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. 2025 Jul 14;72(1):138–146. doi: 10.1093/cz/zoaf033

Elevational patterns of sexual size dimorphism in a Mediterranean lizard

Mar Comas 1,2,✉,b, Senda Reguera 3, Francisco J Zamora-Camacho 4, Gregorio Moreno-Rueda 5
Editor: Zu-Shi Huang
PMCID: PMC13045821  PMID: 41940280

Abstract

Sexual size dimorphism (SSD), typically the result of different optimal body sizes for males and females, shows an enormous inter- and intraspecific variation. Lizards have become a model in the study of SSD, as they show either monomorphism, male- or female-biased SSD. Variations in the strength of intrasexual selection (assumed to favor larger body size in males) and fecundity selection (assumed to favor larger body size in females) are usually considered the main reasons for variation in SSD. Here, we take advantage of a 2,200 m elevational gradient for studying the elevational variation in SSD in the Mediterranean lizard Psammodromus algirus. Previous studies on this species suggest that the strength of sexual selection decreases with ascending elevation, while the strength of fecundity selection on females increases with ascending altitude. Accordingly, we predicted that SSD bias to males should increase at low elevations, while female-biased SSD should increase at high altitudes. We found that both males and females were larger with ascending elevation, but the magnitude of variation in body size with altitude differed between sexes. Females were slightly larger than males (1.1%), although SSD bias toward females increased with elevation. SSD was male-biased only in one locality, at the lowest elevation. Nevertheless, elevational differences in SSD resulted from a concomitant sexual variation in age structure, as females were older than males in every locality except at the lowest elevation, where males were older than females. Since this species shows post-maturational growth, sexual differences in age structure could explain the elevational pattern in SSD.

Keywords: age structure, fecundity selection, sexual selection

Graphical Abstract

Graphical Abstract.

For image description, please refer to the figure legend and surrounding text.

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Many animal species with separate sexes show sexual size dimorphism (SSD), whereby individuals of one sex are generally larger or have body parts more developed than individuals of the other sex (Fairbairn et al. 2007). Sexual size dimorphism has attracted considerable attention since Darwin (1874), mainly because SSD enormously varies among species (Fairbairn 2007). For example, male songbirds are usually larger than females, but female raptors are typically larger than males (Székely et al. 2007). Moreover, sexual size dimorphism shows considerable geographical variation within the same species (e.g., Roitberg 2007; Corl et al. 2010; Littleford-Colquhoun et al. 2019; Roitberg et al. 2020; Muraro et al. 2022). Several selective forces have been proposed to explain general SSD, whereby the resulting SSD will depend on the relative importance of these forces in each sex (Cox and Calsbeek 2009). In reptiles, the main selective forces driving SSD are sexual selection and fecundity selection (Cox et al. 2003, 2007; Pincheira-Donoso and Hunt 2017). The competition with the conspecifics of the same sex for access to territories or partners may prompt larger body sizes in one sex, which more often occurs in males, so favoring male-biased SSD (Andersson 1994; Cox et al. 2003, 2007; Cox and Kahrl 2015; Winkler et al. 2024). On the other hand, females with larger bodies can be more fecund, being able to lay more eggs or have larger offspring (fecundity selection), which may impel an SSD biased in favor of females (Braña 1996; Cox et al. 2003; Roitberg et al. 2013, 2015; Jiménez-Arcos et al. 2017; Liang et al. 2021; but see Olsson et al. 2002; Pincheira-Donoso and Tregenza 2011). Still, SSD results from the interplay of different selective pressures acting on the two sexes. Therefore, selection for larger body size in females may not result in female-biased SSD if (1) other selective pressures for reduced body size are operating, (2) selection for larger body size in males equals or surpasses selection for larger body size in females, (3) genetic correlations between the two sexes provoke the evolution of body size in one sex to be mirrored in the other sex, or (4) environmental constraints preclude organisms from reaching the optimal body size. Consequently, the evolution of SSD shows an extraordinary complexity (reviewed in Cox and Calsbeek 2009).

Certain parts of the body may also display sexual size dimorphism when subjected to sexual selection. For example, intrasexual selection can favor male lizards with larger heads than females (reviewed in Shine 1989; Scharf and Meiri 2013), to harbor greater musculature, being able to deliver more powerful bites and thus win contests (Molina-Borja et al. 1998; Gvozdík and van Damme 2003; Huyghe et al. 2005; Kaliontzopoulou et al. 2008, 2012). Furthermore, male lizards typically have longer limbs than females. Indeed, sexual selection may favor longer limbs because faster males are dominant, maintain larger territories, and sire more offspring (Husak et al. 2006). Males also tend to have longer tails than females (Barbadillo and Bauwens 1997).

Therefore, complex ecological and evolutionary processes trigger diverse SSD body size and shape patterns. Hence, more studies are necessary to obtain a complete picture of the causes of SSD. In this regard, when SSD shows geographic variation, it is thought to result from concomitant geographic variation in selective pressures. Geographic patterns offer a unique opportunity to study how different selective pressures affect SSD. In this respect, elevational patterns provide a natural experiment of great scientific value. The strength of sexual selection can vary along the elevational gradient, resulting in variation in SSD (Badyaev 1997). For example, in the lizard Psammodromus algirus, the number of femoral pores (involved in mate choice; Martín et al. 2007) decreases with elevation (Iraeta et al. 2011; Martín et al. 2017), suggesting a relaxation of sexual selection with increased altitude. Female investment in reproduction may also vary with elevation, as it varies with climate (Mesquita et al. 2016), and P. algirus female reproductive investment tends to increase with elevation (Iraeta et al. 2013; Comas et al. 2020). Indeed, lizard SSD is typically female-biased in cold sites (Tarr et al. 2018).

In this study, we investigate elevational patterns of SSD in P. algirus, focusing on overall body size as well as head, limbs, and tail length along a 2,200 m elevational gradient in Sierra Nevada (southern Spain). Previous studies suggest that female reproductive investment increases with elevation (Iraeta et al. 2013; Comas et al. 2020), while sexual selection pressure on males is stronger at low altitudes (Iraeta et al. 2011; Martín et al. 2017; also see Moreno-Rueda et al. 2021). Based on these findings, we propose two alternative hypotheses to explain SSD variation across elevation: (1) Functional hypotheses: Sexual selection on males and fecundity selection on females act in opposing directions along the elevational gradient. Consequently, we expect male-biased or less female-biased SSD at low elevations, and female-biased or less male-biased SSD at higher elevations. Since traits such as head size, limb length, and tail length are typically larger in males and are likely targets of sexual selection, we predict that sexual size dimorphism in these traits will be more pronounced at lower elevations. (2) Nonfunctional hypothesis: Given that P. algirus exhibits indeterminate growth (Moreno-Rueda et al. 2021), SSD could arise from sexual differences in age structure rather than direct selection (Stamps 1993; Watkins 1996). Prior work has shown that age structure varies with elevation: females tend to live longer than males at most elevations, except at the lowest, where males outlive females (Comas et al. 2020). Thus, we hypothesize that these age differences may generate patterns of SSD independent of functional selection. Specifically, we predict male-biased SSD at the lowest elevation, but female-biased SSD at the remaining elevations. It should be noted that, while both hypotheses predict male-biased SSD at low altitudes, only the functional hypothesis anticipates elevational variation in SSD of sexually selected traits (head, limbs, tail).

Materials and methods

Sampling

The study was conducted in the Sierra Nevada mountain system (SE Spain), where the lizard P. algirus lives from 200 to 2800 m asl (above sea level). We sampled six localities sited at 300, 700, 1200, 1700, 2200, and 2500 m asl. We captured 549 adult lizards by hand during their activity season for 4 years (2010–2013). Lizards were sexed according to their sexual dimorphism in colouration (Moreno-Rueda et al. 2021), number and size of femoral glands, and head size (Iraeta et al. 2011). We took a toe for every lizard, the wound being disinfected with chlorhexidine. The toe-clipping of only a toe has little impact on a lizard’s welfare (Perry et al. 2011) and allowed us to mark lizards and avoid recaptures. In a subsample, the toe was used for skeletochronology (see below). We measured lizards’ snout-vent length (SVL) as an estimation of structural body size, as well as fore limb length (FLL), hind limb length (HLL), and tail length (TL) with a metal ruler to the nearest 1 mm. For tail length, only individuals with a complete original tail were considered; those with regenerated tails were excluded. Head size (HS) was calculated as the cubic root of the product of head width, head length, and head height (i.e., the geometric mean, following Mosimann 1970). The head size variables were measured with a digital caliper (accuracy: 0.01 mm). Some data were lost due to lizards exhibiting incomplete tails, head height not being measured in 2010 and 2011, human errors, and lizard escape behavior. This resulted in different sample sizes for each variable, so sample sizes for each variable per sex and elevation are given in Supplementary Table S1. The complete dataset is available in Supplementary Table S2. We estimated age in a subsample of 116 lizards using skeletochronology (Comas et al. 2016), a technique that accurately estimates lizard age (Zhao et al. 2019). For every elevation, 6–12 adult lizards of each sex were randomly selected for age estimation (more details in Comas et al. 2016, 2020). We also estimated lizard population density and sex ratio because the strength of sexual selection may increase with population density or male-biased sex ratio (Stamps et al. 1997). Population density was estimated from regular transect surveys conducted in 2010 (Zamora-Camacho et al. 2013), counting only adults observed during transects. Density was expressed as the mean number of individuals per transect for each elevation. The sex ratio was calculated as the ratio of males to females captured during sampling at each locality. Finally, average clutch size per elevation was estimated from gravid females brought to the laboratory and maintained until egg-laying (more details in Zamora-Camacho et al. 2014).

Statistical analysis

To investigate how body size varies with elevation and sex, we first fitted a linear model using snout-vent length (SVL, log-transformed; n = 549 lizards) as the dependent variable, with elevation, sex, and their interaction as predictors. This model tests for differences in body size patterns across sexes and elevations. Post hoc comparisons between elevations were performed using the Unequal N HSD test to identify specific elevational differences.

To examine whether post-maturational growth differs between sexes, we fitted a second linear model with SVL as the response variable and sex, age, and their interaction as predictors. This analysis was restricted to individuals with known age (n = 116). In addition, based on the observed relationship between SSD and age differences along the elevational gradient, we performed a generalized linear model (GLM) with a multinomial error distribution to assess how age varies with elevation, sex, and their interaction. To assess multicollinearity in these models, we calculated variance inflation factors (VIF), which were all below 5, indicating acceptable collinearity levels.

A sexual size dimorphism (SSD) index was quantified at each elevation using the formula [(SVL of larger sex/SVL of smaller sex)—1], following Lovich and Gibbons (1992) and Fairbairn (2007). Negative values are arbitrarily assigned to male-biased SSD, while positive values are assigned to female-biased SSD. We then explored potential drivers of SSD variation across elevations by calculating Spearman rank correlations between SSD per locality and (1) elevation, (2) sexual differences in age (female mean age minus male mean age), (3) female mean SVL, (4) average clutch size, (5) male mean SVL, (6) sex ratio, and (7) lizard density. These variables represent potential influences of elevation (1), age structure (2), fecundity selection (3, 4), and sexual selection pressures (5–7). Given the limited sample size (6 populations), we did not apply corrections for type II error; therefore, these results should be interpreted with caution.

To specifically test the role of sexual selection on SSD variation, we analyzed morphological traits presumably under strong sexual selection (head size, tail length, forelimb length, and hindlimb length) in relation to elevation and sex. Since tail and limb lengths scale allometrically with overall body size, we first obtained residuals from Major Axis regressions of each trait on log-transformed SVL (Packard 2013), which serve as size-corrected measures. For head size, which is part of SVL, we controlled for occiput-vent length (OVL = SVL minus head length), following Braña (1996). We then applied a multivariate analysis of variance (MANOVA) with sex, elevation, and their interaction as predictors to evaluate interpopulation variation in these size-corrected morphological traits. Finally, to assess whether allometric relationships between body size and morphological traits vary with elevation and sex, we conducted Major Axis regressions testing three-way interactions between sex, elevation, and body size for each trait. Significant interactions involving sex and body size indicate sexual differences in growth slopes; interactions with elevation reveal elevational changes in allometry; and a significant three-way interaction (sex × elevation × body size) would suggest that sexual selection intensity varies with elevation. Conversely, a nonsignificant three-way interaction implies consistent sexual selection across elevations (Voje 2016).

All statistical analyses were carried out with STATISTICA 8.0 software (StatSoft 2007).

Results

Elevational variation in body size according to sex

A linear model indicated that body size (SVL) increased with elevation in a non-linear way (F5, 537 = 62.31, P < 0.001; Fig. 1a): lizards at 300, 700, and 1,200 m did not differ in body size (post hoc tests, P > 0.90), but they were smaller than lizards above 1,200 m (P < 0.001). From 1,700 to 2,500, a linear increase in body size emerged (Fig. 1a). In general, females were significantly larger than males (females, mean SVL ± SD, 66.0 ± 8.1 mm; males: 65.3 ± 7.3 mm; SSD = 0.01; F1, 537 = 4.25, P = 0.04). However, the interaction between elevation and sex was significant (F5, 537 = 2.91, P = 0.01) and, in the lowest locality, males were larger than females (Fig. 1a; more details in Supplementary Table S3). This finding indicates that SSD varied with elevation.

Figure 1.

Four graphics. Graphic A shows the mean values (with 95% Confidence Intervals) of snout-vent length for each population (six populations, elevation from 300 to 2500 m asl). Females are generally larger than males, except for the lowest elevation. In general, body size is similar from 300 to 1200 m, and then shows a linear increase to 2500 m. Graphic B shows the sexual size dimorphism index, estimated as (snout-vent length of larger sex/snout-vent length of smaller sex)-1 (with positive values when females are the larger sex, and negative when males are the larger sex) according to elevation in the lizard Psammodromus algirus. Only at 300 m is the sexual size dimorphism index negative (that is, males were larger than females). Graphic C shows sexual size dimorphism for every locality according to average female snout-vent length, indicating a general increase in sexual size dimorphism with female size. And the graphic D shows the sexual differences in age, indicating that females were, on average, older than males except for the lowest elevation, where males were older than females.

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(A) Mean values and 95% Confidence Interval (whiskers) of snout-vent length (SVL) for each population (elevation from 300 to 2,500 m asl), for males (blue) and females (red) of the lizard Psammodromus algirus. (B) Sexual size dimorphism (SSD) index, estimated as (SVL of larger sex/SVL of smaller sex)-1 (with positive values when females are the larger sex, and negative when males are the larger sex) according to elevation in the lizard P. algirus. (C) Sexual size dimorphism (SSD) index for every locality (dots) according to average female SVL (mm). The elevation of the locality is indicated next to the dot. (D) Sexual differences in age (female—male age, in years) according to the elevation. Positive values for the localities where females were, on average, older than males, and negative values for the only one where males were older than females.

Elevational variation in sexual size dimorphism according to age

A linear model showed that P. algirus has post-maturation growth (F4, 106 = 14.02, P < 0.001; Fig. 2), but this growth was similar in the two sexes (interaction sex × age, F4, 106 = 0.81, P = 0.52; Fig. 2). Moreover, males and females had similar SVL when maturation occurred (with 1 year; t29 = 0.67, P = 0.51; Supplementary Table S3), suggesting similar pre-maturation growth, too. Consequently, SSD was not explained by sexual differences in growth rate. The multinomial Generalized Linear Model with age as the response variable showed a significant interaction between elevation and sex, indicating elevational sexual differences in age structure (interaction sex × elevation, χ28 = 22.11, P = 0.005; sex, χ24 = 2.14, P = 0.71; elevation, χ216 = 47.31, P < 0.001). Indeed, only in the locality at 300 m were males, on average, older than females (Fig. 1d).

Figure 2.

A graphic showing the mean of snout-vent length of females and males Psammodromus algirus lizards according to age. The graph shows that older lizards are larger.

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Mean (with 95% Confidence Intervals, whiskers) of the snout-vent length (SVL) of female (solid red) and male (hatched blue) Psammodromus algirus lizards in relation to age (estimated according to lines of arrested growth, LAGs).

Interpopulation covariates with SSD index

SSD index positively correlated with elevation (rs = 0.89, P = 0.02, n = 6 localities; Fig. 1b). That is, females became increasingly larger than males as altitude increased (Fig. 1b). The elevational pattern in the SSD index was explained by elevational differences in age between males and females (rs = 0.83, P = 0.042; Fig. 1d). We also found some support for the fecundity selection hypothesis, as SSD index per locality significantly increased with mean female body size (rs = 0.89, P = 0.02; Fig. 1c). Moreover, the SSD index tended to increase with clutch size (rs = 0.77, P = 0.07), although this was apparently caused by females being larger in populations with more female-biased dimorphism (correlation between average clutch size and average female SVL per elevation: rs = 0.94, P = 0.005). However, no support for the sexual selection hypothesis was found: SSD index did not significantly vary with mean male body size (rs = 0.54, P = 0.27), population density (rs = 0.03, P = 0.96), and sex ratio (rs = -0.14, P = 0.79).

Elevational variation in body parts according to sex

The morphological variables measured (head size, limb lengths, and tail length, corrected by body size) varied significantly with elevation (MANOVA, Wilks = 0.60, F20, 455.33 = 3.77, P < 0.001) and sex (Wilks = 0.47, F4, 137.00 = 38.62, P < 0.001), but the interaction sex × elevation was not significant (Wilks = 0.94, F20, 455.33 = 0.45, P = 0.98), indicating that the magnitude of the body size differences between males and females was similar between the analyzed populations. Males showed larger heads and longer tails and limbs than females (Table 1; Fig. 3a–d). These morphological traits showed different patterns with elevation (Table 1; Fig. 3a–d). Nevertheless, the magnitude of differences in the size of body parts between males and females was similar along the elevation gradient, as indicated by the non-significant interaction sex × elevation (Table 1). The relationship between the size of body parts and body size was hypoallometric, except for tail length in males (Table 2). In all traits, the slope of growth with size was steeper in males than in females, as indicated by a significant sex × body size interaction (Table 2). However, the interaction between elevation and body size was significant only for forelimb length (Table 2), suggesting that allometry did not consistently vary with elevation. Crucially, the three-way interaction sex × elevation × body size was not significant for any trait (Table 2). This indicates that sexual differences in allometric relationships were similar across elevations.

Table 1.

Summary of the regression linear model (F values) on head size, tail length and the two fore and hind limbs, statistically controlled for OVL (in the case of head size) or SVL (for the remaining variables)

Lizard traits Elevation Sex Elevation*Sex
Head size F 5, 274 = 0.98, P = 0.43 F 1, 274  = 172.30, P < 0.001 F 5, 274 = 0.28, P = 0.92
Tail length F 5, 239  = 24.64, P < 0.001 F 1, 239  = 85.90, P < 0.001 F 5, 239 = 0.93, P = 0.46
Forelimb length F5, 532 = 2.74, P = 0.019 F 1, 532  = 115.25, P < 0.001 F 5, 532 = 0.51, P = 0.77
Hind limb length F 5, 532  = 7.71, P < 0.001 F 1, 532  = 221.97, P < 0.001 F 5, 532 = 0.52, P = 0.76
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*In bold, those significant results after applying the Bonferroni correction.

Figure 3.

Four graphics showing the mean values (with 95% Confidence Intervals) of head size, tail length, forelimb length, and hindlimb length (in all cases, controlled for snout-vent length) for males and females Psammodromus algirus lizards in each elevation. In all cases, males show traits larger than females. For tail length, a decrease in the two sexes with elevation is clear.

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Mean values and 95% confidence intervals (whiskers) for each population (elevation from 300 to 2,500 m asl), for males (blue) and females (red) of the lizard Psammodromus algirus for (A) head size (residuals, controlled for OVL), (B) tail length (residuals, controlled for SVL), (C) forelimb length (residuals, controlled for SVL), and (D) hindlimb length (residuals, controlled for SVL).

Table 2.

Allometric relationships between body parts and body size (SVL for tail, fore limb, and hindlimb length, OVL for head size). It indicates the slope (allometric relationship) estimated with Major Axis Regressions, as well as the statistics of a test of homogeneity of slopes for the interactions sex*body size, elevation*body size, and the three-way interaction sex*elevation*body size. The numerator degrees of freedom are 1 for the interaction sex*body size, and 5 for the interaction elevation*body size and the three-way interaction. The degrees of freedom of the error term are indicated in the column d.f.

Females Males sex*body size Elevation*body size Three-way interaction
slope N slope N d.f. F P F P F P
Tail length 0.63 125 1.02 126 227 11.34 <0.001 0.67 0.65 1.72 0.13
Forelimb length 0.57 275 0.75 269 520 15.53 <0.001 2.97 0.012 0.92 0.47
Hind limb length 0.42 276 0.89 269 521 30.49 <0.001 0.76 0.58 1.34 0.24
Head size 0.33 143 0.41 143 262 5.15 0.024 0.45 0.82 1.11 0.35
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Discussion

This work shows that, in our study area, P. algirus exhibits a slight SSD biased to females, which were, on average, 1.1% larger than males. However, SSD varied with elevation, ranging from females being 4.9% larger than males at 2200 m, an absence of SSD at 1200 m, to the population located at 300 m, where males were 3.8% larger than females. Although these differences are statistically relevant, the magnitude of variation is relatively small. For context, Roitberg (2007) reported intraspecific SSD variation in Lacerta agilis across Europe ranging from 9% male-biased to 13% female-biased. In contrast, the range we observed (between −0.04 and 0.05 in SSD index) is comparable to previous findings for P. algirus in Spain and Algeria, which vary between −0.06 and 0.02 (Iraeta et al. 2011; Salvador 2015 [and references therein]; Khelfaoui et al. 2023). This suggests that the species generally exhibit weak and variable SSD, with both male- and female-biased patterns depending on local conditions.

The emergence of this elevational pattern in SSD prompted us to consider two non-mutually exclusive hypotheses. The functional hypothesis posits that SSD variation results from opposing selective pressures along the elevational gradient: sexual selection favoring larger males and fecundity selection favoring larger females, potentially shifting in strength with elevation. On the other hand, the nonfunctional hypothesis proposes that SSD patterns arise from elevation-dependent differences in age structure between sexes, without requiring divergent selection. Our data support the nonfunctional explanation: the observed elevational shifts in SSD align closely with variations in age structure. The functional hypothesis received some support, restricted to the role of fecundity selection (see below).

Our study suggests that differences in SSD along the altitudinal gradient might be due to sex differences in age structure. In our study species, adults continue to grow after sexual maturity, and females were older than males at all altitudinal levels where they were larger than males. The exception was the population at 300 m, the only one in which the males were older than the females (~1 yr), and, apparently, for that reason, they were also larger than the females. Similar results were found by Watkins (1996) in the lizard Microlophus occipitalis, where males live longer than females, which contributes to a male-biased SSD. We can discard that elevational variation in SSD is due to sexual variation in post-maturation growth, as this seemed to be similar in the two sexes. Hence, elevational differences in SSD might be due to sexual differences in viability selection (Cox and Calsbeek 2009). Psammodromus algirus is subject to directional selection for larger sizes for both females (larger females have greater clutch size; Díaz et al. 2005, 2007, 2012) and males (larger males have greater mating success; Díaz 1993; Salvador and Veiga 2001). However, larger males also have lower survival, presumably due to being more active, spending more time patrolling their territories, which exposes them to predators (Díaz 1993). Therefore, males must have an optimal body size between the optimal for mating and the optimal for survival. One possible explanation for the sexual variation in age structure with altitude is that predators acting on males (more mobile and exposed) and females differ, and the relative frequency of such predators varies with elevation. Some bird predators, such as kestrels (Falco tinnunculus) and corvids, are present along the elevational gradient, while saurophagous snakes like Coronella sp. and Vipera latastei (which often prey on lizards) are infrequent below 1,000 m (personal observations). Other potential predators, such as shrikes (Lanius sp.), foxes (Vulpes vulpes) and wild boars (Sus scrofa), are more abundant at medium and low elevations (personal observations). If the unequal distribution of these predators affected the elevational sexual differences in survival, it deserves further study.

Environmental conditions drastically vary with elevation, which could affect growth and final body size. Time available for growth typically diminishes with elevation (Adolph and Porter 1993). Moreover, food availability, which may vary with elevation, favors the growth of the largest sex (males in those studies) more than that of the smallest sex, suggesting that body size in the smallest sex has been canalized, while the largest sex shows greater plasticity (Cox and Calsbeek 2010; Bonneaud et al. 2016; Muraro et al. 2022). Further, environmental moisture favors female growth in the lizard Zootoca vivipara, increasing female-biased SSD (Le Galliard et al. 2006). In Sierra Nevada, the time available for growth decreases with elevation (Zamora-Camacho et al. 2013), but high elevations harbor more food availability for lizards (Moreno-Rueda et al. 2018) and are the moister. Still, sexual differences in growth are not plausible given that our findings suggest that post-maturation growth is similar in the two sexes, and the two sexes maturate with similar age and size, which discards sexual differences in pre-maturational growth.

Regarding the functional hypotheses, the investment in reproduction in P. algirus is greater in cold sites (Díaz et al. 2012; Iraeta et al. 2013; Comas et al. 2020). Given that fecundity selection favors increased female body size (Braña 1996; Cox et al. 2003, 2007; Pincheira-Donoso and Hunt 2017) and this species invests more in clutch size in cold sites, we predicted larger females at higher altitudes, which might result (everything being equal) in female-biased SSD. Our findings supported this prediction: SSD increased with elevation and female body size and was (marginally non-significantly) positively correlated with clutch size. However, although average clutch size per elevation tended to be correlated with female-biased SSD, this seemed to be a consequence of females being larger at high elevations, simultaneously resulting in increased female-biased SSD and clutch size. Therefore, the role of fecundity selection in shaping the elevational pattern of SSD remains unclear.

The second part of the functional hypotheses is that males were expected to be relatively larger at lower elevations, where sexual selection pressure in this species seems to be stronger (Iraeta et al. 2011; Martín et al. 2017; Moreno-Rueda et al. 2021). The reported pattern would seem to support this hypothesis; in fact, only the lowest population showed male-biased SSD. However, although males had larger heads, longer limbs, and tails than females (relative to body size), sexual dimorphism for these traits did not vary with elevation. Moreover, the allometry of these traits with body size was similar along the elevational gradient, suggesting that sexual selection was similar along the altitude (Voje 2016; also see Bonduriansky 2007). Further, there was no relationship between SSD and male body size, population density, and sex ratio. Therefore, the results do not support that sexual selection is behind the reported elevational pattern in SSD.

In conclusion, based on previous studies, we predicted that SSD would vary along the elevational gradient studied, being female-biased at high elevations and male-biased at low altitudes. The results confirmed this pattern, and additional analyses provided some support for the relevance of fecundity selection, but no support for a role of sexual selection, on the elevational pattern in SSD. However, a detailed analysis of the age structure suggests that the altitudinal variation in the age structure of males and females influenced the resulting elevational pattern in SSD. Where females lived more than males, female-biased SSD emerged, while the only population where males lived more than females was the only population with male-biased SSD. This study highlights the importance of knowing the age structure when studying SSD in species with indeterminate growth, like the one studied here. Otherwise, misleading conclusions could be reached about the patterns and causes of SSD.

Supplementary Material

zoaf033_suppl_Supplementary_Table_S1
zoaf033_suppl_supplementary_table_s1.docx (15.4KB, docx)
zoaf033_suppl_Supplementary_Table_S2
zoaf033_suppl_supplementary_table_s2.xls (88.5KB, xls)
zoaf033_suppl_Supplementary_Table_S3
zoaf033_suppl_supplementary_table_s3.docx (16.7KB, docx)

Acknowledgments

We thank the personnel from the Espacio Natural de Sierra Nevada for their constant support. We are also grateful to Concepción Hernández, from the Centre of Scientific Instrumentation at the University of Granada, for her help with the freezing microtome. We are also in debt to Humbert Salvadó (University of Barcelona) for allowing us to use the microscope. Comments by anonymous referees greatly improved the manuscript.

Contributor Information

Mar Comas, Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA; Departamento de Zoología, Universidad de Granada, 18071, Granada, Spain.

Senda Reguera, IES Don Pelayo, Joaquín Sorolla, s/n, E-28810 Los Hueros, Madrid, Spain.

Francisco J Zamora-Camacho, Departamento de Biología de Organismos y Sistemas, Área de Zoología, Universidad de Oviedo, C/Valentín Andrés Álvarez s/n, 33071 Oviedo, Spain.

Gregorio Moreno-Rueda, Departamento de Zoología, Universidad de Granada, 18071, Granada, Spain.

Authors’ contributions

GM-R: funding and supervision. SR and FJZ-C: data collection. MC: skeletochronology analysis and statistical analyses. MC: writing, with inputs from the other authors.

Funding

This study was supported by the Ministerio de Ciencia e Innovación (project CGL2009-13185).

Ethics statement

The research was conducted in accordance with both the Junta de Andalucía and National Park of Sierra Nevada research permits (references GMN/GyB/JMIF and ENSN/JSG/JEGT/MCF).

Data availability

Data is provided as a supplementary file in Table S2.

Supplementary material

Supplementary material can be found at https://academic.oup.com/cz.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

zoaf033_suppl_Supplementary_Table_S1
zoaf033_suppl_supplementary_table_s1.docx (15.4KB, docx)
zoaf033_suppl_Supplementary_Table_S2
zoaf033_suppl_supplementary_table_s2.xls (88.5KB, xls)
zoaf033_suppl_Supplementary_Table_S3
zoaf033_suppl_supplementary_table_s3.docx (16.7KB, docx)

Data Availability Statement

Data is provided as a supplementary file in Table S2.

Articles from Current Zoology are provided here courtesy of Oxford University Press

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