Eye orbit geometric shape in Liolaemus as an indicator of polygyny or monogamy

Geometría de la órbita ocular en Liolaemus como indicador de poliginia o monogamia

Marcela. A. Vidal Maldonado*

Laboratorio de Genómica y Biodiversidad, Departamento de Ciencias Básicas, Facultad de Ciencias, Universidad del Bío-Bío. Casilla 447, Chillán, Chile. *E-mail: mavidal@ubiobio.cl, marcela.vidal@gmail.com

ABSTRACT

Most animal groups have sexual dimorphism in morphological characters, especially body size. In many cases, sexual dimorphism may be a consequence of a hierarchical social organization within populations. However, polygyny or monogamy may evolve independently of sexual dimorphism. Two Liolaemus species are known to be good model species to study the relationship between sexual dimorphism and sexual social system: Liolaemus tenuis (polygyny) and Liolaemus copiapoensis (monogamy). In this study, I evaluate the morphological variation in the geometric shape of the orbit between sexes in the two species, comparing their social condition (polygyny, monogamy) and applying a geometric morphometrical methodology. The results show morphological differentiation in orbit shape, suggesting potentially adaptative characters associated with social condition. There are variety of possible causes which could explain these differences (e.g., multiple origins of the social system in Liolaemus), which could provide new perspectives; however, the generalized lack of knowledge of social systems in Liolaemus species imposes barriers to new studies on the subject.

Keywords: Geometric morphometrics, Liolaemus copiapoensis, Liolaemus tenuis, social behavior.

La mayoría de los grupos de animales muestran dimorfismo sexual en los caracteres morfológicos, en particular el tamaño del cuerpo. En muchos casos, el dimorfismo sexual puede ser una consecuencia de una organización social jerarquizada dentro de las poblaciones. Sin embargo, la poliginia o la monogamia pueden evolucionar por líneas independientes del dimorfismo sexual. Existen dos especies de Liolaemus conocidas por ser buenas especies de estudio, puesto que permiten relacionar el dimorfismo sexual y el sistema social: Liolaemus tenuis (poligínica) y Liolaemus copiapoensis (monógama). En este estudio se evalúa la variación morfológica de la forma de las órbitas entre los sexos de ambas especies, comparando su condición social (poliginia, monogamia) y aplicando la metodología de morfometría geométrica. Los resultados muestran diferencias morfológicas en la forma de la órbita, sugiriendo que corresponden a un carácter potencialmente adaptativo asociado a la condición social. En este sentido, hay una variedad de posibles causas que podrían explicar estas diferencias (e.g., orígenes múltiples del sistema social en Liolaemus), las cuales podría llevar a nuevas perspectivas de estudio. Sin embargo, la falta de conocimiento acerca de los sistemas sociales en las especies de Liolaemus impone barreras a nuevos estudios.

Palabras claves: Morfometría geométrica, Liolaemus copiapoensis, Liolaemus tenuis, conducta social

INTRODUCTION

In most animal groups, sexual differences in morphological characters (sexual dimorphism) are a common phenomenon, particularly in body size. The direction of the difference, i.e., whether males or females are larger, differs between animal groups; in vertebrates males are typically the larger sex (Schoener et al. 1982; Shine 1986; Fairbairn 1990, 1997;

Andersson 1994). Several proximate mechanisms have been proposed to explain sexual dimorphism, such as differential mortality of sexes (Stamps 1993) and different growth rates of sexes (Watkins 1996). However, natural or sexual selection remains the ultimate mechanism explaining sexual dimorphism (Shine 1986; Andersson 1994; Watkins 1998). Sexual dimorphism is one consequence of a hierarchical social organization within populations (Verrastro 2004).

However, polygyny or monogamy may be independent of sexual dimorphism (Desjardins et al. 2008). Thus, a species may exhibit sexual dimorphism and a male may have a harem of many females and also defend a territory (Luetenegger 1978; Gage 1994; Fairbairn 1997; Balshine et al. 2001), but in other species a male may pair with a single female during a season (Cuadrado 2002). Although the mechanisms that determine monogamy or polygyny are known (Bull 2000 and references therein), alternative morphological features related to these social conditions (not related to body size) have been poorly studied.

Many lizard species of the genus Liolaemus show sexual dimorphism (Donoso-Barros 1966; Pincheira & Núñez 2005), including polygynous and monogamous species. Two Liolaemus species provide a good model to study the relationship between sexual dimorphism and sexual social system: Liolaemus tenuis (polygyny) and Liolaemus copiapoensis (monogamy). For L. tenuis, Müller & Hellmich (1933) reported color sexual dimorphism; males are very colorful with predominance of yellow in the anterior body region and blue-green colors in the posterior body region, in contrast to the melanistic color of females (Müller & Hellmich 1933; Donoso-Barros 1966; Vidal et al. 2005; Vidal et al. 2007). It has a polygynous social system; males are territorial (Manzur & Fuentes 1979) and use visual displays in their agonistic interactions (Trigosso-Venario et al. 2002). In contrast, L. copiapoensis shows sexual size dimorphism (Donoso-Barros 1966, Pincheira & Núñez 2005) however, the dorsal coloration is gray-brownish and the color variation between sexes is not apparent (Donoso-Barros 1966). Liolaemus copiapoensis has been reported to be monogamous, since when individuals have been extracted from sand caves in the desert they were always observed in couples (i.e. a single male with a single female) (Ortiz 1981). While there is no other reported data explicitly demonstrating monogamy in this species, the observations of Ortiz (pers. com.) were made during several years while doing his doctoral thesis. Monogamy has not been reported in other species of Chilean Liolaemus, thus L. copiapoensis was the best candidate for this study. In a previous study, Vidal et al. (2005) suggested that geometrically the sexual differentiation in L. tenuis is evident in the ocular area; males tend to develop more rounded and extended orbits than the females, with a frontal scale in the posterior position. These authors suggested that the male ocular extension could be related to a greater capacity for territory domination and more efficient vision of the females in the harem. The conjunction of these sexual advantages with the polygynous social system of L. tenuis (Manzur & Fuentes 1979, Labra & Niemeyer 1999) may be the most likely mechanism determining and explaining the observed sexual dimorphism (Vidal et al. 2005).

The aim of this study is to evaluate the morphological variation in the geometric shape of the orbit between sexes

MATERIALS AND METHODS

All materials used in this study belong to the collection of the Museum of Zoology of the Universidad de Concepcion (MZUC). A geometric morphometric analysis was used to assess the variation attributed exclusively to shape by analyzing landmarks or outlines of the shape (Kuhl & Guardina 1982; Bookstein 1991). Dorsal views of the heads of 77 adult specimens (Males = 41; Females = 36) of L. tenuis and 78 adult specimens (Males = 39; Females = 39) of L. copiapoensis were photographed with a Sony-Mavica digital camera. The outlines of the left orbits of each specimen (Fig. 1) were drawn. Using Elliptic Fourier transforms (which express outlines in periodic signals) these signals were then fitted by a sum of trigonometric functions (or harmonics) that have different amplitudes and phases. This method is based on the separate Fourier decompositions of the incremental changes of the x- and y- coordinates as a function of the cumulative length along the outline (Kuhl & Guardina 1982). Any harmonic corresponds to four coefficients: A and B for x and C and ^A n n n

D_n for y, defining an ellipse in the xy-plane. The coefficients of the first harmonic, describing the best-fitting ellipse of any outline, are used to standardize the size and orientation of the object. These coefficients therefore correspond to the residuals after standardization, and should not be included in statistical analyses (Crampton 1995; Renaud & Millien 2001; Renaud & Michaux 2003). This method also limits the influence of measurement errors by filtering out the noise that occurs in the details of the outline (Renaud & Millien 2001). Based on the Fourier coefficients, the shape was reconstructed by an inverse method (Crampton 1995) that allows visualization of the changes of the form involved, which are directly developed in the program Morpheus et al. (Slice 1998).

For each outline, thirty-two variables considering eight harmonics were obtained. Since the first harmonics showed no variation, only 29 coefficients or variables were considered. A characteristic of the Fourier harmonics is that the higher the rank of the harmonic, the more details of the outline are described. This property can be used to filter out measurement noise, which increases with harmonic rank (Renaud 1999). These variables were then used in multivariate statistical analyses. A two-way multivariate analysis of variance (MANOVA) (contrasting by sexes and species) were performed on these variables in order to evaluate the shape differences. Additionally, the orbit shape of all specimens was compared using a one-way analysis of variance (ANOVA), with sexes and species as a factor separately.

RESULTS AND DISCUSSION

Liolaemus tenuis and L. copiapoensis showed morphological differentiation in orbit shape. MANOVA indicated in all cases a morphological differentiation of the orbit shape between species (MANOVA, Wilks Lambda = 0.558; p = 0.0001) and sexes (Wilks Lambda = 0.697; p = 0.0119), but the interaction between the factors was not significant (Wilks Lambda = 0.760; p = 0.1389). Differentiation among Liolaemus species has been frequently evaluated from the morphological and genetic perspective (Donoso-Barros 1966; Cei 1986, 1993; Young 1998; Pincheira & Núñez 2005). Specifically, the variation between L. tenuis and L. copiapoensis has been evaluated only in taxonomic terms, suggesting morphological differentiation because they belong to distinct lineages (Schulte et al. 2000; Lobo 2001), although Pincheira & Núñez (2005) synonymized the species L. copiapoensis with L. bisignatus. On the other hand, from a phylogenetic point of view the polygynous social system

present in Phymaturus palluma is interesting (Habit & Ortiz 1996), since it is an ancestral species of the genus Liolaemus (Schulte et al. 2000; Lobo 2001). This allows speculation that the disappearance of this type of social system as in L. copiapoensis may have had multiple causes, which could be approached from a higher perspective (e.g., multiple origins of the social system in Liolaemus), which could lead to new research on the subject. However, the widespread lack of knowledge of the social systems in Liolaemus imposes a barrier to new studies.

Significant differences were found between sexes for L. tenuis (Wilks Lambda = 0.458; p = 0.019; Fig.2a); males had a more rounded and extended orbit shape than females. Although Vidal et al. (2005) suggested that L. tenuis differentiates its orbit shape according to social condition, there is currently no evidence to indicate that this type of differentiation is related to mating systems, except for the present study. Many other characters have been proposed to explain sexual dimorphism and the existence of a polygynous social system in reptiles, e.g., larger body size in males, occipital crest development, gular folds in males and other traits (Andersson 1994; Fairbairn 1997). Similarly, this new character (orbit shape) may also be related to this kind of differentiation. The results obtained in L. copiapoensis (monogamous) appear to corroborate these results since it did not have significant differences in orbit shape between sexes (Wilks Lambda = 0.578; p = 0.278; Fig. 2b).

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Figure 1. Eye orbit considered in shape analysis. Figura 1. Órbita del ojo considerada en el análisis de forma.

 

There were no significant differences between the orbit shape of L. tenuis females and both sexes of L. copiapoensis (Wilks Lambda = 0.647, p = 0.586) which indicates that differences are given mainly by the orbit shape of males from the polygynous species. While the differences found in this study are interesting, it is important to note that microhabitats used by the two Liolaemus species are different, affecting orbit shape. In fact, Schulte et al. (2004) reported that L. tenuis is an arboreal species that uses high perches, while L. copiapoensis is a desert species whose activity is mainly in the sand (although there are rocks available as perches). However, differences in orbit shape in L. tenuis could be explained because a male increases the height of his perch to increase his number of females (Manzur & Fuentes 1979), favoring morphological changes (shape of the orbit), which could have an adaptive value.

Thanks to J.C. Ortiz for providing the specimens from Museo de Zoología, Universidad de Concepción and to P. Arancibia y L. Eaton for comments in previous version of manuscript.

This study was supported by CONICYT 79090026.

BIBLIOGRAPHY

Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton, New Jersey.         [ Links ]

Balshine, S., Leach, B., Neat, F., Reid, H., Taborsky, M. & Werner, N. 2001. Correlates of group size in a cooperatively breeding cichlid fish (Neolamprologus pulcher). Behavioral Ecology and Sociobiology 50: 134-140.         [ Links ]

BOOKSTEIN, F.L. 1991. Morphometrics tools for landmark data: geometry and biology. New York. Cambridge University Press.         [ Links ]

BULL, C.M. 2000. Monogamy in lizards. Behavioural Processes 51: 7-20.         [ Links ]

Cei, J.M. 1986. Reptiles del centro, centro-oeste y sur de la Argentina. Herpetofauna de las zonas áridas y semiáridas. Museo Regionale di Scienze Naturali Torino (Italy) 4: 1527.         [ Links ]

Cei, J.M. 1993. Reptiles de noroeste, nordeste y este de la Argentina. Herpetofauna de las selvas subtropicales, Puna y Pampas. Museo Regionale di Scienze Naturali (Italy) 14: 1-949.         [ Links ]

Crampton, J.S. 1995. Elliptic Fourier shape analysis of fossil bivalves: some practical considerations. Lethaia 28: 179-186.         [ Links ]

Cuadrado, M. 2002. Sistemas de apareamiento en reptiles: una revisión. Revista Española de Herpetología 2002: 61-69.         [ Links ]

Desjardins, J.K., FITZPATRICK, J.L., Stiver, K.A., Van Der Kraal, G.J. & Balshine, S. 2008. Costs and benefits of polygyny in the cichlid Neolamprologus pulcher. Animal Behaviour 75: 1771-1779        [ Links ]

Donoso-Barros, R. 1966. Los reptiles de Chile. Ediciones de la Universidad de Chile, Santiago, Chile.         [ Links ]

Fairbain, D. 1990. Factors influencing sexual size dimorphism in temperate waterstriders. American Naturalist 136: 61-86.         [ Links ]

Fairnairn, D. 1997. Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology, Evolution, and Systematics 28: 659-687.         [ Links ]

Gage, M.J.G. 1994. Associations between body size, mating pattern, testes size and sperm lengths across butterflies. Proceedings of the Royal Society London-Series B. 258: 247-254.         [ Links ]

Habit, E. & Ortiz J.C. 1996. Patrones de comportamiento y organización social de Phymaturus flagellifer (Reptilia, Tropiduridae). In: Herpertología Neotropical (Ed. J.E. Péfaur) Mérida, Universidad de Los Andes, Consejo de publicaciones. pp. 141-154.         [ Links ]

Kuhl, F.P. & GIARDINA, C.R. 1982. Elliptic Fourier features of a closed contour. Computer Graphics and Image Processing 18: 236-258.         [ Links ]

Labra, A. & NIEMEYER, H.M. 1999. Intraspecific chemical recognition in the lizard Liolaemus tenuis. Journal of Chemical Ecology 25: 1799-1811.         [ Links ]

Lobo, F. 2001. A phylogenetic analysis of lizards of the Liolaemus chiliensis group (Iguania: Tropiduridae). Herpetological Journal 11: 137-150.         [ Links ]

Luetenegger, W. 1978. Scaling of sexual dimorphism in body size and breeding system in primates. Nature 272: 610-611.         [ Links ]

Manzur, M.I. & Fuentes, E.R. 1979. Polygyny and agonistic behavior in the tree-dwelling lizard Liolaemus tenuis (Iguanidae). Behavioral Ecology and Sociobiology 6: 23-28.         [ Links ]

Müller, L. & Hellmich W. 1933. Beitrage zur Kenntnis der Herpetofauna Chiles. VIII. Bermerkungen über Liolaemus tenuis (Duméril et Bibron). Zoologische Anzeiger 104: 305-310.         [ Links ]

Ortiz, J.C. 1981. Révision taxonomique et biologie des Liolaemus du groupe nigromaculatus (Squamata, Iguanidae). Thèse de Doctorat d'Étatès Sciences Naturelles, Université Paris VII.         [ Links ]

PINCHEIRA, D. & Núñez, H. 2005. Las especies chilenas del género Liolaemus Wiegmann 1834 (Iguania: Tropiduridae: Liolaeminae) Taxonomía, sistemática y evolución. Museo Nacional de Historia Natural (Chile) 59: 1-486.         [ Links ]

Renaud, S. 1999. Size and shape variability in relation to species differences and climatic gradients in the African rodent Oenomys. Journal of Biogeography 26: 857-865.         [ Links ]

Renaud, S. & MICHAUX, J.R. 2003. Adaptive latitudinal trends in the mandible shape of Apodemus wood mice. Journal of Biogeography 30: 1617-1628.         [ Links ]

Renaud, S. & MILLIEN, V. 2001. Intra- and interspecific morphological variation in the field mouse species Apodemus argenteus and A. speciosus in the Japanese archipelago: the role of insular isolation and biogeographic gradients. Biological Journal of the Linnean Society 74: 557-569.         [ Links ]

Schoener, T., Slade J. & Stinson, C. 1982. Diet and sexual dimorphism in the very catholic lizard genus, Leiocephalus, of the Bahamas. Oecologia 53: 160-169.         [ Links ]

Schulte II, J.A., Macey, R.J., Espinoza, R.E. & Larson, A. 2000. Phylogenetic relationships in the iguanid lizard genus Liolaemus: multiple origins of viviparous reproduction and evidence for recurring Andean vicariance and dispersal. Biological Journal of the Linnean Society 69: 75-102.         [ Links ]

Schulte II, J.A., Losos, J.B., Cruz, F.B. & Núñez, H. 2004. The relationship between morphology, escape behaviour and microhabitat occupation in the lizard clade Liolaemus (Iguanidae: Tropidurinae: Liolaemini). Journal of Evolutionary Biology 17: 408-420         [ Links ]

Shine, R. 1986. Sexual differences in morphology and niche utilization in an aquatic snake, Acrochordus arafurae. Oecologia 69: 260-267.         [ Links ]

Slice, D.E. 1998. Morpheus et al.: software for morphometric research. Stony Brook, NY: Department of Ecology and Evolution, State Univ. of New York.         [ Links ]

Stamps, J.A. 1993. Sexual size dimorphism in species with asymptotic growth after maturity. Biological Journal of the Linnean Society 50: 123-145.         [ Links ]

Trigosso-Venario, R., Labra, A. & Niemeyer, H.M. 2002. Interactions between males of the lizard Liolaemus tenuis: Roles of familiarity and memory. Ethology 108: 1-8.         [ Links ]

Verrastro, L. 2004. Sexual dimorphism in Liolaemus occipitalis (Iguania, Tropiduridae). Iheringia 94: 45-48.         [ Links ]

Vidal, M.A., Ortiz, J.C. & Labra, A. 2007. Sexual and geographic variation of color patterns in Liolaemus tenuis (Squamata, Liolaeminae). Gayana 71: 27-33.         [ Links ]

Vidal, M.A., Ortiz, J.C., Ramírez, C.C. & Lamborot, M. 2005. Intraspecific variation in morphology and sexual dimorphism in Liolaemus tenuis (Tropiduridae). Amphibia-Reptilia 26: 343-351.         [ Links ]

Watkins, G.G. 1996. Proximate causes of sexual size dimorphism in the iguanian lizard Microlophus occipitalis. Ecology 77: 1473-1482.         [ Links ]

Watkins, G.G. 1998. Function of a secondary sexual ornament: the crest in the South American iguanian lizard Microlophus occipitalis (Peters, Tropiduridae). Herpetologica 54: 161-169.         [ Links ]

Young-Downey, A.R. 1998. Phylogenetic studies on Liolaemus (Sauria: Tropiduridae): an interpretation based on molecular data and a biochemical test of a biogeographic hypothesis. Tesis Doctoral, University of Miami. 84 pp.         [ Links ]

Recibido: 04.05.11

Aceptado: 14.07.11