Research Article |
Corresponding author: Numa P. Pavón ( numapavon@gmail.com ) Academic editor: Uwe Fritz
© 2023 Abraham Lozano, Jack W. Sites Jr, Aurelio Ramírez-Bautista, Jonathon C. Marshall, Numa P. Pavón, Raciel Cruz-Elizalde.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Lozano A, Sites Jr JW, Ramírez-Bautista A, Marshall JC, Pavón NP, Cruz-Elizalde R (2023) Allometric analysis of sexual dimorphism and morphological variation in two chromosome races of the Sceloporus grammicus complex (Squamata: Phrynosomatidae) from Mexico. Vertebrate Zoology 73: 23-34. https://doi.org/10.3897/vz.73.e94004
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Sexual dimorphism is a widespread feature in the Animal Kingdom. In lizards of the Sceloporus grammicus complex, studies of sexual dimorphism that analyze the allometric trajectories of body traits remain unexplored. Here we investigate sexual dimorphism in key phenotypic traits, including body size (snout-vent length, SVL) as well as head length (HL), head width (HW), and forearm length (FL). We use an allometric approach to detect differences in scale relationships among body parts in the S. grammicus complex in Mexico. We focus on two chromosomal races within this complex, F5 (2n = 34) and FM2 (2n = 46). In the complex, we found that males are larger than females in all morphological variables, and this pattern was confirmed in both races. We determined negative allometric trajectories (SVL vs. HL and HW), isometry (SVL vs. FL) and intersexual differences in the slopes of the SVL vs. HL and HW; the males showed steeper slopes. Thus, the growth of the head is more pronounced in males than females. Additionally, we found between-race differences in these trajectories (SVL vs. FL) and in all morphological variables (F5 lizards are larger than those of the FM2 race), which correlate with their chromosomal divergence. We discuss biological implications of our findings in relation to sexual selection and natural selection.
Lizards, morphology, natural selection, sexual selection, shape, size
Lizards of the genus Sceloporus are one of the most species-rich reptiles in North America and are often utilized as focal species in integrative biological research. The genus contains 110+ morphologically and ecologically distinct species (
Within this lizard genus, the mesquite lizard, Sceloporus grammicus Wiegmann, 1828 (Fig.
All members of the S. grammicus complex are viviparous, and distributed across a diversity of environments, from dry tropical, semi-arid, arid, and humid temperate montane habitats that range from sea level to above 3000 m (
Various ecological and evolutionary hypotheses have emerged to explain sexual dimorphism skewed either towards males or females (
Currently, in the S. grammicus complex there have been no previous studies of intersexual divergence that include analyses of scale relationships among body parts (morphometric variables). In this study, using an allometric approach, we first evaluate sexual dimorphism in the entire S. grammicus complex, and second, we compare the patterns of sexual dimorphism between the F5 and FM2 races that coexist in the state of Hidalgo. Based on theoretical considerations and given that these races are likely in the process of speciation (
The Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT) approved this research (permit # SGPA/DGVS/02726/10). Lizards were euthanized and fixed in 10% formaldehyde solution according to
Specimens are deposited in the following scientific collections: the
Bean Life Science Museum Herpetological Collection at Brigham Young University (
We collected morphological data from 1,722 adult lizards, 54% of which were females. We collected four linear measurements from all specimens (from the left side of the body): snout-vent length (SVL), head length (HL), head width (HW), and forearm length (FL) (
We first analyzed the entire S. grammicus complex, and then we compared the FM2 and F5 races separately; because these are the most chromosomally divergent races (
All data were first transformed with logarithm base 10 (log10) and tested for normality (Kolmogorov-Smirnov test, p > 0.05) and homogeneity of variances (F-test, p > 0.05). Several statistical methods have been proposed and evaluated for the study of morphological data in reptiles (e.g.,
Analysis of the eight races of S. grammicus complex showed that males were significantly larger than females in all raw morphological variables used (Table
Variation of measurements of morphometric variables of the entire Sceloporus grammicus complex. Means ± 1 standard error (SE) are given by sex. Abbreviations: snout-vent length (SVL), head length (HL), head width (HW), and forearm length (FL). Bold values denote statistical significance at the p < 0.05 level.
Sexes | SVL (mm) | HL (mm) | HW (mm) | FL (mm) |
Males (n = 776) | 57.05 ± 0.29 | 13.50 ± 0.07 | 11.31 ± 0.06 | 9.33 ± 0.07 |
Females (n = 946) | 54.63 ± 0.22 | 12.52 ± 0.05 | 10.42 ± 0.04 | 8.71 ± 0.05 |
Mean differences | t = 6.53, p < 0.0001 | t = 10.95, p < 0.0001 | t = 11.75, p < 0.0001 | t = 7.19, p < 0.0001 |
Mean differences, adjusted for covariance (ANCOVA) | --- | F = 76.52, p < 0.0001 | F = 109.90, p < 0.0001 | F = 13.17, p = 0.0002 |
Variation of morphometric variables of FM2 and F5 chromosomal races of the Sceloporus grammicus complex. Means ± 1 standard error (SE) are given by sex. Abbreviations: snout-vent length (SVL), head length (HL), head width (HW), and forearm length (FL). Bold values denote statistical significance at the p < 0.05 level.
Chromosomal races | Sexes | SVL (mm) | HL (mm) | HW (mm) | FL (mm) |
FM2 | Males (n = 328) |
56.42 ± 0.45 | 13.20 ± 0.09 | 10.85 ± 0.09 | 8.73 ± 0.10 |
Females (n = 350) |
53.25 ± 0.39 | 12.13 ± 0.07 | 9.83 ± 0.07 | 7.91 ± 0.08 | |
ANOVA | < 0.0001 | < 0.0001 | < 0.0001 | < 0.0001 | |
ANCOVA | --- | < 0.0001 | < 0.0001 | 0.0006 | |
F5 | Males (n = 67) |
59.68 ± 0.94 | 13.63 ± 0.15 | 12.03 ± 0.18 | 10.44 ± 0.21 |
Females (n = 84) |
58.13 ± 0.85 | 12.94 ± 0.11 | 11.32 ± 0.15 | 9.69 ± 0.18 | |
ANOVA | 0.2247 | 0.0043 | 0.0026 | 0.0076 | |
ANCOVA | --- | < 0.0001 | < 0.0001 | 0.0029 | |
FM2 vs. F5 (ANOVA) |
FM2 vs. F5 | < 0.0001 | < 0.0001 | < 0.0001 | < 0.0001 |
M vs. M | 0.0018 | 0.0292 | < 0.0001 | < 0.0001 | |
F vs. F | < 0.0001 | < 0.0001 | < 0.0001 | < 0.0001 | |
FM2 vs. F5 (ANCOVA) | FM2 vs. F5 | --- | < 0.0001 | < 0.0001 | 0.5032 |
M vs. M | --- | p = 0.9772 | < 0.0001 | < 0.0001 | |
F vs. F | --- | p = 0.0795 | < 0.0001 | < 0.0001 |
In general, the SVL was positively and significantly correlated with the other morphological variables (Table
Parameters of regressions between the independent (SVL) and the dependent (HL, HW, and FL) variables. Data from the entire Sceloporus grammicus complex. Abbreviations: snout-vent length (SVL), head length (HL), head width (HW), forearm length (FL), standard error (SE) of b (slope value). Bold values denote statistical significance at the p < 0.05 level.
Regressions | b | SE | r2 | p |
LogSVL vs. LogHL | 0.71 | 0.019 | 0.44 | < 0.0001 |
LogSVL vs. LogHW | 0.85 | 0.016 | 0.62 | < 0.0001 |
LogSVL vs. LogFL | 1.01 | 0.025 | 0.48 | < 0.0001 |
Analysis of slopes of relationships between SVL and the body variables for the complete data set showed differences in males (ANCOVA: F = 24.69, p < 0.0001) and females (ANCOVA: F = 36.87, p < 0.0001); in both sexes, the relative HL growth was lower with respect to SVL, compared to the other variables (HW, FL; Fig.
Allometric relationships of lizards of the Sceloporus grammicus complex. Slope values (± 1 standard error: SE) of the relationships between the independent (snout-vent length: SVL) and the dependent (head length: HL, head width: HW, and forearm length: FL) variables, separating by sexes (males: brown bars, females: purple bars). Sceloporus grammicus complex (grey circles), FM2 race (orange circles), and F5 race (green circles).
We obtained similar results to the complete data set when comparing allometric relationships between the FM2 and F5 races. For the FM2 race, slopes differed significantly in both males (ANCOVA: F = 26.05, p < 0.0001) and females (ANCOVA: F = 23.38, p < 0.0001). Differences between the sexes were found in the slopes of the SVL vs. HW relationships (ANCOVA: F = 7.70, p = 0.0057), but not in the SVL vs. HL (ANCOVA: F = 2.07, p = 0.1505) and SVL vs. FL (ANCOVA: F = 1.11, p = 0.2915) relationships (Fig.
Summary of results of morphological variables and allometric relationships of the Sceloporus grammicus complex. Mean differences of absolute (raw) and relative (size-corrected) morphological variables, and slope differences in the allometric relationships of the entire Sceloporus grammicus complex, FM2 race, and F5 race. Green boxes represent p > 0.05 (failure to reject the null hypothesis of equal means), while red boxes represent p ≤ 0.05 (reject the null hypothesis of equal means). Abbreviations: snout-vent length (SVL), head length (HL), head width (HW), forearm length (FL), males (M), females (F), isometry (i), positive allometry (+), and negative allometry (—).
Raw (mean differences) | SVL | HL | HW | FL | |
Sceloporus grammicus complex | M vs. F | ||||
FM2 | M vs. F | ||||
F5 | M vs. F | ||||
FM2 vs. F5 | M vs. M | ||||
FM2 vs. F5 | F vs. F | ||||
Size-corrected (mean differences) | |||||
Sceloporus grammicus complex | M vs. F | — | |||
FM2 | M vs. F | — | |||
F5 | M vs. F | — | |||
FM2 vs. F5 | M vs. M | — | |||
FM2 vs. F5 | F vs. F | — | |||
Allometry (slope differences) | |||||
Sceloporus grammicus complex | M vs. F | — | – / – | – / – | i / i |
FM2 | M vs. F | — | – / – | – / – | + / i |
F5 | M vs. F | — | – / – | – / – | + / + |
FM2 vs. F5 | M vs. M | — | – / – | – / – | + / + |
FM2 vs. F5 | F vs. F | — | – / – | – / – | i / + |
Sexual dimorphism is biased towards larger male size in the S. grammicus complex, as well as the intersexual divergence of the scale relationships between body size (SVL) and body parts (morphometric variables: HL, HW). These results were expected; males were generally larger than females in both the absolute (raw) and relative (size-corrected) measures of morphological variables. Also, the chromosomal races differed from each other in their morphological attributes. Further, males show higher values of the slopes of the relationships of the morphological variables than the females.
Most species of Sceloporus are sexually dimorphic (
In the S. grammicus complex, between-sex differences in morphometric variables seem to be maintained largely by sexual selection (
Herein we quantify differences in morphological attributes between two S. grammicus chromosomal races; in the analyses performed both male and female F5 lizards are larger than those of the FM2 race. These results are interesting given that the male size (body and limb lengths) and head shape play a very important role in territorial defense in other lizard species (
Body size (SVL) in other lizard species correlates with aspects of behavior, including escape from predators and intra-specific territorial fights (
These allometric trajectories of body features can be explained by two hypotheses, sexual selection (see above) and/or natural selection. Natural selection could drive ecological divergence if dimorphism in head size or shape due to competition for food or habitat, leads to ecological niche partitioning (
This is the first study to analyze such a large data set for the F5 and FM2 chromosome races of the S. grammicus complex. We used an allometric approach to demonstrate significant differences in body size and head shape between the sexes in these two races. Both races are male-biased in body size and size-corrected morphological traits, and we hypothesize that: (1) sexual selection is acting on morphological characteristics associated with behavior, and/or (2) natural selection drives ecological divergence between the sexes via competition for food resources and/or habitat, leading to ecological niche partition. On the basis of these hypotheses, many future research questions can be posed. For instance, are these race morphological differences the result of plastic response to variable environmental factors, or is there a heritable component to the individuals? Is one or several mechanisms operating on sexual dimorphism? In the event that there is more than one, which mechanism is promoting body size and shape dimorphism more strongly, sexual selection, ecological difference between the sexes, or habitat influence? Is there a relationship between morphology and reproductive performance in one or both sexes? If so, what would be the magnitude and direction of this relationship? Such questions could be addressed using a combination of field and laboratory experiments. Therefore, quantification of locomotor performance capacity, behavior, and reproductive characteristics must be performed to shed light on the morphological adaptations of individuals in this widely distributed complex in Mexico.
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
The data that support the findings of this study are available upon reasonable request.
We thank Edmundo Pérez Ramos and Adrián Nieto Montes de Oca for access to specimens from the Collection of the Museo de Zoología, Facultad de Ciencias (MZFC), and Víctor Hugo Reynoso for access to specimens in the Colección Nacional de Anfibios y Reptiles, Instituto de Biología (CNAR-IBH), both from the Universidad Nacional Autónoma de México. We also thank Lee Grismer, Marco Zuffi, and two anonymous reviewers for their helpful comments. This work was supported by the Programa para el Desarrollo Profesional Docente (PRODEP, previously PROMEP) at Universidad Autónoma del Estado de Hidalgo, throughout the project SEP-PROMEP 1103.5/03/1130, and the projects DIP-ICBI-AAB-020, CONACYT-43761, and CONACYT-S52552-Q. The Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT) approved this research (permit # SGPA/ DGVS/02726/10).
File S1
Data type: .docx
Explanation note: Museum voucher numbers of the Sceloporus grammicus complex.