TY - JOUR
AU - Berg, Elena, C.
AB - Abstract The functional significance of bird egg color and patterning is a continuing subject of interest and debate. Extreme polymorphism in eggshell appearance is often thought to be maintained by frequency-dependent selection operating within populations. However, variation could also be explained by small-scale differentiation combined with limited migration. Here, we report the existence of extreme variation in egg color in a population of Mexican Jays (Aphelocoma ultramarina) inhabiting a steep elevation and habitat gradient within a single mountain range, the Sierra del Carmen of Coahuila, Mexico. We quantified egg color of 143 eggs from 54 nests throughout the mountain range, using digital photos. Color was also quantified for a subset of these eggs, using a spectrometer. Results from both methods support the conclusion that egg color has diverged at a remarkably small spatial scale of 3–15 km. Photo color quantification indicated that eggs at high elevation were greener than those at low elevation. Spectrometer results supported this conclusion, with more-pigmented (i.e., less reflectant) eggs occurring at high elevation. Unlike in other species, differences in condition do not seem to drive these divergence patterns in egg color. Further study is needed to determine to what extent differences result from heritable genetic change attributable to divergent selection pressures or from an environmentally induced phenotypic response. Resumen El significado funcional del color y el patrón de coloración de los huevos de las aves es un tema de debate e interés continuo. Frecuentemente se piensa que el polimorfismo extremo en la apariencia de la cáscara de los huevos se mantiene por selección intrapoblacional dependiente de la frecuencia. Sin embargo, la variación podría también ser explicada por diferenciación a pequeña escala combinada con migración limitada. En este estudio documentamos la existencia de variación extrema en el color de los huevos en una población de Aphelocoma ultramarina que habita un gradiente pronunciado de elevación y de hábitat en una sola región de montaña, la Sierra del Carmen de Coahuila, México. Empleando fotografías digitales, cuantificamos la coloración de 143 huevos pertenecientes a 54 nidos a lo largo de la montaña. El color también fue cuantificado para un subgrupo de estos huevos empleando un espectrómetro. Los resultados de ambos métodos avalan la conclusión de que la coloración de los huevos ha divergido a una escala espacial destacablemente pequeña, de 3 a 15 km. La cuantificación del color mediante fotos indicó que los huevos de mayores elevaciones fueron más verdes que aquellos de elevaciones bajas. Los resultados del espectrómetro avalaron esta conclusión: los huevos más pigmentados (i.e., con menor reflectancia) se encontraron a mayores elevaciones. A diferencia de otras especies, las diferencias en la condición no parecen conducir estos patrones divergentes en la coloración de los huevos. Es necesario realizar más estudios para determinar hasta qué punto las diferencias se deben a cambios genéticos hereditarios atribuibles a presiones de selección divergentes o a una respuesta fenotípica inducida por el ambiente. BIRD EGGS HAVE long intrigued biologists because of the astonishing diversity of colors and patterns within and among species (Wallace 1889, Lack 1958). Extreme cases of intrapopulation variation in egg appearance have been explained by identity signaling in crowded nesting sites (Dale 2006) or in the presence of brood parasites (Collias 1993, Davies 2000). In these cases, variation is presumably maintained by frequency-dependent selection, where rare types find themselves at a selective advantage. By contrast, polymorphism could also be generated and maintained by a balance between differentiation (e.g., Gosier et al. 2005, Lahti 2008) and migration, with differentiation resulting from heritable genetic change (assuming that selection is strong enough and migration is limited), an environmentally induced response, or both. To date, there has been no evidence of small-scale divergence in eggshell appearance of the type that could potentially contribute to intrapopulation variation in egg appearance. Presumably this is because conditions suitable for local differentiation (e.g., philopatry combined with strong habitat gradients) are rarely met in birds. Many factors could lead to local differences in eggshell appearance along environmental gradients, including evaporation rate (Rahn et al. 1977), soil minerals (Gosier et al. 2005), contaminants (Jagannath et al. 2008), and solar radiation (Lahti 2008), but it is unclear how general some of these processes are across a broad range of species. On the other hand, blue-green coloration and its causative pigment, biliverdin, have been associated positively with female condition in several species (Moreno et al. 2005, 2006; Siefferman et al. 2006; Hanley et al. 2008; López-Rull et al. 2008; Soler et al. 2008). This link is potentially explained by the antioxidant properties of biliverdin (Kaur et al. 2003), which could confer health benefits on females that experience oxidative metabolism during egg laying (Wiersma et al. 2004). Measures of condition have included immune response (Moreno et al. 2005), antioxidant capacity (Hanley et al. 2008), diet (Moreno et al. 2006), feather condition (Soler et al. 2008), and size-adjusted mass (Moreno et al. 2005, Siefferman et al. 2006). In a study of the Spotless Starling (Sturnus unicolor), López-Rull et al. (2008) found a positive correlation between female body condition (size-adjusted mass) and amount of eggshell biliverdin, although, intriguingly, this did not translate into detectable differences in blue-green coloration. Fig. 1. Open in new tabDownload slide Habitat differences in the Sierra del Carmen, Coahuila, Mexico. (A) A low-elevation canyon (1,700 m) dominated by oaks (Quercus spp.). (B)A high-elevation mixed conifer forest (2,300 m) with pines (Pinus spp.), firs (Pseudotsuga spp. and Abies spp.), and oaks. (C) Range of variation in egg color of Mexican Jays in the Sierra del Carmen. Photographs are of eggs from 4 clutches. The background grid was used to standardize for ambient light. Fig. 1. Open in new tabDownload slide Habitat differences in the Sierra del Carmen, Coahuila, Mexico. (A) A low-elevation canyon (1,700 m) dominated by oaks (Quercus spp.). (B)A high-elevation mixed conifer forest (2,300 m) with pines (Pinus spp.), firs (Pseudotsuga spp. and Abies spp.), and oaks. (C) Range of variation in egg color of Mexican Jays in the Sierra del Carmen. Photographs are of eggs from 4 clutches. The background grid was used to standardize for ambient light. We investigated the possible connection between female condition and local differentiation in blue-green egg color in a population of Mexican Jays (Aphelocoma ultramarina). Three characteristics of Mexican Jays and our study site make this setting ideal for an investigation of small-scale divergence in egg color. First, the Mexican Jays at our study site—the Sierra del Carmen, a sky-island mountain range in northern Mexico—occupy an unusually strong and abrupt habitat transition, which provides the opportunity for local ecological differences to influence intrapopulation phenotypic diversity (McCormack and Smith 2008). Likely because of its isolation from potential colonizing sources, this mountain range does not support stable populations of Steller's Jays (Cyanocitta stelleri) or Western Scrub-Jays (Aphelocoma californica) (Miller 1955, Wauer and Ligon 1974). In the absence of those species, Mexican Jays have filled vacant ecological niches at high and low elevation in which they are normally absent (Brown and Brown 1985) and now occupy a variety of habitats spanning from oak woodland in arid, low-elevation canyons to high-elevation conifer forest (Fig. 1A, B). Previous research in the Sierra del Carmen has documented morphological divergence resulting from this niche expansion (McCormack and Smith 2008). High-elevation Mexican Jays have shorter, straighter bills than low-elevation jays, which possess bills with a larger hook. These differences are presumably adaptive for feeding on locally abundant pine seeds and acorns, respectively. Second, low dispersal in Mexican Jays makes it more likely that small-scale differences could form. Mexican Jays are highly sedentary and live in cooperative flocks with stable, year-round territories (McCormack and Brown 2008). Individuals rarely disperse far from natal flocks and instead remain to help rear young produced by other flock members (Brown and Brown 1981). McCormack and Smith (2008) detected significant genetic differentiation between elevations in the Sierra del Carmen, which indicates moderately restricted gene flow. Third, the population of Mexican Jays in the Sierra del Carmen has strikingly polymorphic eggs (Fig. 1C), with color ranging from white to blue-green and speckling covering 0–41% of the egg's surface (Berg et al. 2009). This amount of variation is not apparent in other parts of the Mexican Jay's range, where eggs are plain and color does not vary as obviously (McCormack and Brown 2008), which leads to the question of what processes have produced and maintained this variation in the region that includes the Sierra del Carmen. A previous study of this population rejected the calcium-deficiency hypothesis for egg speckling (Gosier et al. 2005), finding that speckling did not vary with elevation despite a strong gradient in available soil calcium levels (Berg et al. 2009). By contrast, here we examine whether blue-green ground coloration—another highly variable egg trait in this population—differs with elevation. We also explore the possibility that female condition influences egg color, using two likely surrogates of female condition, egg volume and size-adjusted female body mass. We use these traits to test the hypothesis that high-elevation Mexican Jays are in better condition, which leads to eggs with more blue-green coloration at high elevation. Fig. 2. Open in new tabDownload slide Location of the field site in the Sierra del Carmen, Coahuila, Mexico, and the 51 Mexican Jay nests (open circles) from which egg color was quantified. Light gray shading indicates 1,500 m elevation, and dark gray indicates 2,200 m elevation. Fig. 2. Open in new tabDownload slide Location of the field site in the Sierra del Carmen, Coahuila, Mexico, and the 51 Mexican Jay nests (open circles) from which egg color was quantified. Light gray shading indicates 1,500 m elevation, and dark gray indicates 2,200 m elevation. Methods From 2002 to 2007, we collected data on egg color and egg volume from nests at different elevations throughout the Sierra del Carmen (Fig. 2). Locations and elevations of nests were recorded with a global positioning system (GPS) device. We analyzed egg color digitally from photos taken in ambient light on the ground near the nest tree, and, for a subset of the data, we also measured color at the same time with a portable spectrometer. Egg volume was calculated using the equation 0.51 × length × breadth2 (Hoyt 1979). Length and breadth measurements were in millimeters and were taken in the field using digital calipers to the nearest 0.1 mm. All eggs were returned to their nests after processing, except for 1 that was taken back to the lab for ultraviolet (UV) spectrometry. Fig. 3. Open in new tabDownload slide A sample spectral curve for a Mexican Jay egg (dark black line) showing peak reflectance in blue-green wavelengths and secondary peak in the ultraviolet. Dashed lines represent the full range of spectral variation in the Sierra del Carmen, Coahuila, Mexico. The thin line represents reflectance of a sample white egg. Fig. 3. Open in new tabDownload slide A sample spectral curve for a Mexican Jay egg (dark black line) showing peak reflectance in blue-green wavelengths and secondary peak in the ultraviolet. Dashed lines represent the full range of spectral variation in the Sierra del Carmen, Coahuila, Mexico. The thin line represents reflectance of a sample white egg. Digital photo analysis.—We employed a variation of Villafuerte and Negro's (1998) method for analysis of color from digital photos, which uses red, green, and blue (RGB) values standardized for differences in ambient light. Although this method does not quantify color in the UV range, which is visible to birds, spectrometer readings from Mexican Jay eggs revealed that their major spectral reflectance peak is in the human-visible range (Fig. 3), which is likely to be highly correlated with spectra that also include the UV range (Moreno et al. 2006). We used several methods to address potential problems associated with quantifying color from photographs (Stevens et al. 2007). (1) All photos were taken with the same camera (Canon Powershot A40) in manual mode with the same settings. (2) We included a background standard with each photo to correct for ambient light differences among photos. And (3) although we did not calibrate to an in-camera white standard (Stevens et al. 2007), care was taken to avoid over- and underexposure by photographing the eggs at similar light levels away from direct sunlight. We used JPG images produced by the camera even though they may result in some loss of detail (Stevens et al. 2007), because we sought to quantify only ground pigmentation, which is deposited uniformly over the egg. Also, because our study did not explore the potential signaling function of eggshell coloration, we did not attempt to convert our color scores to the visual system of birds. We used PHOTOSHOP CS2, version 12.0.0 (Adobe Systems, San Jose, California), to calculate RGB values of 3 sample circles per egg. Each sample circle consisted of 384 pixels. To minimize the effects of shadow and reflectance, 1 sample circle was measured along the central axis 1 third of the distance from the foot (top) of the egg. Two other sample circles were measured on either side of this axis, halfway to the edge of the egg. Mean RGB values for the 3 circles were used in further analyses. These values were divided by overall brightness, which was calculated as a total of RGB values (R + G + B). We preferred this unweighted metric for brightness to PHOTOSHOP'S luminosity measure because the latter metric is a weighted average of RGB (L = [0.30 × R] + [0.59 × G] + [0.11 × B]) tuned to peak sensitivity of human vision in green wavelengths. Variation in ambient light was corrected for each egg in each photo using a standard background grid of nonglossy black squares on a synthetic mat included with each photo (see Fig. 1C). We measured RGB values for the black square above each egg, ensuring that the egg did not shield the square from ambient light. After processing all photos, we averaged the measurements for the black squares and used deviation from this average to calculate a study-specific ambient-light correction factor for each egg. Spectrometer analysis.—For a subset of the eggs, we also quantified color using a Digital Swatchbook spectrophotometer (X-Rite, Grand Rapids, Michigan). For each egg, we measured reflectance spectra in relation to a white standard by depressing the instrument against the shell in a spot 7 mm in diameter that was free of speckles. Multiple measurements were taken for each egg to calculate repeatability of reflectance scores. Reflectance values were saved over 32 segments of the visible spectrum (10-nm segments from 410–700 nm), and these variables were further reduced to 16 by binning (i.e., averaging) scores over every 2 segments (20 nm) to prevent high correlations among the segments and therefore satisfy an assumption of principal component analysis (PCA) that variables are independent. We analyzed these 16 variables with PCA of the covariance matrix. Results that used binning every 4 segments (40 nm) produced similar results. Statistical analysis of egg data.—To determine whether the color of eggs within nests was highly correlated and, thus, whether controls for correlations within nests were needed, we used the intraclass correlation coefficient, or repeatability (Lessells and Boag 1987). To test for a relationship between egg color and elevation, we used a linear regression model with robust standard errors for cluster-correlated data (Williams 2000), which controls for correlations within groups (e.g., eggs within a nest) and provides robust standard errors for calculation of significance values. The dependent variable was either blue or green from photo analysis or the first or second principal component (PC1 or PC2) from spectrometer analysis. Continuous predictors were elevation, egg volume (which is correlated with female condition in some species; Amat et al. 2001, Parker 2002; see below), clutch size, year (only for digital color scores because all spectrometer data were collected in a single year), and laying date. Nonsignificant terms were removed with backward elimination. Statistical tests were performed using the software package STATA INTERCOOLED, version 10 (Stata-Corp, College Station, Texas). Female condition along an elevation gradient.—We used egg volume as a surrogate for female condition to test for an effect of condition on the color of eggs laid by females in our study (see above). Because of the difficulty of target-trapping wild Mexican Jays, we were unable to obtain data on body condition of the females known to have laid the eggs. However, over 6 years (2002– 2007), we collected morphological data on Mexican Jays captured with mist nets at various sites throughout the Sierra del Carmen. We used these data to investigate whether body condition varies with elevation. During trapping, mist nets were placed randomly throughout a site, which ensured that we sampled a random cross-section of the population. Elevation for each individual was determined by GPS. When possible, individuals were sexed in the field (by observing a cloacal protuberance or brood patch). All individuals were later sexed genetically from blood or feather samples (Fridolfsson and Ellegren 1999; for details, see McCormack and Smith 2008). We restricted our analysis to second-year (SY) and after-second-year (ASY) birds, as determined through molt limits and pigmentation of the inner upper mandible (Pyle 1997). Body condition was quantified by taking the residuals of a regression of body mass on tarsus length cubed (i.e., size-adjusted body mass). To test for elevational differences in body condition, we used a general linear mixed model, with body condition as the dependent variable, elevation as a continuous predictor, season (spring or fall) as a categorical predictor, age (SY or ASY) as a categorical predictor, and year included as a random effect. We ran four analyses, one using all individuals of both sexes, one using only females, one using only spring females, and one using only known breeding females as determined by observation of a brood patch (for the latter analysis, season and age were not included in the model, because breeding individuals were all ASY and were observed only in spring). Results Eggs measured by digital photography.—We quantified the color of 143 eggs from 51 nests in the Sierra del Carmen at elevations ranging from 1,421 m to 2,585 m (Fig. 2). Although the possibility of egg fading was not controlled for quantitatively by recording the elapsed incubation period at the time of nest discovery, there were no clear elevational biases in the nest stage at the time of measurement. The proportion of nests found before or during laying was high and was similar for high- and low-elevation nests (18 of 25 and 10 of 15, respectively), which suggests that egg fading would probably not contribute to elevational differences in egg color. Digital color ranged from white to various shades of blue-green (Fig. 1). Three nests with white eggs (n = 8) were excluded from further analyses because white eggs represented a discrete morph (see Fig. 3), were all equally lacking pigmentation, and were found in nests in almost the same location in successive years, which suggests that they may have been laid by the same female. Our results did not differ qualitatively when white eggs were included. From knowledge of flock location, we were reasonably certain that 35 of the remaining 48 nests were from different females. The remaining 13 nests were from 10 flocks that were already represented by 1 nest in a different year. Because dominant females often remain as breeders within flocks over multiple years (McCormack and Brown 2008), we were not certain whether these 13 nests represented independent data points. However, because green color was not highly correlated among the nests within a flock (intraflock correlation coefficient = 0.38), we included these nests in our analyses. The conclusions did not change when these data were excluded. Blue and green values from digital photos were positively correlated with each other (Pearson's r = 0.42). The extremely high negative correlation of green with red (Pearson's r = -0.95) suggests that the two measures are not independent axes of variation. Furthermore, absorption of the biliverdin pigment is known to lead to peak reflectance in the blue-green part of the spectrum (Kennedy and Vevers 1976). Thus, we conducted subsequent analyses using blue and green and did not further consider red. Intraclass correlation coefficients of eggs within nests were moderate to high for blue (0.73) and green (0.88). When we controlled for correlation of eggs within nests, green had a significant positive relationship with elevation (regression: F = 7.85, df = 1 and 47, P = 0.007, R2 = 0.11, n= 135; Fig. 4A) after removing the terms year (t= -0.78, P= 0.44), laying date (t= 0.05, P= 0.96), clutch size (t = -0.48, P = 0.63), and egg volume (t = 1.61, P = 0.12), in that order. There was no significant correlation between elevation and blue (regression: F< 0.01, df = 1 and 47, P= 0.98, r2 < 0.01, n= 135). Fig. 4. Open in new tabDownload slide Relationship between elevation and (A) green color from digital photos and (B) PC1 from the spectrometer (brightness) in Mexican Jay eggs in the Sierra del Carmen, Coahuila, Mexico. Fig. 4. Open in new tabDownload slide Relationship between elevation and (A) green color from digital photos and (B) PC1 from the spectrometer (brightness) in Mexican Jay eggs in the Sierra del Carmen, Coahuila, Mexico. Eggs measured by spectrometer.–We took spectrometer readings on 79 eggs from 26 nests (Fig. 3), a subset of those eggs for which color was measured digitally. Multiple measurements (range: 2–10, average = 3.5) were taken on 78 of these eggs. Repeatability of spectral scores was high, averaging 0.96 over spectra in blue-green wavelengths. PC1 explained 95.0% of the variance and loaded positively on all 16 segments, making it a descriptor of brightness (Table 1). PC2 explained 4.5% of the variance and loaded positively on values in the blue-green spectral range and negatively on other spectra, making it a descriptor of chroma, or purity of color (Table 1). PC3 explained only 0.06% of the variance and was not considered further. Correlation coefficients of eggs within nests were high for PC1 and PC2 (intraclass correlation coefficients = 0.92 and 0.72, respectively). PC1 from the spectrometer was negatively correlated with green values from digital photos (r = - 0.71, P < 0.001). After controlling for correlations within nests and removing nonsignificant terms (laying date: t= 0.88, P= 0.39; egg volume: t = -1.53, P = 0.14; clutch size: t = 1.75, P = 0.09), there was a nearly significant negative relationship between spectrometer PC1 (brightness) and elevation (regression: F= 3.78, df= 1 and 24, P = 0.06, R2 = 0.12, n = 75; Fig. 4B). We note that when spectra were averaged into 8 bins instead of 16, the R2 value remained the same and the relationship was significant (regression: F= 5.03, df= 1 and 24, P = 0.03, R2 = 0.12, n = 75). There was no significant relationship between PC2 (chroma) and elevation (regression: F = 0.36, df= 1 and 24, P= 0.55, r2 = 0.01, n = 75). Table 1. Principal component analysis of reflectance scores over 16 segments of the visible spectrum. Open in new tab Table 1. Principal component analysis of reflectance scores over 16 segments of the visible spectrum. Open in new tab Body condition along an elevation gradient.—Egg volume (a surrogate of female condition) did not contribute significantly to either model explaining variation in egg color (see above). With respect to body condition, of the 127 total SY and ASY Mexican Jays captured and sexed from 2002 to 2007,78 were male and 49 were female. The regression of body mass on tarsus length cubed was significant (regression: F= 26.27, df = 1 and 125, P < 0.001, r2 = 0.17, n = 127), and the residuals (size-adjusted body mass) were used in later analysis as a surrogate for body condition. The model relating body condition to elevation was not significant, and the trend was in the direction opposite of that predicted, with low-elevation individuals being in marginally better condition (full model: Wald χ2 = 26.47, P < 0.001, n = 127; elevation: z= -1.66, P = 0.096). In this model, males were in better condition than females (sex: z= 1.98, P = 0.047), ASY individuals were in better condition than SY individuals (age: z=3.44, P=0.001), and fall birds were in better condition than spring birds (season: z= 2.18, P = 0.029). Also, there was no relationship between body condition and elevation in analyses including only females (full model: Wald χ2 = 19.54, P < 0.001, n= 49; elevation: z= -0.32, P = 0.75; age: z= 4.29, P < 0.001; season: z = 0.18, P = 0.86), only spring females (full model: Wald χ2 = 15.46, P < 0.001, n= 42; elevation: z= 0.34, P = 0.73; age: z= 3.93, P < 0.001), and only breeding females (full model: Wald χ2 = 0.19, P < 0.67, n= 16; elevation: z= 0.43, P = 0.67). Discussion Our results indicate that variation in blue-green egg color of Mexican Jays in the Sierra del Carmen is attributable, at least in part, to divergence along an elevation gradient over extremely small spatial scales of 3–15 km. Results from both digital photos and spectrometry support our main conclusion that eggs at high elevation have more pigmentation than those at low elevation. Although the relationship between elevation and brightness quantified from the spectrometer was near the threshold for significance (possibly because of lower sample size and reduced statistical power for the spectrometer data set), this metric showed a strong negative correlation to green color measured from digital photos, which suggests that the two methods quantified related aspects of egg coloration. A negative relationship between these two variables makes sense, considering that eggs with more green pigmentation absorb more light and thus have less reflectance. Blue color, by itself, was not correlated with elevation, but both blue and green scores from digital photos likely represent the same pigment, biliverdin, which is the only pigment known to cause blue-green coloration in bird eggs (Kennedy and Vevers 1976). This suggests that color variation resulting from biliverdin deposition may be better detected in the green channel of digital color. Alternatively, this could also be caused by nonlinearity in the response of the camera's sensors (Stevens et al. 2007), which may overrepresent some wavelengths, such as green, where humans have peak absorbance in medium and longwave cones (Cuthill 2006). Nevertheless, considering that the data were collected under highly variable field conditions, the fact that two different methods produced complementary results indicates that our digital photo method was able to overcome whatever noise was introduced by the process of digitizing and standardizing reflected light. This speaks to the promise of digital photography as an important tool for field biologists, especially as methods are further refined and standardized (Villafuerte and Negro 1998, Stevens et al. 2007, Bergman and Beehner 2008). To our knowledge, our results are the first to document small-scale, spatially structured differences in eggshell appearance. We are aware of only one other study that demonstrated differentiation of egg characteristics at different elevations. In the Red-winged Blackbird (Agelaius phoeniceus) and the native chicken of India (Gallus gallus), pore area was reduced at high elevation to prevent evaporation that proceeds more rapidly at low barometric pressure (Rahn et al. 1977). However, these differences were not observed between populations connected by gene flow, as in the system studied here (McCormack and Smith 2008). Our results, and those of previous studies that demonstrated phenotypic divergence along elevation gradients despite the potential for gene flow, indicate that elevation gradients can be important to the generation of intraspecific diversity in morphological traits (Price 1991, Soobramoney et al. 2005, Kleindorfer et al. 2006, Bears et al. 2008), life history (Bears et al. 2009), and plumage characteristics (Graves 1985). Furthermore, there is also evidence of divergence in bill traits among the populations of Mexican Jays studied here (McCormack and Smith 2008), which suggests that the Sierra del Carmen may be a particularly important source of elevational divergence. Whether this pattern is specific to Mexican Jays or occurs in other species that experience niche expansion in the Sierra del Carmen (Miller 1955) awaits further research. Our conclusion that local differentiation can contribute to variation in egg color also stands in contrast to many studies of eggshell variation that were focused on identity signaling (e.g., Collias 1993, Dale 2006) and, therefore, either explicitly or implicitly ascribed maintenance of variation to frequency-dependent selection. It is important to note, however, that we have not ruled out frequency-dependent selection as a force that contributes to variation in both speckling and coloration of eggs in this population. The link between intensity of blue-green egg color and female condition has been established in several species, including Pied Flycatcher (Ficedula hypoleuca; Moreno et al. 2005, 2006), Eastern Bluebird (Sialia sialis; Siefferman et al. 2006), Gray Catbird (Dumetella carolinensis; Hanley et al. 2008), and Spotless Starling (Sturnus unicolor;Soler et al. 2008). These results have often been used to satisfy intermediate assumptions of the hypothesis that blue-green eggs are a sexually selected signal to males (Moreno and Osorno 2003; but see Reynolds et al. 2009). However, a link between condition and egg color could also develop as a byproduct—for example, if females in better condition produce more biliverdin, which is then deposited in eggshells in higher quantities without a signaling function. Given the evidence for a general pattern of condition-dependent blue-green egg coloration in birds, we investigated whether differences in condition along the habitat gradient in the Sierra del Carmen might be related to the observed differences in egg color. Previous studies on this population have suggested a link between elevation and condition: at high elevation, flock sizes are larger (Bhagabati and Horvath 2006), ectoparasite loads are lower (McCormack 2007), and mast-seeding trees occur in higher density (McCormack 2007), which likely leads to more abundant food resources. Nevertheless, we found no relationship between blue-green egg color and a surrogate of female condition, egg volume (Amat et al. 2001, Parker 2002). We likewise found no evidence that body condition varied along the elevation gradient. These results suggest that differences in condition were not the cause of the observed elevational differences in egg color; however, this conclusion should be considered tentative, given that we did not assess body condition of known egg layers. Another possibility is that the differences in egg color are a genetic response to differential selection pressures at high and low elevation. Considering the small spatial scale of the differences, this scenario would require several restrictive conditions: selection is strong, gene flow is restricted, and variation in blue-green egg color is heritable. Previous genetic work on Mexican Jays in the Sierra del Carmen showed moderately restricted gene flow along the elevation gradient (McCormack and Smith 2008). This result, combined with natural-history data that indicate strong philopatry (McCormack and Brown 2008), makes Mexican Jays among the more likely avian candidates for local microevolution. We have no information on heritability of egg color in Mexican Jays, but in poultry blue coloration is thought to be a Mendelian trait, dominant to white (Punnett 1933). A study on Village Weavers (Ploceus cucullatus) demonstrated a heritable basis to more subtle variation in blue-green color and speckling (Collias 1993) similar to that found in Mexican Jays. As for the selective agents, one candidate is elevational differences in solar radiation, which can drive rapid differentiation in blue-green egg color (Lahti 2008). Mexican Jays may be particularly susceptible to the effects of solar radiation (e.g., overheating and UV damage) because they are open-cup-nesters and their egg-laying stage coincides with leaf regeneration in the evergreen oaks (Quercus spp.) in which they commonly nest (McCormack and Brown 2008), which leads to increased egg exposure in largely denuded trees. Additional study is required to test this and other hypotheses (e.g., crypsis) that involve divergent selection between differential light environments. In summary, we have shown that blue-green egg color in Mexican Jays differs between high and low elevations in the Sierra del Carmen. These differences have, at least in part, contributed to the high degree of variation found in Mexican Jay eggs in this mountain range. Our results demonstrate how local differentiation can contribute to generation and maintenance of variation in egg color. In contrast to the results of other studies, blue-green egg color was not linked to surrogates of female condition. Further study is needed to determine the environmental and genetic components of variance in these egg color differences and whether they result from differential selection pressures or are a neutral by-product of environmental differences. Acknowledgments We thank CEMEX, the McKinneys, D. Roe, and the Del Carmen Project staff for support and access to the land. J. Brotman, A. Byrd, E. Landay, G. Levandoski, E. Miller, E. Peñaloza, and M. Starling helped collect data. M. Sheehan, D. Hanley, K. McGraw, and three anonymous reviewers provided helpful comments on the manuscript. All field procedures were approved by University of California (UC) Animal Use and Care Protocol #2005-126-02. Field research was funded by a UC Mexus Doctoral Dissertation Grant and a Sigma Xi Grant-in-Aid of Research to J.E.M. and an American Philosophical Society Franklin Research Grant to E.C.B. The work of E.C.B. during preparation of the manuscript was supported in part by National Science Foundation grant IOS0639370 to M. T. Murphy. Literature Cited Amat , J. A. , R. M. Fraga , and G. M. Arroyo . 2001 . Variations in body condition and egg characteristics of female Kentish Plovers Charadrius alexandrinus. Ardea 89 : 293 – 299 . WorldCat Bears , H. , M. C. Drever , and K. Martin . 2008 . 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TI - Small-Scale Divergence in Egg Color Along An Elevation Gradient in the Mexican Jay (Aphelocoma ultramarina): A Condition-Dependent Response?Divergencia a Pequeña Escala en la Coloración de los Huevos en un Gradiente de Elevación en Aphelocoma ultramarina: ¿Una Respuesta Dependiente de la Condición?
JO - Auk: Ornithological Advances
DO - 10.1525/auk.2009.09043
DA - 2010-01-01
UR - https://www.deepdyve.com/lp/oxford-university-press/small-scale-divergence-in-egg-color-along-an-elevation-gradient-in-the-6Y3vfus5DS
SP - 35
VL - 127
IS - 1
DP - DeepDyve
ER -