Insularity affects head morphology,bite force and diet in a Mediterranean lizard

Island environments differ with regard to numerous features from the mainland and may induce large‐scale changes in most aspects of the biology of an organism. In this study, we explore the effect of insularity on the morphology and performance of the feeding apparatus, a system crucial for the survival of organisms. To this end, we examined the head morphology and feeding ecology of island and mainland populations of the Balkan green lizard, Lacerta trilineata. We predicted that head morphology, performance and diet composition would differ between sexes and habitats as a result of varying sexual and natural selection pressures. We employed geometric morphometrics to test for differences in head morphology, measured bite forces and analysed the diet of 154 adult lizards. Morphological analyses revealed significant differences between sexes and also between mainland and island populations. Relative to females, males had larger heads, a stronger bite and consumed harder prey than females. Moreover, island lizards differed in head shape, but not in head size, and, in the case of males, demonstrated a higher bite force. Islanders had a wider food niche breadth and included more plant material in their diet. Our findings suggest that insularity influences feeding ecology and, through selection on bite force, head morphology. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 469–484.     

It is all in the head: morphological basis for differences in bite force among colour morphs of the Dalmatian wall lizard

Males of the lizard Podarcis melisellensis occur in three distinct colours that differ in bite performance, with orange males biting harder than white or yellow ones. Differences in bite force among colour morphs are best explained by differences in head height, suggesting underlying variation in cranial shape and/or the size of the jaw adductors. To explore this issue further, we examined variation in cranial shape, using geometric morphometric techniques. Additionally, we quantified differences in jaw adductor muscle mass. No significant differences in size corrected head shape were found, although some shape trends could be detected between the colour morphs. Orange males have relatively larger jaw adductors than yellow males. Not only the mass of the external jaw adductors, but also that of the internal jaw adductors was greater for the orange morph. Data for other cranial muscles not related to biting suggest that this is not the consequence of an overall increase in robustness in orange individuals. These results suggest that differences in bite performance among morphs are caused specifically by an increase in the mass of the jaw adductor, which may be induced by differences in circulating hormone levels.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 13–22.     

On the sexual dimorphism in the skull of the tiger (Panthera tigris)

Sexual dimorphism in the skull of the tiger (Panthera tigris) is reviewed and described in detail. The most significant diagnostic differences between the sexes are absolute length of the cranium, breadth of interorbital region and muzzle, zygomatic arch, and occipital region, length of upper carnassial, and the degree of the development of the cranial prominences. The degree of sexual dimorphism is closely related to geographic variation, and its form is rather complex.     

Chromatophores and color change in the lizard,Anolis carolinensis

Summary The skin of the lizard, Anolis carolinensis, changes rapidly from bright green to a dark brown color in response to melanophore stimulating hormone (MSH). Chromatophores responsible for color changes of the skin are xanthophores which lie just beneath the basal lamina containing pterinosomes and carotenoid vesicles. Iridophores lying immediately below the xanthophores contain regularly arranged rows of reflecting platelets. Melanophores containing melanosomes are present immediately below the iridophores. The ultrastructural features of these chromatophores and their pigmentary organelles are described. The color of Anolis skin is determined by the position of the melanosomes within the melanophores which is regulated by MSH and other hormones such as norepinephrine. Skins are green when melanosomes are located in a perinuclear position within melanophores. In response to MSH, they migrate into the terminal processes of the melanophores which overlie the xanthophores above, thus effectively preventing light penetration to the iridophores below, resulting in skins becoming brown. The structural and functional characteristics of Anolis chromatophores are compared to the dermal chromatophore unit of the frog.This study was supported in part by GB-8347 from the National Science Foundation.Contribution No. 244, Department of Biology, Wayne State University.The authors are indebted to Dr. Joseph T. Bagnara for his encouragement during the study and to Dr. Wayne Ferris for his advice and the use of his electron microscope laboratory.     

Sexual dimorphism in lizard body shape: the roles of sexual selection and fecundity selection

Sexual dimorphism is widespread in lizards, with the most consistently dimorphic traits being head size (males have larger heads) and trunk length (the distance between the front and hind legs is greater in females). These dimorphisms have generally been interpreted as follows: (1) large heads in males evolve through male-male rivalry (sexual selection); and (2) larger interlimb lengths in females provide space for more eggs (fecundity selection). In an Australian lizard (the snow skink, Niveoscincus microlepidotus), we found no evidence for ongoing selection on head size. Trunk length, however, was under positive fecundity selection in females and under negative sexual selection in males. Thus, fecundity selection and sexual selection work in concert to drive the evolution of sexual dimorphism in trunk length in snow skinks.     

Craniofacial sexual dimorphism in a Northern-Greek pre-pubertal population

Craniofacial sexual dimorphism on size and shape in a prepubertal (6–12 years of age) population of northern Greece has been studied by means of both univariate and multivariate analysis. The structure of population was limiting the influence of environmental and genetic factors. Even though there have been observed statistical significant differences between the sexes in most of the variables it has not been concluded any sexual dimorphism in the morphology of the craniofacial area.     

Distribution of arginine vasotocin in the brain of the lizard Anolis carolinensis

Summary The distribution of immunoreactive arginine vasotocin (AVT-ir) was determined in the brain of the lizard Anolis carolinensis. Cells and fibers containing AVT-ir were found in the medial septal region, lamina terminalis, lateral forebrain bundle, preoptic area, supraoptic nucleus, anterior hypothalamus, paraventricular nucleus, periventricular nucleus, arcuate nucleus, and ventromedial nucleus of the thalamus. Occasional AVT-ir cells were found in the interpeduncular nucleus. Fibers containing AVT-ir were found in the cortex, around the olfactory ventricle, in the diagonal band of Broca, amygdala area, dorsal ventricular ridge, striatum, nucleus accumbens, septum, ventromedial hypothalamus, lateral hypothalamus, medial forebrain bundle, median eminence, pars nervosa, nucleus of the solitary tract, locus coeruleus, cerebellar cortex (granular layer), dorsal part of the nucleus of the lateral lemniscus, substantia nigra, and myelencephalon. The intensity of AVT-ir staining was, in general, greater in males than in females. Comparison of AVT-ir distribution in A. carolinensis with those previously published for other reptilian species revealed species-specific differences in distribution of AVT.     

Genetic basis of sexual dimorphism in the threespine stickleback Gasterosteus aculeatus

Sexual dimorphism (SD) in morphological, behavioural and physiological features is common, but the genetics of SD in the wild has seldom been studied in detail. We investigated the genetic basis of SD in morphological traits of threespine stickleback (Gasterosteus aculeatus) by conducting a large breeding experiment with fish from an ancestral marine population that acts as a source of morphological variation. We also examined the patterns of SD in a set of 38 wild populations from different habitats to investigate the relationship between the genetic architecture of SD of the marine ancestral population in relation to variation within and among natural populations. The results show that genetic architecture in terms of heritabilities, additive genetic variances and covariances (as well as correlations) is very similar in the two sexes in spite of the fact that many of the traits express significant SD. Furthermore, population differences in threespine stickleback body shape and armour SD appear to have evolved despite constraints imposed by genetic architecture. This implies that constraints for the evolution of SD imposed by strong genetic correlations are not as severe and absolute as commonly thought.     

A circadian clock measures photoperiodic time in the male lizard Anolis carolinensis

Summary Photoperiod plays an important role in controlling the annual reproductive cycle of the male lizard Anolis carolinensis. The nature of photoperiodic time measurement in Anolis was investigated by exposing anoles to 3 different kinds of lighting paradigms (resonance, T cycles, and night breaks) to determine if photoperiodic time measurement involves the circadian system. Both the reproductive response and the patterns of entrainment of the activity rhythm were assessed. The results show that the circadian system is involved in photoperiodic time measurement in this species and that a discrete photoinducible phase resides in the latter half of the animals' subjective night. Significantly, the ability of the circadian system to execute photoperiodic time measurement is crucially dependent on the length of the photoperiod. Resonance, T cycle and night break cycles utilizing a photoperiod 10–11 h in duration reveal circadian involvement whereas these same cycles utilizing 6 or 8 h photoperiods do not.Abbreviation CRPP circadian rhythm of photoperiodic sensitivity     

Bite force in vertebrates: opportunities and caveats for use of a nonpareil whole-animal performance measure

Measurements of whole-organism performance traits have been useful in studies of adaptation and phenotype–environment correlations. Bite force capacities may be tightly linked to both the type and magnitude of the ecological challenges of food acquisition, mate acquisition, and antipredation in vertebrates. In the present study, we present technical details on bite meters and on measuring bite forces. The ability to take reliable measurements depends on specific features of the measuring device and on where in the mouth the bite is applied. Using both previously available and original data, we demonstrate several ecologically and evolutionarily relevant features of bite force measurements. First, maximal bite forces are repeatable among individuals across all vertebrates studied to date. Second, in ectotherms such as lizards, maximal bite forces are affected by body temperature and motivational states. Third, bite forces are strongly correlated with head size and shape. Fourth, bite forces correlate with features of prey of vertebrates. Finally, bite forces are linked to male dominance and correlated with social-display structures. Thus, bite force performance measures can be used as 'traits', and thus be used in integrative studies at multiple levels of organismal biology. Accordingly, bite force data will help our understanding of the functions, capacities, and evolution of jaw–cranial musculoskeletal systems. Moreover, a plethora of opportunities exist for the use of bite force measurements, and if methods are carefully applied, several levels of organismal and ecological organization can be integrated to aid our understanding of the ecology and evolution of vertebrate taxa.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 709–720.     

Sexual dimorphism in histological characteristics and contractility of the iliofibularis muscle in the lizard Sceloporus torquatus

The iliofibularis is a hindlimb muscle used in lizard locomotion that is composed of at least three types of fibres: fast‐twitch‐glycolytic (FG), fast‐twitch‐oxidative‐glycolytic fibre (FOG) and slow‐twitch‐oxidative (SO). The striated skeletal muscle is a highly plastic tissue undergoing phenotypic change in response to activity. The lizard Sceloporus torquatus has sexual differences associated with microhabitat use, which can be reflected in the physiology and anatomy of the muscle, and thus, in our study, we analysed the morphological and contractile characteristics of the iliofibularis muscle (IF) of S. torquatus males and females. We found a larger prevalence of FOG compared with FG and SO fibres in the muscle of both sexes. We also found that males show larger areas of the three types of fibres, develop greater strength but also faster fatigue than females, suggesting that strength is a key functional feature that enables males to perform faster movements (but for shorter periods), associated with the demands of territoriality.     

Functional and ecological relevance of intraspecific variation in body size and shape in the lizard Podarcis melisellensis (Lacertidae)

Within populations, individual animals may vary considerably in morphology and ecology. The degree to which variation in morphology is related to ecological variation within a population remains largely unexplored. We investigated whether variation in body size and shape among sexes and age classes of the lizard Podarcis melisellensis translates in differential whole-animal performance (sprint speed, bite force), escape and prey attack behaviour in the field, microhabitat use and diet. Male and female adult lizards differed significantly in body size and head and limb proportions. These morphological differences were reflected in differences in bite strength, but not in sprint speed. Accordingly, field measurements of escape behaviour and prey attack speed did not differ between the sexes, but males ate larger, harder and faster prey than females. In addition to differences in body size, juveniles diverged from adults in relative limb and head dimensions. These shape differences may explain the relatively high sprint and bite capacities of juvenile lizards. Ontogenetic variation in morphology and performance is strongly reflected in the behaviour and ecology in the field, with juveniles differing from adults in aspects of their microhabitat use, escape behaviour and diet.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 251–264.     

Ultrastructural localization of hair keratin homologs in the claw of the lizard Anolis carolinensis

The claw of lizards is largely composed of beta‐keratins, also referred to as keratin‐associated beta‐proteins. Recently, we have reported that the genome of the lizard Anolis carolinensis contains alpha keratin genes homologous to hair keratins typical of hairs and claws of mammals. Molecular and immunohistochemical studies demonstrated that two hair keratin homologs named hard acid keratin 1 (HA1) and hard basic keratin 1 (HB1) are expressed in keratinocytes forming the claws of A. carolinensis. Here, we extended the immunocytochemical localization of the novel reptilian keratins to the ultrastructural level. After sectioning, claws were subjected to immunogold labeling using antibodies against HA1, HB1, and, for comparison, beta‐keratins. Electron microscopy showed that the randomly organized network of tonofilaments in basal and suprabasal keratinocytes becomes organized in long and parallel bundles of keratin in precorneous layers, resembling cortical cells of hairs. Entering the cornified part of the claw, the elongated corneous cells fuse and accumulate corneous material. HA1 and HB1 are absent in the basal layer and lower spinosus layers of the claw and are expressed in the upper and precorneous layers, including the elongating corneocytes. The labeling for alpha‐keratin was loosely associated with filament structures forming the fibrous framework of the claws. The ultrastructural distribution pattern of hard alpha‐keratins resembled that of beta‐keratins, which is compatible with the hypothesis of an interaction during claw morphogenesis. The data on the ultrastructural localization of hair keratin homologs facilitate a comparison of lizard claws and mammalian hard epidermal appendages containing hair keratins. J. Morphol., 2011. © 2010 Wiley‐Liss, Inc.     

Ontogenic sources of variation in sexual size dimorphism in a viviparous lizard

To elucidate the developmental aspects of the evolution of sexual size dimorphism (SSD), an understanding of the sex-specific ontogeny of body size is critical. Here, we evaluate the relative importance of genetic and environmental determinants of SSD in juvenile common lizards (Lacerta vivipara). We examined the prenatal and post-natal effects of population density and habitat humidity on SSD, as well as the maternal effects of food availability, corticosterone level, humidity and heat regime during gestation. Analyses indicated strong prenatal and post-natal plasticity in body size per se and yielded three main results with respect to SSD. First, SSD in juvenile common lizards matches qualitatively the SSD observed in adults. Secondly, SSD was influenced by none of the prenatal factors investigated here, suggesting poor sex-biased maternal effects on offspring size. Thirdly, SSD was sensitive to post-natal habitat humidity, which positively affected growth rate more strongly in females than in males. Thus, natural variation in SSD in juvenile common lizards appears to be primarily determined by a combination of sex-biased genetic factors and post-natal conditions. We discuss the possibility that viviparity may constrain the evolution of sex-biased maternal effects on offspring size.     

Scaling relationships between craniofacial sexual dimorphism and body mass dimorphism in primates: implications for the fossil record

Craniofacial remains (the most abundant identifiable remains in the fossil record) potentially offer important information about body size dimorphism in extinct species. This study evaluates the scaling relationships between body mass dimorphism and different measures of craniofacial dimorphism, evaluating taxonomic differences in the magnitude and scaling of craniofacial dimorphism across higher taxonomic groups. Data on 40 dimensions from 129 primate species and subspecies demonstrate that few dimensions change proportionally with body mass dimorphism. Primates show general patterns of greater facial vs. neurocranial and orbital dimorphism, and greater dimorphism in lengths as opposed to breadths. Within any species, though, different craniofacial dimensions can yield very different reconstructions of size dimorphism. There are significant taxonomic differences in the relationships between size and craniofacial dimorphism among primate groups that can have a significant impact on reconstructions of body mass dimorphism. Hominoids tend to show lower degrees of facial dimorphism proportional to size dimorphism than other primates. This in turn implies that strong craniofacial dimorphism in Australopithecus africanus could imply very strong body size dimorphism, conflicting with the relatively modest size dimorphism inferred from postcrania. Different methods of estimating the magnitude of size dimorphism from craniofacial measurements yield similar results, and yield comparatively low percent prediction errors for a number of dimensions. However, confidence intervals for most estimates are so large as to render most estimates highly tentative.     

Mining online genomic resources in Anolis carolinensis facilitates rapid and inexpensive development of cross-species microsatellite markers for the Anolis lizard genus

Online sequence databases can provide valuable resources for the development of cross-species genetic markers. In particular, mining expressed tag sequences (EST) for microsatellites and developing conserved cross-species microsatellite markers can provide a rapid and relatively inexpensive method to develop new markers for a range of species. Here, we adopt this approach to develop cross-species microsatellite markers in Anolis lizards, which is a model genus in evolutionary biology and ecology. Using EST sequences from Anolis carolinensis, we identified 127 microsatellites that satisfied our criteria, and tested 49 of these in five species of Anolis (carolinensis, distichus, apletophallus, porcatus and sagrei). We identified between 8 and 25 new variable genetic markers for five Anolis species. These markers will be a valuable resource for studies of population genetics, comparative mapping, mating systems, behavioural ecology and adaptive radiations in this diverse lineage.     

Using visual modelling to study the evolution of lizard coloration: sexual selection drives the evolution of sexual dichromatism in lacertids

Sexual selection has been invoked as a major force in the evolution of secondary sexual traits, including sexually dimorphic colourations. For example, previous studies have shown that display complexity and elaborate ornamentation in lizards are associated with variables that reflect the intensity of intrasexual selection. However, these studies have relied on techniques of colour analysis based on human – rather than lizard – visual perception. Here, we use reflectance spectrophotometry and visual modelling to quantify sexual dichromatism considering the overall colour patterns of lacertids, a lizard clade in which visual signalling has traditionally been underrated. These objective methods of colour analysis reveal a large, previously unreported, degree of sexual dichromatism in lacertids. Using a comparative phylogenetic approach, we further demonstrate that sexual dichromatism is positively associated with body size dimorphism (an index of intrasexual selection), suggesting that conspicuous coloration in male lacertids has evolved to improve opponent assessment under conditions of intense male–male competition. Our findings provide the first evidence for the covariation of sexual dichromatism and sexual size dimorphism in lacertids and suggest that the prevalent role of intrasexual selection in the evolution of ornamental coloration is not restricted to the iguanian lineage, but rather may be a general trend common to many diurnal lizards.