Abstract

When females vary in reproductive quality, they may be selected to honestly signal that quality and males may be selected to express mate choice based on this variation. In the striped plateau lizard, females with larger and more saturated orange throat patches are of higher phenotypic quality, and males preferentially associate with brighter females. Here, we assess whether this female ornament conveys fitness benefits by relating female ornamentation to offspring quality. We housed groups of male and female Sceloporus virgatus in outdoor enclosures, tracked the seasonal color development of females to determine peak ornament expression, measured offspring body condition from hatching to day 180, and measured offspring sprint speed at day 180. Although we did not eliminate the possibility of assortative mating within enclosures, we controlled for these potential effects by exposing females to small groups of similarly sized males and by including maternal body size, maternal body condition, and egg mass as covariates in our statistical models. Offspring body condition was reliably predicted by female ornament size but not by ornament color intensity or saturation. Similarly, offspring sprint speed was predicted only by ornament size and not by color intensity or saturation. Females with large ornaments tended to produce offspring with higher body condition and faster offspring than did females with small ornaments. These results are consistent with the hypothesis that males may gain fitness benefits from preferentially allocating their reproductive effort toward females with larger orange patches by producing higher quality offspring. Possible mechanisms underlying such female-ornament–offspring-quality relationships are discussed.

The mechanisms underlying the origin and maintenance of male ornaments and female mate preferences have been a key focus of evolutionary biologists for decades (reviewed by Andersson 1994; Kokko et al. 2003). A well-studied category of mechanisms, indicator mechanisms, suggests that females prefer males with well-developed ornaments because these ornaments honestly indicate male condition or viability (Zahavi 1975; Andersson 1994; Kokko et al. 2003). Females may benefit from such preferences directly or indirectly by increasing the phenotypic or genotypic quality of their offspring, and positive relationships between offspring quality and male ornament expression are often used as evidence in support of indicator mechanisms (Andersson 1994; Møller 1994; Kokko et al. 2002; Eilertsen et al. 2009). Bird song is as an example of a well-studied indicator signal, and in this system we know that female songbirds often prefer males with larger song repertoires (e.g., Yasukawa et al. 1980; Searcy 1984), that repertoire size can honestly indicate males’ ability to withstand developmental stressors (Nowicki et al. 1998, 2002), and that males with larger repertoires produce offspring that have increased survivorship (Hasselquist et al. 1996) and reproductive success (Reid et al. 2005). Offspring quality is only rarely measured as overall survival or fitness of the offspring (Møller and Alatalo 1999; Kokko et al. 2003) and instead is frequently measured via proxies of fitness such as body condition (Parker 2003), sprint speed (Nicoletto 1994), predator avoidance skills (Evans et al. 2004), growth rates (Reynolds and Gross 1992; Petrie 1994), and immune response (Hamilton and Zuk 1982; Johnsen et al. 2000).

Recently, there has been an increased interest in the evolution of female ornaments (e.g., ornamental color in female birds: Irwin 1994; Amundsen et al. 1997; Amundsen 2000; Roulin et al. 2000; Griggio et al. 2005; reptiles: LeBas and Marshall 2000; Hagar 2001; Weiss 2002; and fish: Rowland et al. 1991; Amundsen and Forsgren 2001; Massironi et al. 2005). Although once considered to be detrimental to fitness or perhaps neutral to selection and a consequence of a genetic correlation to male ornaments (Lande 1980), female ornaments are now being examined as a product of sexual selection (see reviews by Amundsen 2000; Kraaijeveld et al. 2007; Clutton-Brock 2009). Indeed, the degree of ornamentation expressed by a female may influence female–female competition or male mate choice (West-Eberhard 1983; Amundsen 2000). Male mate choice may be expected in species with conventional sex roles when variation in female quality is high (Parker 1983; Owens and Thompson 1994). Analogous to studies of the evolution of male ornaments by female mate choice, female ornaments should be examined for their effect on male mate choice decisions, their relationship to female quality, and their relationship to offspring quality.

Indeed, the evolution of female ornaments via intersexual selection has been supported by male preferences for more-ornamented females (e.g., Jones and Hunter 1993; Amundsen 2000; Amundsen and Forsgren 2001; Weiss 2002; Griggio et al. 2005; Cornwallis and Birkhead 2007) and by positive relationships between female ornamentation and female quality, including measures of female fecundity (e.g., Potti and Merino 1996; Linville et al. 1998; Domb and Pagel 2001; Hanssen et al. 2006; Weiss 2006; Doutrelant et al. 2008; Huchard et al. 2009). However, results are mixed (reviewed by Amundsen 2000; Kraaijeveld et al. 2007), with a number of studies showing no relationship or a negative relationship (e.g., Mänd et al. 2005) between ornaments and quality in females. Perhaps, the least explored aspect of female sexual selected signals remains the relationship between ornamentation and offspring quality (e.g., Clutton-Brock 2009). An ideal female-ornamented species with which to examine such relationships would express 1) female-specific ornamentation, to avoid confounds suggested by Lande's (1980) genetic correlation hypothesis, 2) no paternal care, to minimize male contribution to offspring quality, and 3) minimal to no maternal care, to further eliminate hypotheses concerning the effect of parental ability on offspring quality. More than 30 species of lizard meet all the above conditions and therefore make excellent systems with which to study sexually selected female ornaments; yet to date, the majority of such work has focused on biparental bird species in which females express reduced forms of male-typical traits. It is only by examining a broad collection of species that we can establish the general principles guiding the evolution of female ornaments.

We have been studying the evolution and function of female ornamentation in the striped plateau lizard, Sceloporus virgatus, which fits the above criteria; they provide no parental care after nest site selection and oviposition by the female, and the ornament is female specific. In many vertebrates, female-specific color is commonly considered a signal of reproductive status as the presence, size, and intensity of the color (called “nuptial color”) often changes in relation to the female reproductive cycle (Rowland et al. 1991; Cooper and Greenberg 1992; Cuadrado 2000; Hagar 2001; Weiss 2002), and males may preferentially court females displaying such color patterns (Amundsen and Forsgren 2001; Weiss 2002; Baird 2004). Among-female variation in the expression of nuptial color, and therefore its potential role as a sexually selected indicator signal, has rarely been addressed (but see Amundsen and Forsgren 2001; Domb and Pagel 2001; Massironi et al. 2005; Weiss 2006). Therefore, little is known about the relationships between the degree of expression of these types of traits and female or offspring quality.

Reproductively active S. virgatus females develop a pair of orange color patches on their throat. Males prefer to associate with and tend to court females manipulated to express bright orange patches more than females manipulated to express pale or no orange patches (Weiss 2002). In addition, females with larger and more saturated orange patches are of higher quality than less-ornamented females, as estimated by larger body size, higher body condition, fewer ectoparasites, and higher average egg mass (Weiss 2006). Thus, males appear to make reproductive decisions on the basis of a female ornament that reliably indicates important aspects of female fitness. It is still unknown, however, what benefits males may gain from their preference for more-ornamented females. Weiss (2006) found no relationship between female color expression and clutch size, suggesting that the opportunity for males to benefit via the production of a greater quantity of offspring may be absent or low. Here, to assess possible benefits to the male via the production of higher quality offspring, we related the color expression of female S. virgatus to the body condition and sprint speed of her offspring.

METHODS

Study species

Sceloporus virgatus is a small, mostly brown lizard that inhabits the mountains of southeastern Arizona, southwestern New Mexico, and northern Mexico. When not reproductively active, males and females are virtually identical in their coloration and patterning with both sexes expressing small blue throat patches; however, females are generally larger than males (data herein). During the reproductive season (from mid-May to early July), females develop 2 bright orange patches on the underside of the throat (see Figure 1 from Weiss 2006) that gradually fade after the female has ovulated (Weiss 2002). These ornaments do not appear to influence female–female competition over food or basking sites (Weiss 2005), and overall, direct female–female aggression is relatively uncommon in this species (Weiss SL, personal observation).

Females produce 1 clutch per year (Vinegar 1975) during a relatively short and synchronous reproductive season; at the study population, male courtship behavior peaks in May and ovulation (i.e., the transition from female receptivity to nonreceptivity) tends to occur in an approximately 2-week period beginning in late May or early June (Weiss 2002; unpublished data). Males generally mate with more than 1 female, and females also can mate with more than 1 male. Thus, offspring from a single clutch can have more than 1 sire (Abell 1997). However, Abell (1997) found that the S. virgatus male that maintains the greatest spatial proximity to a female during the mating season is the most probable sire of that female's offspring. Given the time constraints imposed by the short, synchronous reproductive season and the reproductive benefits obtained by establishing close spatial relationships with females, males are predicted to be discriminatory in how they allocate their time and energy toward individual females in a way that increases their reproductive success.

Figure 1

The bivariate relationship between offspring body condition and maternal (a) orange area and (b) body condition at the time of peak ornament expression and (c) egg mass. Offspring body condition measurements from days 1, 5, 10, 20, 30, 45, 60, 75, 90, and 180 posthatch were averaged for each individual. Vertical groupings in (a) and (b) indicate offspring from one or a few females.

Figure 1

The bivariate relationship between offspring body condition and maternal (a) orange area and (b) body condition at the time of peak ornament expression and (c) egg mass. Offspring body condition measurements from days 1, 5, 10, 20, 30, 45, 60, 75, 90, and 180 posthatch were averaged for each individual. Vertical groupings in (a) and (b) indicate offspring from one or a few females.

Animal maintenance

We captured 45 females (mean snout-to-vent length [SVL] [±standard error]: 62.0 ± 0.4 mm; mean body mass: 7.6 ± 0.5 g) and 15 males (mean SVL: 56.5 ± 0.4 mm; mean body mass: 5.5 ± 0.1 g) by noose on 20–24 May 2005 from areas within 4.8 km of the American Museum of Natural History's Southwestern Research Station (SWRS), Portal, AZ. At SWRS, females were randomly assigned to 3 outdoor enclosures (4.3 × 1.7 × 2.2 m; 15 females per enclosure). Each enclosure contained a soil substrate and several rocks, logs, and bricks for perches and shelter. Each enclosure also contained 5 randomly assigned males. Within enclosures, animals were allowed to mate freely, and thus, it is possible that assortative mating occurred (e.g., larger females may have mated with larger males); however, there is no evidence of size-based assortative mating in free-ranging S. virgatus (Abell 1998). Further, within the size class of males used in this study, there is no tendency for male reproductive success to vary with body size or with the size or intensity of their blue dewlap coloration (Abell 1997), and male body size is unrelated to the fertility of his mate (Abell 1998). Regardless, we attempted to reduce the potential impact of assortative mating on our results by limiting female access to a small set of similarly sized males (SVL average CVwithin enclosures = 3.0 ± 0.2%), by having similarly sized sets of males in all 3 enclosures (SVL CVamong enclosures = 0.4%), and by statistically controlling for 3 factors that could influence or be influenced by assortative mating: female body size, female body condition, and egg mass (detailed below). Animals were toe-clipped for individual identification and provided water ad libitum. About 50 crickets (Acheta sp.) were added to each enclosure every other day. All females gravid by 20 June 2005 were transported back to the University of Puget Sound (UPS), Tacoma, WA, over a 3-day period in individual cloth bags inside a chilled cooler.

At UPS, we housed adult females (n = 19) in glass tanks (26 × 32 × 51 cm) with 4–5 individuals per tank. Females were maintained on a 14:10 h light:dark cycle with 40 W full spectrum and black lights suspended over all cages. Additional light was provided by a 40 W incandescent light suspended in a reflector over the rear of each cage. This setup created an approximate 5.5 °C temperature gradient during the day, allowing for behavioral thermoregulation. Tanks contained a soil substrate to allow for species-typical burrowing behavior as well as polyvinyl chloride (PVC) shelters and a wooden ramp angled up from the substrate to the top of the cage. Adult females were provided with water ad libitum and crickets 3–4 times per week.

Females oviposit at the onset of the summer rainy season, typically in early July, but do not oviposit naturally in captivity (Weiss et al. 2002). Thus, we induced oviposition on 7 July 2005 via intraperitoneal injection of 2 USP units of oxytocin in 0.1 ml aqueous solution; some eggs (13.4%), however, had to be obtained by dissection. Eggs (199 total; 172 fertilized as determined by a visible embryonic disk) were weighed, incubated at 28 °C in individual cups of moist vermiculite covered with parafilm, and checked daily for hatchlings. Hatching success of fertilized eggs was 93.6%, resulting in 161 hatchlings (mean: 8.5 ± 0.9 hatchlings per female). One individual, born with a spinal deformity, was removed as an outlier from all analyses.

On emergence, hatchlings were housed in groups of 10 individuals, established haphazardly by day of hatch (i.e., 1 tank was filled with 10 individuals before the next tank began to be filled), except for the final tank that housed 11 individuals. Rearing tanks included a mix of sibs and nonsibs, except for the first tank that contained all sibs (because the first 10 individuals to hatch were from the same mother). To hatchlings, we provided calcium powdered fruit flies (Drosophila sp.) daily. We began feeding the hatchlings calcium powdered crickets (Acheta sp.) in addition to fruit flies after all individuals were more than 35 days old and reduced feedings to 4 times per week on 4 December 2005 (when hatchlings were 90–113 days old). On 9 December 2005, hatchlings were rearranged into single-sex groups of 4–6 individuals. Hatchling tanks were maintained similarly to those of adult females but included a brick instead of PVC shelters. Each hatchling was permanently marked by toe-clipping.

Measuring maternal characteristics

Female coloration develops over the course of several weeks, and patches reach a peak in size and intensity at about the time the female ovulates, though color intensity tends to peak before patch size (Weiss 2002). For analyses, we wanted to use characteristics of the female on the date of overall peak ornament expression. Thus, we tracked female color development and determined peak ornament expression as follows. Every 2–4 days from 25 May to 22 June 2005 we matched each female's developing throat color to Munsell color chips (Weiss 2002). Munsell chips are classified by individual measures of value (intensity or amount of white), chroma (saturation or purity of color), and hue (shade of color). Because the hue of each animal was measured to be the same (10R), it was excluded from analyses. Color measurements were standardized by using one person (S.L.W.) and a standardized light source (a flashlight) to collect these data. At the same time, we also photographed the right color patch of every female (along with a calibration scale) using an Olympus Camedia 5.0 mega-pixel digital camera, and we measured SVL and body mass. An independent viewer (L. D. Lucas) and E.A.K. separately examined every individual's series of photographs to visually determine the date at which that individual's ornamentation reached its peak expression. In cases of disagreement, a third viewer (S.L.W.) independently analyzed the photo series, and peak expression was determined to occur on the date that had the most agreement between viewers.

We analyzed these peak photographs using an automated “select color” command in Adobe Photoshop CS2 9.0 to standardize the color shade selection, and we calculated the area of the selected region in square millimeter, hereafter called “orange area,” using Scion Image release Alpha 4.0.3.2. Other maternal characteristics on the day of peak ornament expression (value and chroma of patch, SVL, and body condition [ratio of body mass to SVL3 in units of gram per cubic centimeter]) were also used for analyses.

Measuring offspring quality

Body condition

We measured body mass and SVL of each individual throughout development, when offspring were 1, 5, 10, 20, 30, 45, 60, 75, 90, and 179–181 (referred to as 180) days old, and used the ratio of body mass to SVL3 (in units of gram per cubic centimeter) as our measure of body condition. To determine SVL, we placed individuals into an ice water bath for a few seconds until they were immobile and then measured SVL with digital calipers. Individuals were aroused naturally at room temperature.

Sprint speed

At 180–182 (referred to as 180) days old, offspring were incited to run down a 1-m racetrack by gentle tapping of the tail with a paintbrush (Tsuji et al. 1989; van Berkum et al. 1989). The time at which the lizard passed photocell stations (Pasco Scientific digital photogate timers) positioned at 0, 0.5, and 1.0 m was logged (Huey et al. 1981). Each individual was raced 3 times on a single day with a mean rest time of 15.4 ± 0.1 min (range: 13–30 min) between runs. The fastest 0.5 m distance was used to determine an individual's sprint speed (meter per second). We controlled for the effect of body temperature on sprint speed by placing animals in an incubator at 33 °C on the day prior to racing; in the field, S. virgatus maintains an average body temperature of 33.4 °C (Smith and Ballinger 1994). Animals were returned to their normal housing environment after their third sprint trial. Data from one individual, who resisted running down the track and did not complete a single 1-m trial run, were excluded from analyses.

Statistical analyses

Statistical analyses were conducted using the software R (R Development Core Team 2008). To verify that adult males and females were assigned to enclosures at SWRS in an unbiased way, we used analysis of variance tests to compare the SVL and body mass of individuals in each enclosure (separately for males and females). The relationship between our 2 estimates of offspring phenotype was examined by correlation.

Four females did not have any offspring survive to day 180 (in fact none of their offspring survived to day 60); these females contributed to the analysis of offspring body condition but not to the analysis of offspring sprint speed. We used t-tests or Mann–Whitney U tests to determine whether these 4 females differed from the other females in their reproductive output, and we used logistic regression to determine whether these 2 groups of females differed from each other in terms of the maternal phenotypic variables considered in the study (i.e., orange area, value, chroma, body condition, and SVL at peak ornament expression).

To determine relationships between maternal characteristics and offspring body condition, we performed hierarchical mixed model analysis using the lme4 package in R (Bates et al. 2008) and used restricted maximum likelihood to fit the model. The model included offspring body condition as the response variable, offspring age as a repeated factor, and characteristics of maternal peak ornament expression (orange area, value, and chroma) as covariates. To partially control for the potential impact of assortative mating within enclosures (though no evidence of assortative mating has been documented for the size class of individuals used in this study; Abell 1997, 1998), we included female body size, female body mass, and offspring egg mass as additional covariates in our model; a second reason to include these 3 covariates is that they each have previously been found to positively relate to aspects of female ornamentation (Weiss 2006). To control for the lack of independence of offspring, we included mother ID as a random effect. Finally, to control for offspring rearing conditions, we included rearing tanks (mixed-sex tanks until 9 December 2005 and single-sex tanks for remainder of study) as well as the interaction between the 2 tanks as additional random effects; the random-effect coefficients give estimates of the standard deviations in each group. After much consideration of biological factors, we chose to present only this one full model, deemed the most biologically appropriate, rather than to shape the model based on the solely statistical decisions involved in model selection. Although the Akaike information criterion of the model can be greatly improved by removing all random effects, such a model seems less biologically relevant and, importantly, produced no difference in the overall interpretation.

To determine relationships between maternal characteristics and offspring sprint speed, we performed a similar hierarchical mixed model analysis. This model excluded age (as sprint speed was measured at only one time point) but included the remaining 6 fixed factors and 4 random effects described above.

Because the appropriate number of degrees of freedom to use in assessing the statistical significance in mixed-effects models is controversial (Baayen et al. 2008), we present 2 methods to assess the significance of the factors in our models. First, as recommended by Bates et al. (2008), we present model coefficients with estimates of highest posterior density (HPD) intervals, which are similar to confidence intervals, calculated at the 95% level using Markov chain Monte Carlo (MCMC) sampling with 10 000 samples. In this case, a coefficient is deemed significantly different from zero when the HPD interval does not include zero. Second, as recommended by Baayen et al. (2008), we used MCMC sampling (again, with 10 000 samples) to calculate P values based on the posterior distribution with the languageR package (Baayen 2008) in R. These P values are only provided for fixed factors; the statistical literature suggests that there is no reliable method to generate accurate P values for random effects in models such as the ones we present here.

RESULTS

Adult males of the 3 enclosures neither differ in mean SVL (F2,12 = 0.09, P = 0.91) nor in mean body mass (F2,12 = 0.38, P = 0.69). Similarly, females of the 3 enclosures did not differ in either of these variables (SVL: F2,42 = 0.32, P = 0.73; body mass: F2,42 = 0.65, P = 0.53). Females that became gravid by 20 June were bigger and heavier at the time of initial capture than females that did not become gravid (SVL: 62.8 ± 0.6 mm vs. 61.0 ± 0.5 mm, t43 = 2.08, P = 0.04; body mass: 8.7 ± 0.3 g vs. 7.6 ± 0.2 g, t43 = 3.29, P = 0.002). Of females that provided offspring to this study, the 4 females who had no offspring surviving to 180 days old had significantly fewer eggs hatch (3.8 ± 1.1 hatchlings) than did the rest of the females (9.7 ± 0.9 hatchlings; t17 = 3.27, P = 0.005); this is due to a lower fertilization success (60.7 ± 16.1% vs. 91.4 ± 3.8%; t17 = 2.87, P = 0.01) and not a difference in the total number of eggs produced (9.0 ± 1.5 vs. 10.9 ± 0.7; U18 = 18.5, P = 0.25). However, these 2 groups of females did not differ in any of the maternal phenotypic variables considered in the hierarchical mixed model analyses (Table 1). Our 2 estimates of offspring quality—body condition and sprint speed—were uncorrelated with each other (r57 = −0.05, P > 0.70).

Table 1

Logistic regression comparing phenotype of females that did and did not have offspring survive to 180 days old

Parameter Coefficient estimate Z P 
Peak area (mm20.1703 1.30 0.20 
Peak value 0.3909 0.92 0.36 
Peak chroma 0.0135 0.10 0.92 
Body condition (g/cm3−258.3773 −1.49 0.14 
Body size (mm) −0.0289 −0.25 0.81 
Parameter Coefficient estimate Z P 
Peak area (mm20.1703 1.30 0.20 
Peak value 0.3909 0.92 0.36 
Peak chroma 0.0135 0.10 0.92 
Body condition (g/cm3−258.3773 −1.49 0.14 
Body size (mm) −0.0289 −0.25 0.81 

Offspring body condition

The only maternal characteristics significantly related to offspring body condition were peak orange area and body condition (Table 2). When accounting for the effects of other model parameters, females with larger orange patches (HPD interval: 0.0002 to 0.0009 (g/cm3)/(mm2); P = 0.009) and females with lower body condition (HPD interval: −1.3973 to −0.2378; P = 0.01) tended to produce offspring with higher body condition (Figure 1). No significant relationship was found between offspring body condition and either maternal color value (i.e., intensity; HPD interval: −0.0008 to 0.0013 g/cm3, P = 0.60) or color chroma (i.e., saturation; HPD interval: −0.0002 to 0.0006 g/cm3, P = 0.27) at peak ornament expression; however, there was a nearly significant negative relationship between offspring body condition and maternal SVL (HPD interval: −0.0006 to 0.49 × 10−5 (g/cm3)/(mm), P = 0.06) at peak ornament expression (Table 2). Offspring of higher body condition tended to hatch from heavier eggs (HPD interval: 0.0059 to 0.0286 (g/cm3)/(g); P = 0.003; Figure 1 and Table 2).

Table 2

Hierarchical mixed model relating maternal phenotype to offspring body condition

Parameter Mean ± SE Coefficient estimate HPD interval P 
Peak area (mm22.59 ± 0.52 0.0005 (0.0002, 0.0009) 0.01 
Peak value 4.8 ± 0.2 0.0002 (−0.0008, 0.0013) 0.60 
Peak chroma 12.4 ± 0.5 0.0002 (−0.0002, 0.0006) 0.27 
Body condition (g/cm30.0298 ± 0.0005 −0.7736 (−1.3973, −0.2378) 0.01 
Body size (mm) 64.3 ± 0.7 −0.0003 (−0.0006, 0.49 × 10−50.06 
Egg mass (g) 0.345 ± 0.004 0.0179 (0.0059, 0.0286) 0.003 
Offspring ID (age) — 0.47 × 10−4 (0.35 × 10−4, 0.53 × 10−4— 
Mother ID — 0.0014 (0, 0.0017) — 
Rearing tank 1 — 0.16 × 10−6 (0, 0.0008) — 
Rearing tank 2 — 0.51 × 10−7 (0, 0.0010) — 
Tank 1 × tank 2 — 0.0012 (0, 0.0012) — 
Residual — 0.0030 (0.0026, 0.0029) — 
Parameter Mean ± SE Coefficient estimate HPD interval P 
Peak area (mm22.59 ± 0.52 0.0005 (0.0002, 0.0009) 0.01 
Peak value 4.8 ± 0.2 0.0002 (−0.0008, 0.0013) 0.60 
Peak chroma 12.4 ± 0.5 0.0002 (−0.0002, 0.0006) 0.27 
Body condition (g/cm30.0298 ± 0.0005 −0.7736 (−1.3973, −0.2378) 0.01 
Body size (mm) 64.3 ± 0.7 −0.0003 (−0.0006, 0.49 × 10−50.06 
Egg mass (g) 0.345 ± 0.004 0.0179 (0.0059, 0.0286) 0.003 
Offspring ID (age) — 0.47 × 10−4 (0.35 × 10−4, 0.53 × 10−4— 
Mother ID — 0.0014 (0, 0.0017) — 
Rearing tank 1 — 0.16 × 10−6 (0, 0.0008) — 
Rearing tank 2 — 0.51 × 10−7 (0, 0.0010) — 
Tank 1 × tank 2 — 0.0012 (0, 0.0012) — 
Residual — 0.0030 (0.0026, 0.0029) — 

HPD intervals that exclude zero and P < 0.05 indicate significant effects. SE, standard error.

Offspring sprint speed

Peak orange area and body size were the only maternal characteristics significantly related to offspring sprint speed (Table 3). When accounting for the effects of other model parameters, females with larger patches (HPD interval: 0.0056 to 0.0437 (m/s)/(mm2); P = 0.02) and females of smaller body size (HPD interval: −0.0401 to −0.0019 (m/s)/(mm); P = 0.03) tended to produce faster offspring (Figure 2). There were nearly significant relationships between offspring sprint speed and maternal peak color value (HPD interval: −0.0036 to 0.1090 m/s; P = 0.052) and maternal body condition (HPD interval: −56.8406 to 1.4160 (m/s)/(g/cm3); P = 0.07), and offspring spring speed was unrelated to maternal peak chroma (HPD interval: −0.0218 to 0.0151 m/s, P = 0.75) (Table 3). Offspring sprint speed was also unrelated to egg mass (HPD interval: −1.3135 to 0.0595 (m/s)/(g); P = 0.09; Table 3).

Table 3

Hierarchical mixed model relating maternal phenotype to offspring sprint speed

Parameter Mean ± SE Coefficient estimate HPD interval P 
Peak area (mm22.95 ± 0.62 0.0234 (0.0056, 0.0437) 0.02 
Peak value 4.7 ± 0.2 0.0528 (−0.0036, 0.1090) 0.052 
Peak chroma 12.4 ± 0.6 −0.0038 (−0.0218, 0.0151) 0.75 
Body condition (g/cm30.0299 ± 0.0005 −27.6599 (−56.8406, 1.4160) 0.07 
Body size (mm) 64.3 ± 0.8 −0.0205 (−0.0401, −0.0019) 0.03 
Egg mass (g) 0.342 ± 0.008 −0.4361 (−1.3135, 0.0595) 0.09 
Mother ID — 0.0946 (0, 0.0559) — 
Rearing tank 1 — 0.40 × 10−5 (0, 0.0441) — 
Rearing tank 2 — 0.0489 (0, 0.0513) — 
Tank 1 × tank 2 — 0.69 × 10−6 (0, 0.0334) — 
Residual — 0.1919 (0, 0.1309) — 
Parameter Mean ± SE Coefficient estimate HPD interval P 
Peak area (mm22.95 ± 0.62 0.0234 (0.0056, 0.0437) 0.02 
Peak value 4.7 ± 0.2 0.0528 (−0.0036, 0.1090) 0.052 
Peak chroma 12.4 ± 0.6 −0.0038 (−0.0218, 0.0151) 0.75 
Body condition (g/cm30.0299 ± 0.0005 −27.6599 (−56.8406, 1.4160) 0.07 
Body size (mm) 64.3 ± 0.8 −0.0205 (−0.0401, −0.0019) 0.03 
Egg mass (g) 0.342 ± 0.008 −0.4361 (−1.3135, 0.0595) 0.09 
Mother ID — 0.0946 (0, 0.0559) — 
Rearing tank 1 — 0.40 × 10−5 (0, 0.0441) — 
Rearing tank 2 — 0.0489 (0, 0.0513) — 
Tank 1 × tank 2 — 0.69 × 10−6 (0, 0.0334) — 
Residual — 0.1919 (0, 0.1309) — 

HPD intervals that exclude zero and P < 0.05 indicate significant effects. SE, standard error.

Figure 2

The relationship between offspring sprint speed at day 180 and maternal (a) orange area and (b) body size at the time of peak ornament expression. Vertical groupings indicate offspring from one or a few females.

Figure 2

The relationship between offspring sprint speed at day 180 and maternal (a) orange area and (b) body size at the time of peak ornament expression. Vertical groupings indicate offspring from one or a few females.

DISCUSSION

We have shown that more-ornamented female striped plateau lizards tend to produce offspring that are in better body condition and produce faster offspring than do less-ornamented females. Specifically, we found that maternal ornament size, but not ornament intensity or saturation, predicts these 2 aspects of offspring phenotype. In congeners of S. virgatus, both body condition and sprint speed are repeatable over ontogeny, possibly up to a year, and additionally, sprint speed is repeatable year to year among adults (Huey and Dunham 1987; van Berkum et al. 1989). Further, these characters can potentially affect survival, social dominance, and reproductive success (e.g., Abell 1999; Civantos and Forsman 2000; Robson and Miles 2000; Warner and Andrews 2002; Husak 2006; Husak et al. 2006; Salvador et al. 2008). Therefore, S. virgatus males that assess and prefer larger ornamented females may produce offspring with greater fitness, on average, than do males that mate randomly with respect to female ornament size. These findings provide a possible route by which S. virgatus males can benefit from mate discrimination behavior and are consistent with an indicator mechanism underlying the evolution of female ornament size and male mate choice.

Offspring characteristics were also related to nonornamental characteristics of the mother and to egg mass. Offspring body condition was negatively related to maternal body condition and positively related to egg mass; offspring sprint speed was negatively related to maternal body size. Although a full understanding of these relationships will require additional analyses and experimentation outside the scope of this current study, they may be partially explained by positive trends found between both the body condition and the size of mothers with clutch size and negative relationships between clutch size and both egg mass and offspring body mass found for S. virgatus by Abell (1999); body mass is generally found to be positively related to sprint speed within populations of lizards (e.g., Huey and Hertz 1982; Garland and Losos 1994). Informal post hoc exploration of our own data (not presented) found at least weak support for each of these relationships. Thus, females that are in good condition and are large may trade-off egg and offspring mass for offspring number, and offspring of low mass tend to be slow. This additionally suggests that slower hatchlings should emerge from smaller eggs, which has been found in another Sceloporus lizard (Sinervo 1990); however, we found no such relationship here.

There are several nonmutually exclusive mechanisms by which a more-ornamented female may produce higher quality offspring. Because S. virgatus provides no parental care other than nest site selection by the female, hypotheses concerning the effect of female ornamentation on male or female parental effort and/or parental ability (e.g., Burley 1986; Hoelzer 1989; Linville et al. 1998; Smiseth and Amundsen 2000; Griggio et al. 2003) can be discarded and we can focus on mechanisms concerning genetic and nongenetic provisioning to the egg.

One potential mechanism underlying female-ornament–offspring-quality relationships is that more-ornamented females may gain access to more or higher quality males (Burley 1986), which benefits offspring quality via an enhanced complementarity between the maternal and paternal genomes or a higher quality paternal genetic contribution (Madsen et al. 1992; Foerster et al. 2003; Neff and Pitcher 2005). Such a mechanism represents an adaptive benefit to the female for ornament expression and may be critical to the evolution of female ornaments. Weiss (2006) hypothesized that S. virgatus females may benefit from their ornamentation in this way by attracting males into their home range, possibly inciting male–male competition, while they themselves remain sedentary and thus reduce energy expended on mate searching. However, a recent review suggests that indirect genetic benefits to females have only weak support among reptiles (Uller and Olsson 2008; but also see Madsen 2008). Further, even if such a mechanism were operating in free-ranging populations, we suggest that it is unlikely to strongly impact our current results. The study presented here minimized mate-searching costs by maintaining small groups of males and females in enclosures and was designed to experimentally reduce (though not eliminate) the potential impact of male genetic quality by 1) limiting females to a small set of similarly sized males as potential mates and 2) statistically controlling for female body size and body condition—potential proxies of paternal body size and condition if assortative mating was occurring within the limited degree of male variation present in each enclosure. Further, recall that Abell (1997, 1998) found no evidence of assortative mating for the size class of individuals used in this study. Experimentally eliminating this mechanism requires controlled mating trials, which would be an interesting avenue for further study. Studies that instead directly tested for such a mechanism in free-ranging populations also would make valuable contributions to our understanding of female ornamentation.

Certainly the capability of passing on high-quality genes to offspring is not limited to males given that fathers and mothers contribute equally to offspring genotype. Thus, a second potential mechanism underlying the relationships found herein is that the ornament size expressed by a female is indicative of her own genetic quality and that larger ornamented, higher genetic quality females pass along their higher quality genes to their offspring. A third potential mechanism involves nongenetic contributions that mothers make to their offspring (i.e., maternal effects); variation in female ornamentation may correlate to variation in the provisioning of maternally derived yolk components in a way that influences embryonic development and thus offspring quality (Mousseau and Fox 1998; Svensson et al. 2006). Previous work has shown that maternal contributions to yolk can influence offspring body condition, behavior, ectoparasite susceptibility, and survival in common lizards (Lacerta vivipara; de Fraipont et al. 2000; Uller and Olsson 2003; Belliure et al. 2004; Meylan and Clobert 2005). It is therefore possible that our results are due to differential investment by S. virgatus females of some yolk components that influence offspring body condition and speed. In support of this hypothesis, a positive relationship between yolk antioxidant content and ornament size, but not ornament intensity or saturation, has recently been discovered in S. virgatus (Weiss SL, Kennedy EA, Safran RJ, and McGraw KJ, in preparation); it is intriguing that the same ornament characteristic that predicts offspring quality also predicts allocation of yolk antioxidants.

These various mechanisms are not mutually exclusive and may interact. For instance, more-ornamented females may gain access to more-attractive males and then, in response, adjust the allocation to their eggs in a way that maximizes their expected fitness. In species where females receive only sperm from males, as in many lizard species as well as in lekking species, differential investment in offspring by the mother in response to male phenotype would seem to require that a paternal good genes mechanism is also at work (Sheldon 2000; Loyau et al. 2007)—otherwise, it is unclear why a female would allocate more resources to offspring of one sire over those of another. Here, such interactions are at least partially controlled for by including egg mass in our statistical models; female ornament size relates positively to offspring quality when controlling for the effects of egg mass. However, extending the differential allocation hypothesis (Burley 1986) to nonparental species by considering measures of egg composition (e.g., Sheldon 2000) and relating it to benefits of female ornamentation will be an interesting avenue for future research.

Much more work is necessary, across a variety of taxa, both to document female-ornament–offspring-quality relationships, as we did here, and to experimentally address the underlying mechanisms—some of which represent benefits to the female for the expression of the ornament (i.e., male genetic quality) and some of which represent benefits to the male from discriminating among females with different degrees of ornament expression (i.e., female genetic quality or maternal effects). Certainly, whereas female ornaments have begun to attract more attention from evolutionary biologists in recent years, the way in which males might benefit from responding to female attractiveness has lagged behind. A handful of studies have found evidence for male benefits via increased paternity assurance or number of offspring (Berglund et al. 1997; Domb and Pagel 2001; Griggio et al. 2005; Doutrelant et al. 2008; Huchard et al. 2009); far fewer have assessed whether males benefit from their preference via the production of higher quality offspring, which may result in an overall greater number of descendants.

Because an ornament can have several measurable characteristics, each with different developmental trajectories (Weiss 2002) and regulatory mechanisms (Badyaev et al. 2001; Roulin 2004), it is important to examine ornaments as traits that vary along several distinct dimensions. It is possible that all, some, or none of these dimensions may be subject to sexual selection and that those ornament characteristics that do function as indicator signals could each be advertising different benefits. We found that only the size of the maternal ornament, and not its intensity or saturation of color, is positively related to offspring quality. Similarly, Roulin (2004) found that the size, and not number, of melanin-based spots on the plumage of female barn owls (Tyto alba) is predictive of offspring quality, as measured by immunocompetence, parasite resistance, and fluctuating asymmetry. In both species, a single characteristic of the female ornament serves as the best indicator of offspring quality, and assessment of this characteristic may be prioritized by males when making decisions of how to allocate their reproductive effort among available females in nature. From previous work, we know that S. virgatus males preferentially respond to females manipulated to express brighter ornamentation (with ornament size held constant; Weiss 2002) and that both ornament color saturation and size can predict various aspects of female phenotype (Weiss 2006); current work is examining the specific effect of ornament size on male response. The results herein suggest that although males may gain information about female phenotype by assessing both ornament saturation and size, they may benefit from prioritizing information about ornament size by influencing future offspring phenotype. The fact that this female-specific ornament signals any aspect of offspring phenotype, as does female-biased spottiness in barn owls (Roulin 2004), suggests that indicator mechanisms may play an underappreciated role in the evolution of female ornaments.

FUNDING

University of Puget Sound Enrichment Grant to E.A.K. and funds to S.L.W.

We thank Leslie Mayer and Karen Preusch for their help collecting data on offspring sprint speed. We thank LeiLani D. Lucas for her help determining peak ornament expression of mothers. In addition, we thank L. D. Lucas and Pam Michael for assistance with animal care and collection; Michal Morrison, Al Vallecorsa, and the American Museum of Natural History's SWRS for logistical support; Robin Foster and Kevin David for their consultation; and many SWRS researchers and volunteers for their assistance. We thank Jennifer Burnaford, R. Foster, Melissa Hughes, Denise Pope, and Christine Smith for their comments.

References

Abell
AJ
Estimating paternity with spatial behavior and DNA fingerprinting in the striped plateau lizard, Sceloporus virgatus (Phrynosomatidae)
Behav Ecol Sociobiol
 , 
1997
, vol. 
41
 (pg. 
217
-
226
)
Abell
AJ
Phenotypic correlates of male survivorship and reproductive success in the striped plateau lizard, Sceloporus virgatus
Herpetol J
 , 
1998
, vol. 
8
 (pg. 
173
-
180
)
Abell
AJ
Variation in clutch size and offspring size relative to environmental conditions in the lizard Sceloporus virgatus
J Herpetol
 , 
1999
, vol. 
33
 (pg. 
173
-
180
)
Amundsen
T
Why are female birds ornamented?
Trends Ecol Evol
 , 
2000
, vol. 
15
 (pg. 
149
-
155
)
Amundsen
T
Forsgren
E
Male mate choice selects for female coloration in a fish
Proc Natl Acad Sci USA
 , 
2001
, vol. 
98
 (pg. 
13155
-
13160
)
Amundsen
T
Forsgren
E
Hansen
LT
On the function of female ornaments: male bluethroats prefer colourful females
Proc R Soc Lond B
 , 
1997
, vol. 
264
 (pg. 
1579
-
1586
)
Andersson
MP
Sexual selection
 , 
1994
Princeton (NJ)
Princeton University Press
Baayen
RH
language R: data sets and functions with “Analyzing Linguistic Data: A practical introduction to statistics”
 , 
2008
 
R package version 0.953. [cited 2008 December 13]. Available from http://www.R-project.org
Baayen
RH
Davidson
DJ
Bates
DM
Mixed-effects modeling with crossed random effects for subjects and items
J Mem Lang
 , 
2008
, vol. 
59
 (pg. 
390
-
412
)
Badyaev
AV
Hill
GE
Dunn
PO
Glen
JC
Plumage color as a composite trait: development and functional integration of sexual ornamentation
Am Nat
 , 
2001
, vol. 
158
 (pg. 
221
-
235
)
Baird
TA
Reproductive coloration in female collared lizards, Crotophytus collaris, stimulates courtship by males
Herpetologica
 , 
2004
, vol. 
60
 (pg. 
337
-
348
)
Bates
D
Maechler
M
Dai
B
lme4: linear mixed-effects models using S4 classes
 , 
2008
 
R package version 0.999375-27. [cited 2008 December 13]. Available from http://www.R-project.org
Belliure
J
Meylan
S
Clobert
J
Prenatal and postnatal effects of corticosterone on behavior in juveniles of the common lizard, Lacerta vivipara
J Exp Zool
 , 
2004
, vol. 
301A
 (pg. 
401
-
410
)
Berglund
A
Rosenqvist
G
Bernet
P
Ornamentation predicts reproductive success in female pipefish
Behav Ecol Sociobiol
 , 
1997
, vol. 
40
 (pg. 
145
-
150
)
Burley
N
Sexual selection for aesthetic traits in species with biparental care
Am Nat
 , 
1986
, vol. 
127
 (pg. 
415
-
445
)
Civantos
E
Forsman
A
Determinants of survival in juvenile Psammodromus algirus lizards
Oecologica
 , 
2000
, vol. 
124
 (pg. 
64
-
72
)
Clutton-Brock
T
Sexual selection in females
Anim Behav
 , 
2009
, vol. 
77
 (pg. 
3
-
11
)
Cooper
WE
Jr
Greenberg
N
Gans
C
Crews
D
Reptilian coloration and behavior
Biology of the reptilia, Vol. 18. Hormones, brain, and behavior
 , 
1992
Chicago (IL)
University of Chicago Press
(pg. 
298
-
422
)
Cornwallis
CK
Birkhead
TR
Experimental evidence that female ornamentation increases the acquisition of sperm and signals fecundity
Proc R Soc Lond B
 , 
2007
, vol. 
274
 (pg. 
283
-
590
)
Cuadrado
M
Body colors indicate the reproductive status of female common chameleons: experimental evidence for the intersex communication function
Ethology
 , 
2000
, vol. 
106
 (pg. 
79
-
91
)
de Fraipont
M
Clobert
J
John-Alder
H
Meylan
S
Increased pre-natal maternal corticosterone promotes philopatry of offspring in common lizards Lacerta vivipara
J Anim Ecol
 , 
2000
, vol. 
69
 (pg. 
404
-
413
)
Domb
LG
Pagel
M
Sexual swellings advertise female quality in wild baboons
Nature
 , 
2001
, vol. 
410
 (pg. 
204
-
206
)
Doutrelant
C
Grégoire
A
Grnac
N
Gomez
D
Lambrechts
MM
Perret
P
Female coloration indicates female reproductive capacity in blue tits
J Evol Biol
 , 
2008
, vol. 
21
 (pg. 
226
-
233
)
Eilertsen
EM
Bardsen
B-J
Liljedal
S
Rudolfsen
G
Folstad
I
Experimental evidence for paternal effects on offspring growth rate in Arctic charr (Salvelinus alpinus)
Proc R Soc B
 , 
2009
, vol. 
276
 (pg. 
129
-
136
)
Evans
JP
Kelley
JL
Bisazza
A
Finazzo
E
Pilastro
A
Sire attractiveness influences offspring performance in guppies
Proc R Soc Lond B
 , 
2004
, vol. 
271
 (pg. 
2035
-
2042
)
Foerster
K
Delhey
K
Johnsen
A
Tifjeld
JT
Kempenaers
B
Females increase offspring heterozygosity and fitness through extra-pair matings
Nature
 , 
2003
, vol. 
425
 (pg. 
714
-
717
)
Garland
T
Jr
Losos
JB
Wainwright
PC
Reily
SM
Ecological morphology of locomotor performance in squamate reptiles
Ecological morphology: integrative organismal biology
 , 
1994
Chicago (IL)
University of Chicago Press
(pg. 
240
-
302
)
Griggio
M
Matessi
G
Pilastro
A
Male rock sparrow (Petronia petronia) nest defense correlates with female ornament size
Ethology
 , 
2003
, vol. 
109
 (pg. 
659
-
669
)
Griggio
M
Valera
F
Casas
A
Pilastro
A
Males prefer ornamented females: a field experiment of male choice in the rock sparrow
Anim Behav
 , 
2005
, vol. 
69
 (pg. 
1243
-
1250
)
Hagar
SB
The role of nuptial coloration in female Holbrookia maculata: evidence for a dual signaling system
J Herpetol
 , 
2001
, vol. 
35
 (pg. 
624
-
632
)
Hamilton
WD
Zuk
M
Heritable true fitness and bright birds—a role for parasites?
Science
 , 
1982
, vol. 
218
 (pg. 
384
-
387
)
Hanssen
SV
Folstad
I
Erikstad
KE
White plumage reflects individual quality in female eiders
Anim Behav
 , 
2006
, vol. 
41
 (pg. 
337
-
343
)
Hasselquist
D
Bensch
S
von Schantz
T
Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler
Nature
 , 
1996
, vol. 
381
 (pg. 
229
-
232
)
Hoelzer
GA
The good parent process of sexual selection
Anim Behav
 , 
1989
, vol. 
38
 (pg. 
1067
-
1078
)
Huchard
E
Courtiol
A
Benavides
JA
Kanpp
LA
Raymond
M
Cowlishaw
G
Can fertility signals lead to quality signals? Insights from the evolution of primate sexual swellings
Proc R Soc Lond B
 , 
2009
, vol. 
276
 (pg. 
1889
-
1897
)
Huey
RB
Dunham
AE
Repeatability of locomotor performance in natural populations of the lizard Sceloporus merriami
Evolution
 , 
1987
, vol. 
41
 (pg. 
1116
-
1120
)
Huey
RB
Hertz
PE
Effects of body size and slope on sprint speed of a lizard (Stellio (Agama) stellio)
J Exp Biol
 , 
1982
, vol. 
97
 (pg. 
401
-
409
)
Huey
RB
Schneider
W
Erie
GL
Stevenson
RD
A field-portable racetrack and timer for measuring acceleration and speed of small cursorial animals
Experientia
 , 
1981
, vol. 
37
 (pg. 
1356
-
1357
)
Husak
JF
Does speed help you survive? A test with collared lizards of different ages
Funct Ecol
 , 
2006
, vol. 
20
 (pg. 
174
-
179
)
Husak
JF
Fox
SF
Lovern
MB
Van Den Bussche
RA
Faster lizards sire more offspring: sexual selection on whole-animal performance
Evolution
 , 
2006
, vol. 
60
 (pg. 
2122
-
2130
)
Irwin
RE
The evolution of plumage dichromatism in the New World blackbirds: social selection on female brightness?
Am Nat
 , 
1994
, vol. 
144
 (pg. 
890
-
907
)
Johnsen
A
Andersen
V
Sunding
C
Lifjeld
JT
Female bluethroats enhance offspring immunocompetence through extra-pair copulations
Nature
 , 
2000
, vol. 
406
 (pg. 
296
-
299
)
Jones
IJ
Hunter
FM
Mutual sexual selection in a monogamous seabird
Nature
 , 
1993
, vol. 
362
 (pg. 
238
-
239
)
Kokko
H
Brooks
R
Jennions
MD
Morley
J
The evolution of mate choice and mating biases
Proc R Soc Lond B
 , 
2003
, vol. 
270
 (pg. 
653
-
664
)
Kokko
H
Brooks
R
McNamara
JM
Houston
AI
The sexual selection continuum
Proc R Soc Lond B
 , 
2002
, vol. 
269
 (pg. 
1331
-
1340
)
Kraaijeveld
K
Kraaijeveld-Smit
FJL
Komdeur
J
The evolution of mutual ornamentation
Anim Behav
 , 
2007
, vol. 
74
 (pg. 
657
-
677
)
Lande
R
Sexual dimorphism, sexual selection, and adaptation in polygenic characters
Evolution
 , 
1980
, vol. 
34
 (pg. 
292
-
305
)
LeBas
NR
Marshall
NJ
The role of colour in signalling and male choice in the agamid lizard Ctenophorus ornatus
Proc R Soc Lond B
 , 
2000
, vol. 
267
 (pg. 
445
-
452
)
Linville
SU
Breitwisch
R
Schilling
AJ
Plumage brightness as an indicator of parental care in northern cardinals
Anim Behav
 , 
1998
, vol. 
55
 (pg. 
119
-
127
)
Loyau
A
Saint Jalme
M
Mauget
R
Sorci
G
Male sexual attractiveness affects the investment of maternal resources into the eggs in peafowl (Pavo cristatus)
Behav Ecol Sociobiol
 , 
2007
, vol. 
61
 (pg. 
1043
-
1052
)
Madsen
T
Female nonavian reptiles benefit from multiple matings
Mol Ecol
 , 
2008
, vol. 
17
 pg. 
3753
 
Madsen
T
Shine
R
Loman
J
Hakansson
T
Why do female adders copulate so frequently?
Nature
 , 
1992
, vol. 
355
 (pg. 
440
-
441
)
Mänd
R
Tilgar
V
Møller
AP
Negative relationship between plumage colour and breeding output in female great tits, Parus major
Evol Ecol Res
 , 
2005
, vol. 
7
 (pg. 
1013
-
1023
)
Massironi
M
Rasotto
MB
Mazzoldi
C
A reliable indicator of female fecundity: the case of the yellow belly in Knipowitschia panizzae (Teleostei: Gobiidae)
Marine Biol
 , 
2005
, vol. 
147
 (pg. 
71
-
76
)
Meylan
S
Clobert
J
Is corticosterone-mediated phenotype development adaptive? Maternal corticosterone treatment enhances survival in male lizards
Horm Behav
 , 
2005
, vol. 
48
 (pg. 
44
-
52
)
Møller
AP
Male ornament size as a reliable cue to enhanced offspring viability in the barn swallow
Proc Natl Acad Sci USA
 , 
1994
, vol. 
91
 (pg. 
6929
-
6932
)
Møller
AP
Alatalo
RV
Good-genes effects in sexual selection
Proc R Soc Lond B
 , 
1999
, vol. 
266
 (pg. 
85
-
91
)
Mousseau
TA
Fox
CW
Maternal effects as adaptations
 , 
1998
New York
Oxford University Press
Neff
BD
Pitcher
TE
Genetic quality and sexual selection: an integrated framework for good genes and compatible genes
Mol Ecol
 , 
2005
, vol. 
14
 (pg. 
19
-
38
)
Nicoletto
PF
Offspring quality and female choice in the guppy, Poecilia reticulata
Anim Behav
 , 
1994
, vol. 
49
 (pg. 
377
-
387
)
Nowicki
S
Peters
S
Podos
J
Song learning, early nutrition and sexual selection in songbirds
Am Zool
 , 
1998
, vol. 
38
 (pg. 
179
-
190
)
Nowicki
S
Searcy
WA
Peters
S
Brain development, song learning, and mate choice in birds: a review and experimental test of the “nutritional stress hypothesis”
J Comp Physiol
 , 
2002
, vol. 
188
 (pg. 
1003
-
1014
)
Owens
IPF
Thompson
DBA
Sex differences, sex ratios and sex roles
Proc R Soc Lond B
 , 
1994
, vol. 
258
 (pg. 
93
-
99
)
Parker
GA
Bateson
P
Mate quality and mating decisions
Mate choice
 , 
1983
New York
Cambridge University Press
(pg. 
141
-
166
)
Parker
TH
Genetic benefits of mate choice separated from differential maternal investment in red junglefowl (Gallus gallus)
Evolution
 , 
2003
, vol. 
57
 (pg. 
2157
-
2165
)
Petrie
M
Improved growth and survival of offspring of peacock with more elaborate trains
Nature
 , 
1994
, vol. 
371
 (pg. 
598
-
599
)
Potti
J
Merino
S
Decreased levels of blood trypanosome infection correlate with female expression of a male secondary sexual trait: implications for sexual selection
Proc R Soc Lond B
 , 
1996
, vol. 
263
 (pg. 
1199
-
1204
)
R Development Core Team
R: a language and environment for statistical computing
 , 
2008
 
[Internet]. R Foundation for Statistical Computing, Vienna (Austria). [cited 2008 December 13]. Available from: http://www.R-project.org
Reid
JM
Arcese
P
Cassidy
ALEV
Hiebert
SM
Smith
JNM
Stoddard
PK
Marr
AB
Keller
LF
Fitness correlates of song repertoire size in free-living song sparrows (Melospiza melodia)
Am Nat
 , 
2005
, vol. 
165
 (pg. 
299
-
310
)
Reynolds
JD
Gross
MR
Female mate preference enhances offspring growth and reproduction in a fish, Poecilia reticulata
Proc R Soc Lond B
 , 
1992
, vol. 
250
 (pg. 
57
-
62
)
Robson
MA
Miles
DB
Performance and dominance in male tree lizards, Urosaurus ornatus
Funct Ecol
 , 
2000
, vol. 
14
 (pg. 
338
-
344
)
Roulin
A
Proximate basis of the covariation between a melanin-based female ornament and offspring quality
Oecologia
 , 
2004
, vol. 
140
 (pg. 
668
-
675
)
Roulin
A
Jungi
TW
Pfister
H
Dijkstra
C
Female barn owls (Tyto alba) advertise good genes
Proc R Soc Lond B
 , 
2000
, vol. 
267
 (pg. 
937
-
941
)
Rowland
WJ
Baube
CL
Horan
TT
Signaling of sexual receptivity by pigmentation pattern in female sticklebacks
Anim Behav
 , 
1991
, vol. 
42
 (pg. 
243
-
249
)
Salvador
A
Díaz
JA
Veiga
JP
Bloor
P
Brown
RP
Correlates of the reproductive success in male lizards of the alpine species Iberolacerta cyreni
Behav Ecol
 , 
2008
, vol. 
19
 (pg. 
169
-
176
)
Searcy
WA
Song repertoire size and female preference in song sparrows
Behav Ecol Sociobiol
 , 
1984
, vol. 
14
 (pg. 
281
-
286
)
Sheldon
BC
Differential allocation: tests, mechanisms and implications
Trends Ecol Evol
 , 
2000
, vol. 
15
 (pg. 
397
-
402
)
Sinervo
B
The evolution of maternal investment in lizards: an experimental and comparative analysis of egg size and its effects on offspring performance
Evolution
 , 
1990
, vol. 
44
 (pg. 
279
-
294
)
Smiseth
PT
Amundsen
T
Does female plumage coloration signal parental quality? A male removal experiment with the bluethroat (Luscinia s. svecica)
Behav Ecol Sociobiol
 , 
2000
, vol. 
47
 (pg. 
205
-
212
)
Smith
GR
Ballinger
RE
Thermal ecology of Sceloporus virgatus from southeastern Arizona, with comparison to Urosaurus ornatus
J Herpetol
 , 
1994
, vol. 
28
 (pg. 
65
-
69
)
Svensson
PA
Pélabon
C
Blount
JD
Surai
PF
Amundsen
T
Does female nuptial coloration reflect egg carotenoids and clutch quality in the two-spotted goby (Gobiusculus flavescens, Gobiidae)?
Funct Ecol
 , 
2006
, vol. 
20
 (pg. 
689
-
698
)
Tsuji
JS
Huey
RB
van Berkum
FH
Garland
T
Jr
Shaw
RG
Locomotor performance of hatchling fence lizards (Sceloporus occidentalis): quantitative genetics and morphometric correlates
Evol Ecol
 , 
1989
, vol. 
3
 (pg. 
240
-
252
)
Uller
T
Olsson
M
Prenatal exposure to testosterone increases ectoparasite susceptibility in the common lizard (Lacerta vivipara)
Proc R Soc Lond B
 , 
2003
, vol. 
270
 (pg. 
1867
-
1870
)
Uller
T
Olsson
M
Multiple paternity in reptiles: patterns and processes
Mol Ecol
 , 
2008
, vol. 
17
 (pg. 
2566
-
2580
)
van Berkum
FH
Huey
RB
Tsuji
JS
Garland
T
Jr
Repeatability of individual differences in locomotor performance and body size during early ontogeny of the lizard Sceloporus occidentalis (Baird and Girard)
Funct Ecol
 , 
1989
, vol. 
3
 (pg. 
97
-
105
)
Vinegar
MB
Demography of the striped plateau lizard, Sceloporus virgatus
Ecology
 , 
1975
, vol. 
56
 (pg. 
172
-
182
)
Warner
DA
Andrews
RM
Laboratory and field experiments identify sources of variation in phenotypes and survival of hatchling lizards
Biol J Linn Soc
 , 
2002
, vol. 
76
 (pg. 
105
-
124
)
Weiss
SL
Reproductive signals of female lizards: pattern of trait expression and male response
Ethology
 , 
2002
, vol. 
108
 (pg. 
793
-
813
)
Weiss
SL
Response of conspecifics to reproductive color of female striped plateau lizards, Sceloporus virgatus
J Negat Results Ecol Evol Biol
 , 
2005
, vol. 
2
 (pg. 
10
-
19
)
Weiss
SL
Female-specific color is a signal of quality in the striped plateau lizards (Sceloporus virgatus)
Behav Ecol
 , 
2006
, vol. 
17
 (pg. 
726
-
732
)
Weiss
SL
Jennings
DH
Moore
MC
Effect of captivity in semi-natural enclosures on the reproductive endocrinology of female lizards
Gen Comp Endocrinol
 , 
2002
, vol. 
128
 (pg. 
238
-
246
)
West-Eberhard
MJ
Sexual selection, social competition, and speciation
Q Rev Biol
 , 
1983
, vol. 
58
 (pg. 
155
-
183
)
Yasukawa
K
Blank
JL
Patterson
CB
Song repertoires and sexual selection in the red-winged blackbird
Behav Ecol Sociobiol
 , 
1980
, vol. 
7
 (pg. 
233
-
238
)
Zahavi
A
Mate selection—a selection for a handicap
J Theor Biol
 , 
1975
, vol. 
53
 (pg. 
205
-
214
)