards. J Herpetol 46:461–465. ences in three morphs of the lizard Sceloporus undulatus erythrocheilus. Llanos-Garrido A, Dı ´az JA, Pe ´ rez-Rodrı´guez A, Arriero E, 2017. Variation in Copeia 1995:397–408. male ornaments in two lizard populations with contrasting parasite loads. Ressel S, Schall JJ, 1989. Parasites and showy males: malarial infection and J Zool. doi: 10.1111/jzo.12478. color variation in fence lizards. Oecologia 78:158–164. Loew ER, Fleishman LJ, Foster RG, Provencio I, 2002. Visual pigments and Salvador A, Veiga JP, 2001. Male traits and pairing success in the lizards oil droplets in diurnal lizards: a comparative study of Caribbean anoles. Psammodromus algirus. Herpetologica 57:77–86. J Exp Biol 205:927–938. Schall JJ, Dearing MD, 1987. Malarial parasitism and male competition for Maia JP, Harris DJ, Carranza S, Go ´ mez-Dı´az E, 2016. Assessing the diversity, mates in the western fence lizard Sceloporus occidentalis. Oecologia 73: host-specificity and infection patterns of apicomplexan parasites in reptiles 389–392. from Oman, Arabia. Parasitology 143:1730–1747. Schall JJ, Houle PR, 1992. Malarial parasitism and home range and social sta- Martı´n J, Lo ´ pez P, 2009. Multiple color signals may reveal multiple messages tus of male western fence lizards Sceloporus occidentalis. J Herpetol 26: in male Schreiber’s green lizards Lacerta schreiberi. Behav Ecol Sociobiol 74–76. 63:1743–1755. Sheldahl LA, Martins EP, 2000. The territorial behavior of the western fence Martı´nez-de la Puente J, Merino S, Toma ´ s G, Moreno J, Morales J et al., lizard Sceloporus occidentalis. Herpetologica 56:469–479. 2010. The blood parasite Haemoproteus reduces survival in a wild bird: a Skarstein F, Folstad I, 1996. Sexual dichromatism and the immunocompetence medication experiment. Biol Lett 6:663–665. handicap: an observational approach using the Arctic charr. Oikos 76: Martı´nez-Padilla J, Mougeot F, Pe ´ rez-Rodrı´guez L, Bortolotti GR, 2007. 359–367. Nematode parasites reduce carotenoid-based signalling in male red grouse. Smith IC, John-Alder HB, 1999. Seasonal specificity of hormonal, behavioral, Biol Lett 3:161–164. and coloration responses to within- and between-sex encounters in male liz- Martins EP, 1993. Contextual use of the push-up display by the sagebrush liz- ards Sceloporus undulatus. Horm Behav 36:39–52. ards Sceloporus graciosus. Anim Behav 45:25–36. Speer CA, Baker DG, Yamaguchi A, Dubey JP, 1997. Ultrastructural charac- Megı´a-Palma R, Mart´nez ı J, Acevedo I, Martı´n J, Garcı´a-Roa R et al., 2015. teristics of a Lankesterella-like coccidian causing pneumonia in a northern Phylogeny of the reptilian Eimeria: are Choleoeimeria and Acroeimeria cardinal Carduelis cardinalis. Acta Protozool 36:39–47. valid generic names? Zool Scr 44:684–692. Stebbins RC, McGinnis SM, 2012. Field Guide to Amphibians and Reptiles of Megı´a-Palma R, Mart´nez ı J, Merino S, 2013. Phylogenetic analysis based on California: California Natural History Guides Revised Edition. Berkeley 18S rRNA gene sequences of Schellackia parasites (Apicomplexa: lankester- and Los Angeles: University of California Press. ellidae) reveals their close relationship to the genus Eimeria. Parasitology Stoehr AM, McGraw KJ, 2001. Ultraviolet reflectance of color patches in male 140:1149–1157. Sceloporus undulatus and Anolis carolinensis. J Herpetol 35:168–171. Megı´a-Palma R, Martı ´nez J, Merino S, 2014. Molecular characterization of Svensson EI, McAdam AG, Sinervo B, 2009. Intralocus sexual conflict over hemococcidia genus Schellackia (Apicomplexa) reveals the polyphyletic ori- immune defense and the resolution of gender load in a natural lizard popula- gin of the family Lankesterellidae. Zool Scr 43:304–312. tion. Evolution 63:3124–3135. Megı´a-Palma R, Martı´nez J, Merino S, 2016a. Structural- and Svensson EI, Ra ˚ berg L, 2010. Resistance and tolerance in animal carotenoid-based throat color patches in males of Lacerta schreiberi reflect enemy-victim coevolution. Trends Ecol Evol 25:267–274. different parasitic diseases. Behav Ecol Sociobiol 70:2017–2025. Swierk L, Langkilde T, 2013. Bearded ladies: females suffer fitness consequen- Megı´a-Palma R, Martı´nez J, Merino S, 2016b. A structural colour ornament ces when bearing male traits. Biol Lett 9:20130644. correlates positively with parasite load and body condition in an insular liz- Telford SRJr, 2008. Hemoparasites of the Reptilia: Color Atlas and Text. Boca ard species. Naturwissenschaften 103:1–10. Raton (FL): CRC Press. Megı´a-Palma R, Martı´nez J, Merino S, 2017a. Manipulation of parasite load Thompson CW, Hillgarth N, Leu M, McClure HE, 1997. High parasite load induces significant changes in the structural-based throat color of male in house finches Carpodacus mexicanus is correlated with reduced expres- Iberian green lizards. Curr Zool. doi: 10.1093/cz/zox036. sion of a sexually selected trait. Am Nat 149:270–294. Megı´a-Palma R, Martı ´nez J, Paranjpe D, D’amico V, Aguilar R et al., 2017b. Va ´ clav R, Prokop P, Fekia c V, 2007. Expression of breeding colouration in Phylogenetic analyses reveal that Schellackia parasites (Apicomplexa) European green lizards Lacerta viridis: variation with morphology and tick detected in American lizards are closely related to genus Lankesterella:is infestation. Can J Zool 85:1199–1206. the range of Schellackia restricted to Old World? Par Vec 10:470. von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H, 1999. Good Merila ¨ J, Sheldon BC, Lindstro ¨ m K, 1999. Plumage brightness in relation to genes, oxidative stress and condition-dependent sexual signals. Proc R Soc haematozoan infections in the greenfinch Carduelis chloris: bright males are B 266:1–12. a good bet. Ecoscience 6:12–18. Ward PI, 1988. Sexual dichromatism and parasitism in British and Irish fresh- Merino S, Moreno J, Sanz JJ, Arriero E, 2000. Are avian blood parasites water fish. Anim Behav 36:1210–1215. pathogenic in the wild? A medication experiment in blue tits Parus caeru- Weiss SL, 2002. Reproductive signals of female lizards: pattern of trait expres- leus. Proc R Soc B 267:2507–2510. sion and male response. Ethology 108:793–813. Molina-Borja M, Padro ´ n-Fumero M, Alfonso-Martı´n T, 1998. Morphological Weiss SL, Foerster K, Hudon J, 2012. Pteridine, not carotenoid, pigments and behavioural traits affecting the intensity and outcome of male contests underlie the female-specific orange ornament of striped plateau lizards in Gallotia galloti galloti (Family Lacertidae). Ethology 104:314–322. Sceloporus virgatus. Comp Biochem Phys B 161:117–123. Mondal S, Rai U, 1999. Sexual dimorphism in phagocytic activity of wall liz- Worden BD, Parker PG, Pappas PW, 2000. Parasites reduce ard’s splenic macrophages and its control by sex steroids. Gen Comp attractiveness and reproductive success in male grain beetles. Anim Behav Endocr 116:291–298. 59:543–550. Montgomerie R, 2006. Quantifying colors. In: Hill GE, McGraw KJ, editors. Zuk M, 1988. Parasite load, body size, and age of wild-caught male field crick- Bird Coloration, Vol 1. Mechanism and Measurements. Cambridge: ets (Orthoptera: gryllidae): effects on sexual selection. Evolution 42: Harvard University Press, 41–89. 969–976. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Megı´a-Palma et al.  Sexual coloration and parasites 9 Appendix A Yellow patch Blue patch 400 400 500 500 600 600 7 700 00 Wavelength (nm) CD Yellow patch Blue patch 400 500 600 700 Wavelength (nm) Figure A1. Ventral coloration and mean6 SE spectral profiles of both yellow and blue patches of female (A, B) and male (C, D) Sceloporus occidentalis bocourtii. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Reflectance (%) Reflectance (%) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Current Zoology Oxford University Press

Multiple color patches and parasites in Sceloporus occidentalis: differential relationships by sex and infection

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Abstract

Parasites generally have a negative influence on the color expression of their hosts. Sexual selec- tion theory predicts resistant high-quality individuals should show intense coloration, whereas sus- ceptible low-quality individuals would show poor coloration. However, intensely colored males of different species of Old and New World lizards were more often infected by hemoparasites. These results suggest that high-quality males, with intense coloration, would suffer higher susceptibility to hemoparasites. This hypothesis remains poorly understood and contradicts general theories on sexual selection. We surveyed a population of Sceloporus occidentalis for parasites and found infections by the parasite genera Lankesterella and Acroeimeria. In this population, both males and females express ventral blue and yellow color patches. Lankesterella was almost exclusively infect- ing males. The body size of the males significantly predicted the coloration of both blue and yellow patches. Larger males showed darker (lower lightness) blue ventral patches and more saturated yellow patches that were also orange-skewed. Moreover, these males were more often infected by Lankesterella than smaller males. The intestinal parasite Acroeimeria infected both males and females. The infection by intestinal parasites of the genus Acroeimeria was the best predictor for the chroma in the blue patch of the males and for hue in the yellow patch of the females. Those males infected by Acroeimeria expressed blue patches with significantly lower chroma than the uninfected males. However, the hue of the yellow patch was not significantly different between infected and uninfected females. These results suggest a different effect of Lankesterella and Acroeimeria on the lizards. On the one hand, the intense coloration of male lizards infected by Lankesterella suggested high-quality male lizards may tolerate it. On the other hand, the low chroma of the blue coloration of the infected males suggested that this coloration could honestly express the infection by Acroeimeria. Key words: animal communication, coloration, Hamilton and Zuk, parasites, sexual selection. V C The Author(s) (2018). Published by Oxford University Press. 1 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/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 2 Current Zoology, 2018, Vol. 0, No. 0 In 1982, Hamilton and Zuk proposed a co-evolutionary mechanism yellow coloration of lizards in the genus Sceloporus in relation to to explain how sexual selection favors resistance against parasitic the infection by 2 closely related hematic and intestinal parasites in diseases in nature: The parasite hypothesis (Hamilton and Zuk a population where both males and females express color patches. 1982). This Hamilton–Zuk (H–Z) hypothesis predicts a negative The aim of the study was to test whether the different color patches relationship between the expression of the host’s secondary sexual in males and females reflect information on these parasitic infections characters and the degree of its parasitic infections (Balenger and and also whether the observed relationships have a negative sign as Zuk 2014). Thus, sexual selection favors resistance against parasites expected by the H–Z hypothesis. Considering previous results of the because individuals would mate with highly ornamented individuals parasite hypothesis from studies of lizards, we predicted that males (Hamilton and Zuk 1982). Evidence supporting the parasites with more intense coloration will be infected by hemoparasites. hypothesis (Hamilton and Zuk 1982) exists for insects (Zuk 1988; However, we might expect a negative relationship between the Worden et al. 2000), fish (Ward 1988; Houde and Torio 1992), and male’s color expression and the infection by intestinal parasites. In birds (Merila ¨ et al. 1999; Ho ¨ rak et al. 2001; del Cerro et al. 2010). addition, we expect different relationships of parasitic infections, In all these host–parasite systems, the infected individuals usually with color expression depending on the sex of the host. show poor breeding coloration (Thompson et al. 1997; Martı ´nez- Padilla et al. 2007, but see also Skarstein and Folstad 1996) and suf- Material and Methods fer reduced survival (Merino et al. 2000; Martı ´nez-de la Puente et al. 2010). However, studies of both Old and New World lizards The host model have produced mixed results. On the one hand, studies investigating Sceloporus occidentalis (Squamata: Phrynosomatidae) is usually the relationships between the expression of the breeding coloration described as sexually dimorphic. Adult males express blue ventral and the infection by ticks or nematodes in lizards suggest that these patches, whereas females typically show gray bellies (e.g., Stebbins parasites negatively affect the expression of breeding coloration in and McGinnis 2012). However, in some populations of this lizard male lizards (Va ´ clav et al. 2007; Megı ´a-Palma et al. 2016a, 2017a; species, both sexes present ventral blue patches (Bell and Price Llanos-Garrido et al. 2017). On the other hand, studies considering 1996). In a closely related species, S. jarrovi, patches of males had chronic infections produced by hematic parasites contradict pre- reduced lightness, greater saturation and a higher angular hue (i.e., vious results and, therefore, the parasite hypothesis. In these studies, were more bluish) than ventral patches of females (Cox et al. 2008). male lizard hosts with more hematic parasites usually have more In addition to the blue coloration, S. occidentalis has yellow patches intense colorations (Ressel and Schall 1989; Megı ´a-Palma et al. on their forelimbs that are fundamentally based on pterins in lizards 2016a, 2016b). Similarly as it occurs in birds, coloration in New of the family Phrynosomatidae (Morrison et al. 1995; Weiss et al. and Old World lizards reflect individual quality, and males with 2012; Haisten et al. 2015). The function of pterine-based coloration more intense colors may be of better quality because they are usually as a potential intraspecific signal has been documented in female liz- bigger, keep larger home ranges, and have better mating success ards of the genus Sceloporus (Weiss 2002; Weiss et al. 2012). than paler individuals (Dı ´az 1993; Salvador and Veiga 2001; However, there is little evidence for its function in male lizards of Langkilde and Boronow 2010). Thus, the importance of the parasite this genus where, on the contrary, blue coloration seems to have hypothesis to sexually dimorphic coloration remains poorly under- received a major attention (e.g., Cooper and Burns 1987; Martins stood in lizards. 1993; Smith and John-Alder 1999). The presence of multiple color Visual communication is important in lizards and plays a key patches in males and females in some populations of S. occidentalis role in male intrasexual selection (Bajer et al. 2010; Abalos et al. makes this species a good model to test whether variation in social 2016). Dominant males have intense colors (Martı ´n and Lo ´ pez coloration in lizards of both sexes could reflect chronic parasitic 2009), and females might also prefer these intensely colored males infections as expected by the H–Z hypothesis. Several intestinal and (Salvador and Veiga 2001). However, costs and benefits of colora- hematic parasite genera were described as infecting S. occidentalis tion may differ between sexes (Svensson et al. 2009; Swierk (Bonorris and Ball 1955; Clark 1970; Ressel and Schall 1989). and Langkilde 2013). In New World lizards of the family Recently, we molecularly characterized the blood and the intestinal Phrynosomatidae, males use the coloration of conspecifics for sex parasites found in the population of S. occidentalis that we will discrimination (Cooper and Burns 1987). Indeed, in some popula- study here and we classified them, respectively, in the genera tions where males and some females show similar colorations, those Lankesterella (Eimeriorina: Lankesterellidae) and Acroeimeria females that have male-like coloration suffer reduced fitness because (Eimeriorina: Eimeriidae) (Megı ´a-Palma et al. 2015, 2017b). The males invest more time courting females with female-like pheno- intestinal parasites, genus Acroeimeria, that infect S. occidentalis types (Swierk and Langkilde 2013). That said, selection may also act undergo direct horizontal transmission among hosts without the on female coloration if it varies with reproductive status and may intervention of a vector. In contrast, hemoparasites of the genus serve to either attract or dissuade potential mates (Cooper and Lankesterella are transmitted by hematophagous arthropods. All of Crews 1988). these endoparasites undergo reproduction in internal organs of the Parasites can affect males and females differently owing to sexual host and break down the host’s tissues with every reproductive differences in behavior or hormone levels (Duneau and Ebert 2006). cycle, causing negative effects (Telford 2008). Thus, given these or other sexual differences in life-history traits, we might also expect sexual differences in the level or the sign of the Sampling methods relationship between the degree of infection and the color expres- We collected 68 S. occidentalis bocourtii (45 males and 23 females) sion, even in cases where both sexes show similar ornaments (e.g., in May 2014, corresponding to the breeding season of this species. Megı ´a-Palma et al. 2016 b). Thus, studying species where both sexes show color patches offers a good opportunity to investigate sexual Lizards were captured in a linear transect of 400 m (from differences in the expression of shared traits in relation to parasitic 36.985270, 122.061440 to 36.985287, 122.056934) on the infections. Here, we analyzed the spectral reflectance of blue and campus of the University of California, Santa Cruz, CA (UCSC). Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Megı´a-Palma et al.  Sexual coloration and parasites 3 Each lizard was individually identified using a xylene-free marker with a blue number that was written in the gray area of the belly out of the color patches as examples in the Appendix. The lizards were transported in a cooler to the lab in the UCSC facilities to perform all the color measurement under standardized light conditions (see below). Snout-to-vent length (SVL) for each lizard was measured with a ruler to the nearest millimeter and the individuals were weighed to the nearest centigram with a digital balance (Scout Pro SP202, Ohaus Corp., NJ, USA). A body condition index (BCI) was calculated as the residuals of the regression of log mass on log SVL (Dunlap and Mathies 1993). The sex of the individuals was deter- mined by the presence of enlarged post-anal scales (Cox et al. 2005; Langkilde and Boronow 2012). No lizard died during the study, and all were released at their site of capture following data collection. Screening of blood smears for parasites Blood samples were collected from the base of the tail of each lizard using sterilized needles (Megı ´a-Palma et al. 2013, 2014). In the case of male lizards, blood was collected by carefully avoiding the area of the hemipenis (by bleeding the tail at least 2 cm from the cloaca). The drop of blood obtained by this method was collected with a heparinized microcapillary tube (BRAND, 75 1.1 mm, Na- heparinized). These blood samples were used to make thin-layer blood smears. The dried blood smears were fixed with methanol Figure 1. (A) Comparison of the mean6 SE spectra of the blue patches of and stained for 40 min with Giemsa 1:10 at pH 7.2. The same per- males taking in consideration infection by parasites of the genus son (RMP) screened 15,000 red blood cells of each individual lizard Acroeimeria. (B) Comparison of mean6 SE spectra of the yellow patches of females considering infection by the same parasite. at 1,000 magnification (Megı ´a-Palma et al. 2017b) for diagnosing the presence of parasites in the blood of the lizards. (Ocean Optics Inc., Dunedin, FL, USA). The light source used was a deuterium–tungsten light (MINI DT1000A-112; Analytical Screening of fecal samples Instruments System, Inc., Ringoes, NJ, USA). We used an integra- Fecal samples were collected directly into 1.5-mL micro-centrifuge tion time of 10 ms, a boxcar width of 5, and 10 averaged readings tubes by briefly massaging the belly of the lizards (e.g., Megı ´a- per spectrum. In a darkened room, we measured the reflectance Palma et al. 2016a). These fecal samples were stored in 1 mL potas- from the color patches with a probe at 45 of inclination and a con- sium dichromate (Duszynski and Wilber 1997). We applied stant distance of 3 mm from the skin surface. We recorded 3 spectra Sheather’s sugar flotation technique (Megı ´a-Palma et al. 2015)to per patch. Ventral blue coloration shifts from blue to green depend- concentrate intestinal parasites. Each sample was screened at 600 ing on the body temperature in the closely related species, magnification. S. undulatus (Langkilde and Boronow 2012). To account for this, all individuals remained at room temperature (24 C) for 20 min Measuring reflectance of color patches before we measured coloration. All measurements were relative to a We measured the reflectance from the blue patch on the right side of 99% WS-1 white reflectance standard. the belly; and the yellow patch located on the anterior part of the right forelimb (Appendix). We avoided the blue markings that we Statistical analyses used to identify the individuals during the color measurements. All The mean reflectance spectra of each color patch and lizard were spectral measurements of the colorful patches were obtained by summarized in 1-nm bin-size spectra using the CLR v1.1 software spectrophotometry from 400 to 700 nm. Unfortunately, we could for analyzing reflectance spectra (Montgomerie 2009). Thereafter, not measure ultraviolet (UV) reflectance due to a problem with the the data of the 3 spectral measurements were averaged in Microsoft UV lamp in the spectrophotometer and, thus, it remained off during Excel (2010) per patch and lizard. Spectral data of color reflectance the measurements (the UV lamp is independent of the deuterium– can be broken down into 3 variables for its analysis: that is, light- tungsten light used for the visible range). Thus, our analyses are cen- ness, chroma, and hue (Montgomerie 2006). The total lightness for tered exclusively in the reflection of the visible range of the spec- trum. It is known that blue ventral coloration of Sceloporus lizards each spectrum was calculated as RQ , with Q being the per- 400-700 peaks in the blue–green spectral area and the reflectance is residual centage of reflectance for a given wavelength (k). Lightness is the total amount of light reflected by a surface and it is interpreted as in the near-UV range (see Figures 1a and 1b in Stoehr and McGraw how dark or light a surface is (Montgomerie 2006). Hue can be 2001). Pterins—and not carotenoids—are known to be the main pig- ment that produce the yellow or orange-based coloration of phryno- interpreted as a categorical variable of color describing a surface somatids (Morrison et al. 1995; Weiss et al. 2012; Haisten et al. (blue, green, yellow, red, etc). The hue variable for the blue and the 2015) and, apparently, no significant biological information is con- yellow patches was defined as the value of k for the Q (i.e., k ; max max Montgomerie 2006). Thus, lower values of hue in the blue patch tained in the near-UV region of color patches based on this pigment (Haisten et al. 2015; Cuervo et al. 2016). The spectrophotometer, define more bluish coloration, whereas higher values of hue in the an USB2000 Ocean Optics, was connected to a fiber-optic probe yellow patch define orange-like patches. For chroma calculation of Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 4 Current Zoology, 2018, Vol. 0, No. 0 each color patch, we selected the defined range of blue and yellow in Sexual dimorphism and dichromatism Males and females did not significantly differ in SVL (males mean the visible range (Endler 1990; Grill and Rush 2000), which assigns SVL6 SE¼ 59.46 0.9 mm, range¼ 41.0–69.0; females mean wavelength ranges of 75 nm to each color (i.e., blue, green, yellow, SVL6 SE¼ 56.46 1.0 mm, range¼ 48.0–68.0; F ¼ 3.78, and red) and we calculated RQ /RQ . Thus, we obtained 1, 66 segment 400-700 P¼ 0.05). Our model-selection procedure produced a set of models a relative reflectance, or saturation, of the segment of interest (Table 1) that included the sex of the individuals as the best predic- for each color patch (i.e., 400–475 nm in the blue patch and tor for the chromatic variables in the blue patch (best models for the 550–625 nm in the yellow patch). blue patch: lightness  sexþ SVL, AICc¼ 927.04, weight¼ 0.49; We analyzed the relationships among the chromatic variables, chroma  Acroeimeriaþ sexþ SVL, AICc¼186.55, weight¼ the morphological variables, and the presence of parasites using 0.28; hue  Acroeimeriaþ sexþ Acroeimeria*sex, AICc¼ 179.62, Akaike’s information criterion (AIC) to select the model with the weight¼ 0.22). The coefficients in our model-averaging procedure best fit (¼ with the lowest AIC, Burnham and Anderson 2004). suggested that the sex of the individuals was a significant predictor Furthermore, we performed model averaging using MuMIn (Barton for the lightness (relative importance ¼ 1.0, P< 0.001) and the hue 2013) and calculated the relative importance of each predictor sum- of the blue patch (relative importance ¼ 1.0, P< 0.001), whereas it ming the weights of all the models where the term appears. For that, was nearly significant in relation to the blue chroma (relative we considered sufficiently informative all the models with D AIC 2 importance¼ 0.68, P¼ 0.05). The blue patches of the males were (Burnham and Anderson 2004). In addition, we calculated the sig- significantly darker (the mean6 SE lightness for the blue patch was nificance of the coefficients for each predictor in the final models. 494.66 27.9 for the males and 1,154.66 61.6 for the females; For those predictors that were significant (<0.05), we calculated the F ¼ 126.09, P< 0.0001) and significantly more bluish (the 1, 66 maximum likelihood estimate and its standard error. Each chro- mean6 SE hue for the blue patch was 494.76 3.0 for the males and matic variable was independently tested in 2 sets of tests. First, we 535.86 9.3 for the females; F ¼ 27.41, P< 0.0001) compared 1, 66 ran the analyses for both males and females together. The sex and with those of females (Table 1). Thus, the blue patch was sexually the presence of Acroeimeria were fixed as factors. The SVL, BCI, dichromatic. In addition, the SVL was a significant predictor for and interaction sex*Acroeimeria were the independent predictors. lightness in the blue patch of males (relative importance ¼ 1.0, Second, we tested the relationships among the chromatic variables, P< 0.001; Pearson’s correlation: P< 0.0001, R ¼ 0.39). Larger the morphological variables, and the presence of parasites in males males had darker blue patches than smaller individuals (Table 2). and females separately. As we found Lankesterella in only 2 females, Among the females, none of the predictors explored here signifi- cantly explained the chromatic variables of the blue coloration. we tested for the effects of infection of the hemoparasite on males Although the sex of the individuals was included in the best models only. We tested differences in SVL and BCI between individuals of for all the chromatic variables in the yellow patch (best models for the both sexes with absence/presence of Acroeimeria with one-way yellow patch: lightness  Acroeimeriaþ BCIþ sexþ Acroeimeria*sex, ANOVA. AICc¼ 982.59, weight¼ 0.31; chroma  sexþ SVL, AICc¼289.62, weight¼ 0.27; hue  Acroeimeriaþ BCIþ sexþ Acroeimeria*sex, BCIc¼151.46, weight¼ 0.55), our model-averaging procedure sug- Results gested that neither sex nor the infection by Acroeimeria were impor- Parasites detected tant predictors for the chromatic variables of the yellow patch when We found parasites of the genus Acroeimeria in the feces and para- males and females are analyzed together because their coefficients were sites of the genus Lankesterella in the blood of the lizards (Megı ´a- not significant in the resulting averaged models (Table 1). Palma et al. 2015, 2017). No infection by malarial parasites was Nevertheless, the SVL of the lizards significantly predicted the chroma detected. We found a similar prevalence of Acroeimeria (33.8%) in (relative importance¼ 1.0, P< 0.001) and the hue (relative the sample (v ¼ 0.71). There were no differences between sexes importance¼ 1.0, P< 0.001) of the yellow patch in both sexes with 1, 68 in the prevalence of Acroeimeria: 31% (14/45) of the males and thesamesign (Table 2). Larger individuals had higher yellow chroma 39% (9/23) of the females were infected (v ¼ 0.3, P¼ 0.6). We and higher values of hue (i.e., orange) than smaller individuals 1, 68 found 30.8% (21/68) prevalence of Lankesterella in the sample. (Pearson’s correlation for chroma: P< 0.0001, R ¼ 0.27; and hue: P¼ 0.002, R ¼ 0.12; Figure 2). Furthermore, SVL was a significant However, only 2 females were infected and, therefore, the preva- predictor of the yellow lightness in males (relative importance¼ 0.78, lence was significantly higher in males (42.2%) than in females P< 0.01; Pearson’s correlation: P¼ 0.04, R ¼ 0.09). Larger males had (8%; v ¼ 7.7, P¼ 0.005). 1, 68 darker yellow patches (Figure 2). In addition, BCI was a significant predictor of the hue in the yellow patch of males (relative Parasites, body size, and body condition importance¼ 0.96, P< 0.01; Pearson’s correlation: P¼ 0.02, There were no differences in SVL among males or females with respect R ¼ 0.11). Males with better body condition had higher values of hue. to the presence/absence of Acroeimeria (differences of SVL in males: F ¼ 0.23, P¼ 0.63; difference of SVL in females: F ¼ 0.35, 1, 43 1, 21 Parasite infection and coloration P¼ 0.55. In contrast, the males infected by Lankesterella were signifi- Our model-selection procedure suggested that the infection by the cantly larger (mean SVL6 SE¼ 61.76 1.0 mm) than the uninfected intestinal parasites of the genus Acroeimeria was a good predictor for ones (mean SVL6 SE¼ 57.76 1.4 mm; F ¼ 4.78, P¼ 0.03). 1, 43 coloration when males and females were analyzed separated. The indi- Significant differences were present neither in BCI between infected vidual models for the chromatic variables of both sexes (Table 2)sug- and uninfected males with respect to Acroeimeria, nor in males (F 1, 42 gested that infection by Acroeimeria was a significant predictor of the ¼ 0.09, P¼ 0.75) or in females (F ¼ 0.18, P¼ 0.66). Neither were 1, 20 chroma in the blue patches of the males (best models for the blue patch the differences in BCI significant with respect to Lankesterella (F of the males: blue chroma  Acroeimeria,AICc¼116.58, 1, ¼ 1.55, P¼ 0.21). weight¼ 0.42, coefficient for Acroeimeria ¼ 0.96) and the hue in the Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Megı´a-Palma et al.  Sexual coloration and parasites 5 Table 1. Akaike analyses of the chromatic variables for males and females together and summarized by model-averaging procedure Blue: L SE Blue: C SE Blue: H SE Yellow: L SE Yellow: C SE Yellow: H SE n (D AIC 2) 32 42 5 2 N 43 45 5 5 TOTAL_V Importance Sex ***1.00 *0.68 ***1.00 0.93 *1.00 0.57 SVL ***1.00 0.25 0.48 **0.82 ***1.00 ***1.00 BCI 0.19 0.22 0.18 **0.79 0.40 ***1.00 Acroeimeria 0.32 **0.90 0.43 0.56 0.51 0.56 Sex*Acroeimeria 0.09 **0.50 *0.29 **0.44 *0.38 ***0.46 Estimates Sex 619.65 58.52 43.27 10.27 SVL 215.01 4.33 214.33 6.53 <0.01 <0.001 1.25 0.36 BCI 21363.65 634.72 112.47 35.89 Acroeimeria 20.04 0.02 Sex*Acroeimeria 0.06 0.03 371.94 168.45 225.72 9.47 Notes: n (D AIC 2)¼ number of probable models with D AIC 2. N ¼ total number of variables included in the models with D AIC 2. TOTAL_V Importance ¼ relative weight of the variables in the resulting averaged model. In the row “importance,” values shown in bold indicate the coefficients of the maxi- mum likelihood estimates that are significant with level of significance: *P¼ 0.05, **P< 0.01, ***P< 0.001. In the row “estimates,” we show the slope of the coefficients and their standard error. L, C, and H are lightness, chroma, and hue, respectively. Table 2. Akaike analyses of the chromatic variables for males and females separated and summarized by model-averaging procedure Males Blue: L SE Blue: C SE Blue: H SE Yellow: L SE Yellow: C SE Yellow: H SE n (D AIC 2) 226 7 4 4 N 223 4 4 3 TOTAL_V Importance SVL ***1.00 0.21 0.22 **0.78 ***1.00 **0.68 BCI 0.19 0.21 0.64 0.38 *0.66 **0.96 Acroeimeria 0.19 ***0.96 0.58 *0.67 *0.66 0.53 Lankesterella *0.57 0.25 0.30 0.43 0.29 0.25 Estimates SVL 217.25 3.72 215.13 7.23 <0.01 <0.001 0.92 0.45 BCI 130.01 49.51 Acroeimeria 20.05 0.02 Lankesterella Females Blue: L SE Blue: C SE Blue: H Yellow: L SE Yellow: C SE Yellow: H SE n (D AIC 2) 334 3 1 2 N 223 2 1 3 TOTAL_V Importance SVL 0.16 0.50 0.39 0.15 **0.81 ***1.00 BCI 0.30 0.24 0.20 *0.63 0.20 0.19 Acroeimeria 0.24 0.17 0.24 0.30 0.16 **1.00 Estimates SVL <0.01 0.001 2.99 0.58 BCI Acroeimeria 216.15 6.02 Notes: n (D AIC 2)¼ number of probable models with D AIC 2. N ¼ total number of variables included in the models with D AIC 2. TOTAL_V Importance ¼ relative weight of the variables in the resulting averaged model. In the row “importance,” values shown in bold indicate the coefficients of the maxi- mum likelihood estimates that are significant with level of significance: *P¼ 0.05, **P< 0.01, ***P< 0.001. In the row “estimates,” we show the slope of the coefficients and their standard error. L, C, and H are lightness, chroma, and hue, respectively. yellow patches of the females (yellow hue  Acroeimeriaþ SVL, Males and females infected by intestinal parasites of the genus AICc¼40.57, weight¼ 0.47, coefficient for Acroeimeria¼ 1.00). Acroeimeria expressed lower coloration as predicted by the H–Z The males infected with parasites of the genus Acroeimeria had blue hypothesis, although the differences observed in the females were patches with significantly less chroma (mean6 SE¼ 23.26 0.01) than not significant. The infected males expressed blue patches with a the uninfected males (mean6 SE¼ 28.76 0.01; F ¼ 7.31, mean 5.5% less chroma than the blue patch of the uninfected males. 1, 43 P¼ 0.009; Figure 1A); meanwhile, the females that were infected by Hormonal differences between infected and uninfected males might Acroeimeria expressed yellow patches that had lower values of hue explain the chromatic differences observed in the blue patch. In this (yellow-like patches: mean6 SE¼ 629.46 7.5) than the uninfected sense, reduction of testosterone level by castration of male S. jarrovi females (orange-like patches: mean6 SE¼ 641.46 6.6), but this differ- induced a significant reduction in chroma in the blue coloration ence was not significant (F ¼ 1.77, P¼ 0.19; Figure 1B). 1, 21 (Cox et al. 2008). Similarly to the castrated males in the study of Cox et al. (2008), male S. occidentalis that were infected by Acroeimeria expressed blue patches with low chroma. Castrated Discussion male S. jarrovi reduced their territorial and sexual behavior (Moore We found partial evidence supporting the parasite hypothesis 1987), and malarial parasites have similar effects in S. occidentalis (Hamilton and Zuk 1982) in this population of S. occidentalis. (Dunlap and Schall 1995) because they hinder their ability to Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 6 Current Zoology, 2018, Vol. 0, No. 0 Figure 2. Relationship between the SVL and the chromatic variables of the blue (A) and the yellow (B, C, and D) patches. In each of the analyses, the sex analyzed is shown in the bottom-left corner. compete for females or to actively patrol their home ranges (Schall in the blue patch could be related to sexual differences in testoster- and Dearing 1987; Schall and Houle 1992). Eimeriid parasites of one secretion because this hormone influences dimorphism in immu- strict intestinal life cycle, such as the genus Acroeimeria, are largely nocompetence in lizards (e.g., Mondal and Rai 1999) and, further, known to cause multiple diseases—and even death—in livestock and is responsible for sexual dichromatism in Sceloporus (Cox et al. wild fauna (Coudert et al. 1993; Blake and Tomley 2014). Similarly 2005, 2008; Calisi and Hews 2007). Testosterone increases the to males infected by malarial parasites, the presence of low chroma expression of the blue coloration in males of Sceloporus that may be in the blue patches of the males infected by Acroeimeria suggested important in S. occidentalis because this coloration is displayed that the infection might have a negative effect on the fitness of the toward competitors at short distance, reduces aggressive escalation male lizards in this population. during fights, and is used by conspecific for sex discrimination Besides the relationships found between the blue coloration of (Cooper and Burns 1987; Sheldahl and Martins 2000). However, the males with respect to the infection by Acroeimeria, we found the production of testosterone reduces both macrophage production low statistical evidence that supports any relationship of the infec- and the inflammatory response in male lizards (Mondal and Rai tion by Lankesterella with the expression of the color patches meas- 1999; Belliure et al. 2004). In addition, it may augment the meta- ured. Interestingly, hemoparasites of the genus Lankesterella bolic rate (e.g., Feuerbacher and Prinzinger 1981), increasing the infected almost exclusively males that, additionally, were larger oxidative stress and the cellular damage in the individuals (von than the uninfected ones. Larger males expressed darker blue Schantz et al. 1999). At the same time, oxidative stress can impair patches (i.e., less lightness) than uninfected males and, moreover, as immune functions (Alonso-Alvarez et al. 2007), and renders males previously commented, had darker yellow patches, with high more susceptible to parasitic infections (Mondal and Rai 1999). chroma and high hue. Langkilde and Boronow (2010) found that In addition to the relationships achieved between the parasitic larger males of the closely related species, S. undulatus, had darker infections and the coloration and morphology of the male lizards, blue patches than smaller males, suggesting that the coloration we found a strong effect of SVL on the chromatic variables of the might shift ontogenetically and, thus, larger males of S. occidentalis yellow coloration, with the same sign in both males and females. with intense coloration might be older. There are few reported cases Large males expressed orange-like (high values of hue) yellow of Lankesterella parasites in reptiles (Telford 2008), although its patches (also explained by BCI), which had more chroma and were presence may be more common than previously thought (e.g., Maia darker than those of smaller males. Similarly, large females et al. 2016; Megı ´a-Palma et al. 2017b). To our knowledge, only 1 expressed orange-like yellow patches with more chroma than study describes a negative effect of Lankesterella parasites causing smaller females. Thus, it seems to be a non-dichromatic patch that pneumonia in avian hosts (Speer et al. 1997). In S. occidentalis,we might have similar signaling function irrespective of the sex of the found low intensities of infection (i.e., mean parasite load/15,000 bearer. The Western Fence Lizard is considered a territorial lizard cells6 SE ¼ 4.66 1.1, max¼ 40) in comparison to other studies of species because both sexes show high site fidelity and defend their Old World lizards (e.g., Megı ´a-Palma et al. 2014 found a mean load home ranges (Sheldahl and Martins 2000). One of its most frequent of Lankesterella in 10,000 cells¼ 27.8, with max¼ 115 in behaviors is a series of short push-ups that they display to potential Acanthodactylus erythrurus). This might mean that, in this popula- mates or rivals from the distance (e.g., Schall and Houle 1992; tion it is important to maintain infections by Lankesterella under Sheldhal and Martins 2000). During this display, individuals may low thresholds because only high-quality individuals can tolerate it increase the visibility of the yellow patches of the forelimbs that or, alternatively, it might suggest a low virulence of this hemopara- might inform to conspecifics on their body size. The body size of the site (sensu Svensson and Ra ˚ berg 2010). In addition, the sexual dif- ferences in infection by Lankesterella and the sexual dichromatism individuals correlates with the female’s fecundity in the genus Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Megı´a-Palma et al.  Sexual coloration and parasites 7 Belliure J, Smith L, Sorci G, 2004. Effect of testosterone on T cell-mediated Sceloporus (Jime ´ nez-Arcos et al. 2017) and with fighting ability in immunity in two species of Mediterranean lacertid lizards. J Exp Zool Part lizards in general (Carpenter 1995; Molina-Borja et al. 1998). A 301:411–418. Based on the current knowledge of the high visual sensitivity of Blake DP, Tomley FM, 2014. Securing poultry production from the the visual system in closely related lizards of the family Iguanidae ever-present Eimeria challenge. Trends Parasitol 30:12–19. (i.e., Loew et al. 2002), we may speculate on the perceptual capacity Bonorris JS, Ball GH, 1955. Schellackia occidentalis n. sp., a blood-inhabiting of S. occidentalis to discriminate the chromatic characteristics of coccidian found in lizards in Southern California. J Protozool 2:31–34. conspecifics. Unfortunately, our spectral data did not include the Burnham KP, Anderson DR, 2004. Multimodel inference, understanding AIC UV range, although probably not being relevant in the color patches and BIC in model selection. Soc Methods Res 33:261–304. of Sceloporus (Stoehr and McGraw 2001), it precludes the applica- Calisi RM, Hews D, 2007. Steroid correlates of multiple color traits in the tion of tetrachromatic visual models in this study and, therefore, the spiny lizard Sceloporus pyrocephalus. J Comp Physiol B 177:641–654. consecution of stronger conclusions. We can only speculate whether Carpenter GC, 1995. Modeling dominance: the influence of size, coloration, these differences could be discriminated by conspecifics. It seems and experience on dominance relations in tree lizards Urosaurus ornatus. Herpetol Monogr 9:88–101. reasonable that the visual system of lizards co-evolves with the Clark GW, 1970. Eimeria ahtanumensis n. sp. from the northwestern fence liz- subtle variation of the coloration of conspecifics (Stoehr and ard Sceloporus occidentalis in central Washington. J Protozool 17:526–530. McGraw 2001), especially if those could transmit Acroeimeria.A Cooper WE, Jr, Burns N, 1987. Social significance of ventrolateral coloration proper discrimination between infected and uninfected potential in the fence lizard Sceloporus undulatus. Anim Behav 35:526–532. mates may be important for these lizards to decrease the probability Cooper WE, Jr, Crews D, 1987. Sexual coloration, plasma concentration of of infection whereas increasing the resistance to this parasite in the sex steroid hormones, and responses to courtship in the female keeled earless population. lizard Holbrookia propinqua. Horm Behav 22:12–25. In conclusion, we found partial support for the parasite hypothe- Coudert P, Licois D, Provot F, Drouet-Viard F, 1993. Eimeria sp. from the sis (Hamilton and Zuk 1982)in S. occidentalis because lizards rabbit Oryctolagus cuniculus: pathogenicity and immunogenicity of infected with parasites of the genus Acroeimeria expressed duller Eimeria intestinalis. Parasitol Res 79:186–190. colorations than the uninfected individuals. Although parasites Cox RM, Skelly SL, Leo A, John-Alder HB, 2005. Testosterone regulates sexu- ally dimorphic coloration in the Eastern Fence Lizard, Sceloporus undula- might mediate the sexual selection of this species (e.g., Schall and tus. Copeia 2005:597–608. Dearing 1987; Schall and Houle 1992), the Lankesterella–lizard Cox RM, Zilberman V, John-Alder HB, 2008. Testosterone stimulates the host system studied here did not support the H–Z hypothesis expression of a social color signal in the Yarrows Spiny Lizard, Sceloporus because infected males were bigger and more intensely colored than jarrovii. J Exp Zool 309A:505–514. the uninfected ones. Cuervo JJ, Belliure J, Negro JJ, 2016. Coloration reflects skin pterin concentra- tion in a red-tailed lizard. Comp Biochem Phys B 193:17–24. del Cerro S, Merino S, Martı´nez-de la Puente J, Lobato E, Ruiz-de-Castaneda ~ Acknowledgments et al., 2010. Carotenoid-based plumage colouration is associated with blood We want to thank the staff in the Arboretum of the Campus of Santa Cruz, parasite richness and stress protein levels in blue tits Cyanistes caeruleus. CA, for providing logistic support and K. Paulling, N. Bunn, and C. Wertin Oecologia 162:825–835. who contributed to collecting the lizards and doing the color measurements. Dı ´az JA, 1993. Breeding coloration, mating opportunities, activity, and survival in the lacertid lizard Psammodromus algirus. Can J Zool 71:1104–1110. Duneau D, Ebert D, 2006. Host sexual dimorphism and parasite adaptation. Funding PLoS Biol 10:e1001271. Financial support was provided by Spanish Ministerio de Economı´a y Dunlap KD, Mathies T, 1993. Effects of nymphal ticks and their interactions Competitividad (projects CGL2012-40026-C02-01 and CGL2015-67789- with malaria on the physiology of male fence lizards. Copeia 4:1045–1048. C2-1-P (MINECO/FEDER) to SM, and CGL2012-40026-C02-02 to JM, and Dunlap KD, Schall JJ, 1995. Hormonal alterations and reproductive inhibition grant numbers BES-2010-038427 and EEBB-I-14-08326 to RM-P). in male fence lizards Sceloporus occidentalis infected with the malarial para- Ministerio de Educacio ´ n funded SR with FPU grant number AP-2009-1325 site Plasmodium mexicanum. Physiol Zool 68:608–621. and EST13/00196. Permits for carrying out this investigation and collecting Duszynski DW, Wilber PG, 1997. A guideline for the preparation of species lizards were provided by the UCSC ethics committee (IACUC) and CDFG to descriptions in the Eimeriidae. J Parasitol 83:333–336. RDC. Research at the UCSC was supported by an NSF grant to BS (EF- Endler JA, 1990. On the measurement and classification of colour in studies of 1241848). animal colour patterns. Biol J Linn Soc 41:315–352. Feuerbacher I, Prinzinger R, 1981. The effects of the male sex-hormone testos- terone on body temperature and energy metabolism in male Japanese quail References Coturnix coturnix japonica. Comp Biochem Physiol 70A:247–250. ´ Grill CP, Rush VN, 2000. Analysing spectral data: comparison and applica- Abalos J, Pe ´ rez I de Lanuza G, Carazo P, Font E, 2016. The role of male colo- tion of two techniques. Biol J Linn Soc 69:121–138. ration in the outcome of staged contests in the European common wall liz- Haisten DC, Paranjpe D, Loveridge S, Sinervo B, 2015. The cellular basis of ard Podarcis muralis. Behaviour. doi: 10.1163/1568539X–00003366. polymorphic coloration in common side-blotched lizards Uta stansburiana. Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G, 2007. Herpetologica 71:125–135. Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc Hamilton WD, Zuk M, 1982. Heritable true fitness and bright birds: a role for R Soc B 274:819–825. parasites? Science 218:384–387. Barton K, 2013. MuMIn: Multi-model inference. R package, version1.40.0. Ho ¨ rak P, Ots I, Vellau H, Spottiswoo C, Møller AP, 2001. Carotenoid-based Bajer K, Molna ´ r O, To¨ro ¨ k J, Herczeg G, 2010. Female European green lizards plumage coloration reflects hemoparasite infection and local survival in Lacerta viridis prefer males with high ultraviolet throat reflectance. Behav breeding great tits. Oecologia 126:166–173. Ecol Sociobiol 64:2007–2014. Houde AE, Torio AJ, 1992. Effect of parasitic infection on male color pattern Balenger SL, Zuk M, 2014. Testing the Hamilton-Zuk hypothesis: past, present, and future. Int Comp Biol 54:601–613. and female choice in guppies. Behav Ecol 3:346–351. Bell EL, Price AH, 1996. Sceloporus occidentalis. Catalogue of American Jime ´ nez-Arcos VH, Sanabria-Urba ´ n S, Cueva del Castillo R, 2017. The inter- Amphibians and Reptiles (CAAR) 631:1–17. play between natural and sexual selection in the evolution of sexual size Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 8 Current Zoology, 2018, Vol. 0, No. 0 dimorphism in Sceloporus lizards (Squamata: phrynosomatidae). Ecol Evol Montgomerie R, 2009. CLR, version 1.1. Queen’s University, 7:905–917. Kingston, Canada. Available from http://post.queensu.ca/mont/color/ana Langkilde T, Boronow KE, 2010. Color as a signal: the relationship between lyze.html. coloration and morphology in male Eastern fence lizards, Sceloporus undu- Moore MC, 1987. Castration affects territorial and sexual behaviour of latus. J Herpetol 44:261–271. free-living lizards Sceloporus jarrovi. Anim Behav 35:1193–1199. Langkilde T, Boronow KE, 2012. Hot boys are blue: temperature-dependent Morrison RL, Rand MS, Frost-Mason SK, 1995. Cellular basis of color differ- color change in male Eastern Fence Lizards. J Herpetol 46:461–465. ences in three morphs of the lizard Sceloporus undulatus erythrocheilus. Llanos-Garrido A, Dı ´az JA, Pe ´ rez-Rodrı´guez A, Arriero E, 2017. Variation in Copeia 1995:397–408. male ornaments in two lizard populations with contrasting parasite loads. Ressel S, Schall JJ, 1989. Parasites and showy males: malarial infection and J Zool. doi: 10.1111/jzo.12478. color variation in fence lizards. Oecologia 78:158–164. Loew ER, Fleishman LJ, Foster RG, Provencio I, 2002. Visual pigments and Salvador A, Veiga JP, 2001. Male traits and pairing success in the lizards oil droplets in diurnal lizards: a comparative study of Caribbean anoles. Psammodromus algirus. Herpetologica 57:77–86. J Exp Biol 205:927–938. Schall JJ, Dearing MD, 1987. Malarial parasitism and male competition for Maia JP, Harris DJ, Carranza S, Go ´ mez-Dı´az E, 2016. Assessing the diversity, mates in the western fence lizard Sceloporus occidentalis. Oecologia 73: host-specificity and infection patterns of apicomplexan parasites in reptiles 389–392. from Oman, Arabia. Parasitology 143:1730–1747. Schall JJ, Houle PR, 1992. Malarial parasitism and home range and social sta- Martı´n J, Lo ´ pez P, 2009. Multiple color signals may reveal multiple messages tus of male western fence lizards Sceloporus occidentalis. J Herpetol 26: in male Schreiber’s green lizards Lacerta schreiberi. Behav Ecol Sociobiol 74–76. 63:1743–1755. Sheldahl LA, Martins EP, 2000. The territorial behavior of the western fence Martı´nez-de la Puente J, Merino S, Toma ´ s G, Moreno J, Morales J et al., lizard Sceloporus occidentalis. Herpetologica 56:469–479. 2010. The blood parasite Haemoproteus reduces survival in a wild bird: a Skarstein F, Folstad I, 1996. Sexual dichromatism and the immunocompetence medication experiment. Biol Lett 6:663–665. handicap: an observational approach using the Arctic charr. Oikos 76: Martı´nez-Padilla J, Mougeot F, Pe ´ rez-Rodrı´guez L, Bortolotti GR, 2007. 359–367. Nematode parasites reduce carotenoid-based signalling in male red grouse. Smith IC, John-Alder HB, 1999. Seasonal specificity of hormonal, behavioral, Biol Lett 3:161–164. and coloration responses to within- and between-sex encounters in male liz- Martins EP, 1993. Contextual use of the push-up display by the sagebrush liz- ards Sceloporus undulatus. Horm Behav 36:39–52. ards Sceloporus graciosus. Anim Behav 45:25–36. Speer CA, Baker DG, Yamaguchi A, Dubey JP, 1997. Ultrastructural charac- Megı´a-Palma R, Mart´nez ı J, Acevedo I, Martı´n J, Garcı´a-Roa R et al., 2015. teristics of a Lankesterella-like coccidian causing pneumonia in a northern Phylogeny of the reptilian Eimeria: are Choleoeimeria and Acroeimeria cardinal Carduelis cardinalis. Acta Protozool 36:39–47. valid generic names? Zool Scr 44:684–692. Stebbins RC, McGinnis SM, 2012. Field Guide to Amphibians and Reptiles of Megı´a-Palma R, Mart´nez ı J, Merino S, 2013. Phylogenetic analysis based on California: California Natural History Guides Revised Edition. Berkeley 18S rRNA gene sequences of Schellackia parasites (Apicomplexa: lankester- and Los Angeles: University of California Press. ellidae) reveals their close relationship to the genus Eimeria. Parasitology Stoehr AM, McGraw KJ, 2001. Ultraviolet reflectance of color patches in male 140:1149–1157. Sceloporus undulatus and Anolis carolinensis. J Herpetol 35:168–171. Megı´a-Palma R, Martı ´nez J, Merino S, 2014. Molecular characterization of Svensson EI, McAdam AG, Sinervo B, 2009. Intralocus sexual conflict over hemococcidia genus Schellackia (Apicomplexa) reveals the polyphyletic ori- immune defense and the resolution of gender load in a natural lizard popula- gin of the family Lankesterellidae. Zool Scr 43:304–312. tion. Evolution 63:3124–3135. Megı´a-Palma R, Martı´nez J, Merino S, 2016a. Structural- and Svensson EI, Ra ˚ berg L, 2010. Resistance and tolerance in animal carotenoid-based throat color patches in males of Lacerta schreiberi reflect enemy-victim coevolution. Trends Ecol Evol 25:267–274. different parasitic diseases. Behav Ecol Sociobiol 70:2017–2025. Swierk L, Langkilde T, 2013. Bearded ladies: females suffer fitness consequen- Megı´a-Palma R, Martı´nez J, Merino S, 2016b. A structural colour ornament ces when bearing male traits. Biol Lett 9:20130644. correlates positively with parasite load and body condition in an insular liz- Telford SRJr, 2008. Hemoparasites of the Reptilia: Color Atlas and Text. Boca ard species. Naturwissenschaften 103:1–10. Raton (FL): CRC Press. Megı´a-Palma R, Martı´nez J, Merino S, 2017a. Manipulation of parasite load Thompson CW, Hillgarth N, Leu M, McClure HE, 1997. High parasite load induces significant changes in the structural-based throat color of male in house finches Carpodacus mexicanus is correlated with reduced expres- Iberian green lizards. Curr Zool. doi: 10.1093/cz/zox036. sion of a sexually selected trait. Am Nat 149:270–294. Megı´a-Palma R, Martı ´nez J, Paranjpe D, D’amico V, Aguilar R et al., 2017b. Va ´ clav R, Prokop P, Fekia c V, 2007. Expression of breeding colouration in Phylogenetic analyses reveal that Schellackia parasites (Apicomplexa) European green lizards Lacerta viridis: variation with morphology and tick detected in American lizards are closely related to genus Lankesterella:is infestation. Can J Zool 85:1199–1206. the range of Schellackia restricted to Old World? Par Vec 10:470. von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H, 1999. Good Merila ¨ J, Sheldon BC, Lindstro ¨ m K, 1999. Plumage brightness in relation to genes, oxidative stress and condition-dependent sexual signals. Proc R Soc haematozoan infections in the greenfinch Carduelis chloris: bright males are B 266:1–12. a good bet. Ecoscience 6:12–18. Ward PI, 1988. Sexual dichromatism and parasitism in British and Irish fresh- Merino S, Moreno J, Sanz JJ, Arriero E, 2000. Are avian blood parasites water fish. Anim Behav 36:1210–1215. pathogenic in the wild? A medication experiment in blue tits Parus caeru- Weiss SL, 2002. Reproductive signals of female lizards: pattern of trait expres- leus. Proc R Soc B 267:2507–2510. sion and male response. Ethology 108:793–813. Molina-Borja M, Padro ´ n-Fumero M, Alfonso-Martı´n T, 1998. Morphological Weiss SL, Foerster K, Hudon J, 2012. Pteridine, not carotenoid, pigments and behavioural traits affecting the intensity and outcome of male contests underlie the female-specific orange ornament of striped plateau lizards in Gallotia galloti galloti (Family Lacertidae). Ethology 104:314–322. Sceloporus virgatus. Comp Biochem Phys B 161:117–123. Mondal S, Rai U, 1999. Sexual dimorphism in phagocytic activity of wall liz- Worden BD, Parker PG, Pappas PW, 2000. Parasites reduce ard’s splenic macrophages and its control by sex steroids. Gen Comp attractiveness and reproductive success in male grain beetles. Anim Behav Endocr 116:291–298. 59:543–550. Montgomerie R, 2006. Quantifying colors. In: Hill GE, McGraw KJ, editors. Zuk M, 1988. Parasite load, body size, and age of wild-caught male field crick- Bird Coloration, Vol 1. Mechanism and Measurements. Cambridge: ets (Orthoptera: gryllidae): effects on sexual selection. Evolution 42: Harvard University Press, 41–89. 969–976. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Megı´a-Palma et al.  Sexual coloration and parasites 9 Appendix A Yellow patch Blue patch 400 400 500 500 600 600 7 700 00 Wavelength (nm) CD Yellow patch Blue patch 400 500 600 700 Wavelength (nm) Figure A1. Ventral coloration and mean6 SE spectral profiles of both yellow and blue patches of female (A, B) and male (C, D) Sceloporus occidentalis bocourtii. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy007/4819261 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Reflectance (%) Reflectance (%)

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