Experimental and demographic analyses of growth rate and sexual size dimorphism in a lizard, Sceloporus undulatus

Sexual size dimorphism (SSD) is a common phenomenon caused by a variety of environmental and genetic mechanisms in animals. In the current study, we investigate the demography of a population of eastern fence lizards ( Sceloporus undulatus ) to compare age structure and survivorship between the sexes, and we examine growth rates of juveniles under both natural and controlled laboratory conditions to elucidate causes of SSD in this species. Furthermore, using our laboratory growth data, we examine the heritability of juvenile growth rates. Our results show that SSD develops in the field before the end of the first year of age (before sexual maturity) because juvenile females grow more rapidly than juvenile males. In the laboratory environment, however, we observed no sexual difference in growth rates for lizards up to the size of maturity in the field. Thus, sexual differences in growth rate and subsequent development of SSD in this population are highly plastic and subject to strong proximal control. We found high levels of additive genetic variance for juvenile growth, indicating a strong potential for selection to operate on juvenile growth rates. Our results indicate that selection on juvenile growth rate could account for differences in growth among populations but would not necessarily contribute to SSD within our population due to the high plasticity in growth rate.     

Seasonal alterations in adrenocortical cell function associated with stress-responsiveness and sex in the eastern fence lizard (Sceloporus undulatus)

We characterized steroidogenic properties of dispersed adrenocortical cells from field-active male and female eastern fence lizards (Sceloporus undulatus) to investigate whether alterations in cell function could, in part, explain seasonal variation in baseline and stress-induced plasma corticosterone (B). Lizards were collected during the breeding and postbreeding seasons and shortly prior to hibernation. Dispersed cells in vitro produced B, aldosterone (ALDO), and progesterone in response to 8-Br-cAMP, 25-(OH)cholesterol, adrenocorticotropin (ACTH; as little as 100 fM), and angiotensin II. Maximal progesterone, B, and ALDO responses to ACTH were roughly 1000%, 500%, and 100% greater than corresponding basal values. Angiotensin II was an effective steroidogenic stimulant but much less so than ACTH. Corticosteroid production exhibited considerable steroid-specific variation among seasons. Maximal ACTH-induced B production was lower in the postbreeding season than at either of the other two measurement points, essentially opposite to the pattern for ALDO. Males and females generally produced B at similar rates, but ALDO and progesterone showed numerous sex differences that usually covaried between the two steroids. Cellular sensitivity to 25-(OH)cholesterol and angiotensin II showed few sex differences or seasonal changes. In contrast, sensitivity to ACTH decreased markedly from the breeding to the postbreeding season in males, corresponding to the decrease in stress-responsiveness, and in both sexes was considerably lower prior to hibernation than during the breeding season. Under some conditions, plasma B may be limited by the production capacity of adrenocortical cells. In summary, seasonal variations in body condition, reproductive activity, and baseline and stress-induced plasma B may be attributed at least in part to alterations in adrenocortical cell steroidogenic function.     

Indomethacin influences arginine vasotocin-induced parturition and oviposition in lizards (Sceloporus jarrovi and Sceloporus undulatus )

The effect of the prostaglandin blocker indomethacin on arginine vasotocin-induced birth was examined. Gravid female, oviparous (Sceloporus undulatus ) and viviparous (Sceloporus jarrovi ) lizards were pretreated with saline or indomethacin, a potent blocker of PG synthesis. Pretreatment was followed by an intraperitoneal injection of AVT. Pretreatment with indomethacin significantly delayed the onset of AVT-induced oviposition in S. undulatus , whereas it had no effect on latency to birth in S. jarrovi . Female S. jarrovi treated with indomethacin, however, gave birth to only part of the total litter, whereas control females gave birth to complete litters. In viviparous females, an interaction of embryonic age with pretreatment was evident; females having more developed embryos decreased birth latency significantly and increased the percentage of parturition when compared with females that had embryos at earlier stages of development. Our data suggest that although exogenous AVT can stimulate oviposition or parturition, these events occur more rapidly and completely when prostaglandin synthesis is not inhibited.     

Plasma androgens and their association with the reproductive cycle of the male fence lizard, Sceloporus undulatus

Seasonal variation in plasma androgen levels was determined for males of the lizard Sceloporus undulatus. Plasma androgens peaked in both spring and in fall prior to brumation, coinciding with periods of maximum testicular enlargement and advanced spermatogenic development. Plasma androgen concentrations were minimal during summer, following testicular regression and breeding in spring. Epididymal masses were positively correlated to plasma androgen levels, while abdominal fat body masses demonstrated a negative correlation.     

Thermal sensitivity of sprint-running in the lizard Sceloporus undulatus: support for a conservative view of thermal physiology

Summary The thermal sensitivity of sprint-running ability was investigated in two populations of Sceloporus undulatus that occupy thermally distinct habitats. Integration of field and laboratory data indicates that lizards inhabiting a cool, high-elevation habitat are frequently active at body temperatures that retard sprint-running velocity, which could affect adversely their ability to evade predators and to capture prey. These negative effects might be expected to select for local adaptation of thermal physiology. No differences in thermal physiology (optimal temperature for sprinting, critical thermal limits) were found, however, between lizards from the two habitats.Preferred body temperature of Sceloporus undulatus is lower than the body temperature that maximizes sprint velocity but is still well within an optimal performance range where lizards can run at better than 95% of maximum velocity. Analysis of data from other studies shows a similar concordance of preferred body temperature and temperatures that maximize sprint velocity for some, but not all lizard species studied.Low diversity of predators and high levels of food may compensate in part for the reduced sprinting ability of highelevation lizards active at low body temperatures. The lack of population differentiation supports the view that lizard thermal physiology is evolutionarily conservative.     

The Ontogeny of Display Behaviour in Sceloporus undulatus: (Sauria: Iguanidae)

A longitudinal study (from neonate to adult) was made of the display behaviour of 36 fence lizards from 8 clutches. A frame-by-frame analysis of 941 video-taped displays revealed that the hatchlings possessed almost all of their adult display patterns by the first two days of life. Of the total variance in the display behaviour, 7% or less was attributed to experience. Of the variance among lizards, approximately half came from between clutches and half from between clutchmates. Our data indicate that the visual communication signals (head bob displays) of this vertebrate species are almost totally innate.     

Ultrastructural analysis of iridophore organellogenesis in a lizard, Sceloporus graciosus (Reptilia: Phrynosomatidae)

Transmission electron microscopy (TEM) data from the ultrastructure of lizard skin iridophores (reflective dermal chromatophores) are used to illustrate the organellogenesis of small rectangular reflecting platelets, which are the color-generating components of these cells. During the development of reflecting platelets, crystals are deposited within double-membraned vesicles from electron-dense material located within the vesicles. The crystals are initially small but expanded lengthwise eventually to fill the vesicle that contains them. The inner membrane then tightly surrounds the crystal whereas the outer membrane is much more loosely associated with the inner-membrane-bound crystal. These observations allow discussion of the possible origin of the precursor double-membraned vesicles from endoplasmic reticulum (ER) and Golgi-derived vesicles. A model is proposed that incorporates our findings and other published reports to explain the origin of the precursor double-membraned vesicles via three alternative pathways.     

Purification and characterization of liver lectins from a lizard, Sceloporus spinosus

This study discusses the purification of soluble beta-galactose lectins obtained from the lizard liver of Sceloporus spinosus. The first lectin named lizard hepatic lectin-1 (LHL-1) presented a molecular weight of 31,750, with an isoelectric point of 4.25. The highest specific hemagglutinating activity was achieved using human blood type A1: N-acetylgalactosamine (GalNAc)-galactose (Gal)-fucose (Fuc). Carbohydrate inhibition assays indicated a higher lectin specificity for GalNAc. For LHL-2 the molecular weight obtained was 23,850 with an isoelectric point of 3.25. The highest carbohydrate specificity was observed for Gal. These lizard hepatic lectins are similar to the mammal hepatic lectins previously reported. However, it is different from the alligator hepatic lectin (AHL). The homology analyses of LHL-1 resulted in 100% identity with the Steroidogenic acute regulatory protein (StAR), while LHL-2 was similar to adenylate kinase (75% identity). We suggest that these liver lectins are related to the inherent functions of liver previously reported.     

An experimental manipulation of food and water: growth and time-space utilization of hatchling lizards (Sceloporus undulatus)

Summary At a site in western Nebraska, we studied the effects of supplemental food and water on growth, survival, and habitat utilization of hatchling iguanid lizards, Sceloporus undulatus. Hatchlings were randomly assigned to one of four experimental groups and received either (1) supplemental food only, (2) supplemental water only, (3) supplemental food and water, or (4) neither supplemental food nor water (control). Neither supplemental food nor supplemental water affected growth rate in length, growth rate in mass, or size-specific body mass (i.e. robustness) at the end of the treatment period. Over the 45 day treatment pierod, there were no significant differences among treatment groups in survival, home-range size, or habitat utilization. There were, however, significant differences in the index of activity. Hatchlings in the treatment groups receiving supplemental water were sighted more often than hatchlings in the control group. We conclude that, during our study, neither food nor water limited growth but that water limited activity.     

Female-specific color is a signal of quality in the striped plateau lizard (Sceloporus virgatus)

Recent theoretical and empirical studies confirm that male matechoice and/or female–female mate competition can be expressedin the absence of sex-role reversal. Such reproductive patternsmay select for the evolution of female traits that indicatefemale phenotypic or genotypic quality among non–role-reversedspecies. Although attention to the evolution and function offemale ornaments is increasing, additional focus is needed onfemale-specific ornaments (those not expressed in conspecificmales) and on nonavian systems in order to gain a broad understandingof how selection acts directly on ornamentation of female animals.In the striped plateau lizard, Sceloporus virgatus, only femalesdevelop orange throat patches during the reproductive season.The color peaks in expression near the time of ovulation andappears to stimulate male courtship. Here, I examine whetherthis female-specific ornament can be used by males to reliablyassess female phenotypic quality. Using multivariate regressionanalyses, I show that the area of the orange color patch predictsbody condition and mite load, the chroma (i.e., saturation)of the color patch predicts body size, and both patch area andchroma reliably predict average egg mass. Thus, female reproductivecolor may function as a condition-dependent signal, indicatingphenotypic quality to potential mates.     

Reproductive ecology of red-chinned lizards (Sceloporus undulatus erythrocheilus) in Southcentral Colorado: comparisons with other populations of a wide-ranging species

Summary We studied the reproductive ecology of a population of Sceloporus undulatus erythrocheilus near Walsenburg, CO during the summers of 1987–1990. Reproductive activity commences soon after emergence in early May and continues until the middle of July. Females mature in their second year following hatching at an age of 20–21 months and a size of 60–63 mm snout-vent length (SVL). Two clutches, averaging10.9 eggs, are produced per year. Larger females produce larger clutches with an increase of one egg per 3 mm SVL. Average SVL of females was 71 mm. Eggs are reasonably large (0.32 g) and relative clutch mass was the largest reported for the species (34% of body mass). A principal component analysis was used to examine relationships among reproductive characters in 12 populations of Sceloporus undulatus. The analysis suggested that patterns of reproduction in this wide-ranging species result from several factors reflecting both adaptive and phylogenetic sources of variation.     

Natural history of the lizard Enyalius brasiliensis (Lesson, 1828) (Leiosauridae) from an Atlantic forest of southeastern Brazil.

Information on the ecology of lizard species from the Brazilian Atlantic Forest is scarce and almost nothing is known about the ecology of lizards of the genus Enyalius. In this study, we provide information about some aspects of the natural history of E. brasiliensis from an area of Atlantic Forest in Ilha Grande, RJ. Enyalius brasiliensis (N = 15) feeds mainly on arthropods. The most frequent food items were insect larvae, orthopterans, and ants; in terms of volume, larvae and termites were the most important food items; ants and termites were the most numerous prey categories. Two females were reproductive (one had 10 and the other, five vitellogenic follicles); the smallest measured 92.4 mm in SVL. Seven lizards were found on forest leaf litter. The other microhabitats used were vines, fallen logs, branches, and a crevice on a slope.     

Comparative aggression in Sceloporus virgatus, S. undulatus consobrinus, and S. u. tristichus (Sauria: iguanidae).

Aggressive behaviour in both sexes of Sceloporus virgatus, S. undulatus consobrinus, and S. u. tristichus were compared by introducing a conspecific to a resident lizard in the field. Males of S. u. consobrinus exhibited high intensity aggression more commonly than did males of the other forms. Of the females, S. u. tristichus showed the greatest propensity for aggressive behaviour; S. u. consobrinus showed the least. In males, degree of aggression was correlated positively with degree of sexual dichromatism. The high degree of aggression in male S. u. consobrinus may be selectively advantageous because of (1) low density increasing space between females, (2) low density reducing selection against a relatively high frequency of violent fighting, and (3) high predation favouring lizards that do not leave their sites upon intrusion of another male. High aggression in female S. u. tristichus may be selectively advantageous because of (1) higher density leading to reduced food supply and fewer egg-laying sites, and (2) lower predation reducing selection against mobility and fighting in females.     

Changes in oviducal vascularity during the reproductive cycle of three oviparous lizards (Eumeces obsoletus, Sceloporus undulatus and Crotaphytus collaris)

Histologically derived estimates and ink suspension vascular casts were used to examine oviducal vascular changes. Vascularity peaked during gravidity and was correlated with maximal plasma progesterone concentrations. The vascular increase in the oviducal tissue was attributed exclusively to increased capillary densities. The greatest change occurred in the anterior uterus where incubation and egg shell secretion occur. Similar patterns of change in vascularity occurred in the infundibulum, although not as extreme as that seen in the anterior uterus, whereas no significant alterations were noted in the posterior uterus. These modifications mimic the pattern of vascular change occurring in viviparous lizards during simple placentation. We suggest that major changes in uterine vascularity may not be required for the evolution of simple chorioallantoic placentae in lizards.     

Testosterone inhibits growth in juvenile male eastern fence lizards (Sceloporus undulatus): implications for energy allocation and sexual size dimorphism

In the eastern fence lizard, Sceloporus undulatus, female-larger sexual size dimorphism develops because yearling females grow faster than males before first reproduction. This sexual growth divergence coincides with maturational increases in male aggression, movement, and ventral coloration, all of which are influenced by the sex steroid testosterone (T). These observations suggest that male growth may be constrained by energetic costs of activity and implicate T as a physiological regulator of this potential trade-off. To test this hypothesis, we used surgical castration and subsequent administration of exogenous T to alter the physiological and behavioral phenotypes of field-active males during the period of sexual growth divergence. As predicted, T inhibited male growth, while castration promoted long-term growth. Males treated with T also exhibited increased daily activity period, movement, and home range area. Food consumption did not differ among male treatments or sexes, suggesting that the inhibitory effects of T on growth are mediated by patterns of energy allocation rather than acquisition. On the basis of estimates derived from published data, we conclude that the energetic cost of increased daily activity period following T manipulation is sufficient to explain most (79%) of the associated reduction in growth. Further, growth may have been constrained by additional energetic costs of increased ectoparasite load following T manipulation. Similar studies of the proximate behavioral, ecological, and physiological mechanisms involved in growth regulation should greatly improve our understanding of sexual size dimorphism.     

Larval nematodes (Ascarops sp., Spirurida, Spirocercidae) in liver granulomata of the western fence lizard, Sceloporus occidentalis (Iguanidae)

Prevalence of larval nematodes (Ascarops sp., Spirurida, Spirocercidae) and associated granulomata are reported from livers of wild populations of the western fence lizard, Sceloporus occidentalis. Granulomata were circumscribed by layers of fibrocytes. The encysted nematode was surrounded by masses of histiocytes, cellular debris and cells with pyknotic nuclei.     

Effects of natural habitat fragmentation on an endemic scrub lizard (Sceloporus woodi): an historical perspective based on a mitochondrial DNA gene genealogy

The Florida scrub lizard, Sceloporus woodi, is endemic to scrub habitat patches along the central portion of the Florida peninsula and xeric coastal regions. Scrub ecosystems are the patchily distributed remnants of previously widespread habitats formed during the Pleiocene and early Pleistocene. Scrub lizards appear to have limited dispersal capabilities due to high habitat specificity and low mobility. To assess the population structure and phylogeography of S. woodi, 135 samples were collected from 16 patches on five major ridges in Florida, USA. Analysis of 273 bp of mitochondrial DNA (mtDNA) cytochrome b reveals a very strong geographic distribution of genetic diversity. Haplotype frequencies are significantly different in 63 of 66 comparisons between patches. With one exception, samples from the five major ridges are characterized by fixed differences in haplotype distribution and deep evolutionary separations (3-10%). Fixed genetic differences were also observed between northern and southern segments of several ridges. Analysis of molecular variance (AMOVA) shows an estimated 10.4% total genetic variation within patches, 17.5% among patches (within ridges), and 72.1% among ridges. This strong population structure among patches within ridges indicates that the distribution of S. woodi is tightly linked to sandy scrub habitat and that the discontinuous distribution of scrub habitats significantly inhibits dispersal and gene flow. Phylogeographic analyses indicate a pattern of dispersal down the Florida peninsula during the late Pliocene-early Pleistocene, followed by habitat fragmentation and variant isolation events. Therefore, the deep genetic structuring among scrub lizard populations on separate ridges is attributed to ancient isolation events induced by a shift from dry (xeric) to wet (mesic) conditions on the Florida peninsula. These findings indicate that some scrub lizard populations have persisted in isolation for time frames in excess of 1 Myr, providing a case history on the genetic consequences of habitat fragmentation.     

Temporal germ cell development strategy during continuous spermatogenesis within the montane lizard, Sceloporus bicanthalis (Squamata; Phrynosomatidae)

Sceloporus bicanthalis is a viviparous lizard that lives at higher elevations in Mexico. Adult male S. bicanthalis were collected (n = 36) from the Nevado de Toluca, Mexico (elevation is 4200 m) during August to December, 2007 and January to July, 2008. Testes were extracted, fixed in Trumps, and dehydrated in a graded series of ethanol. Tissues were embedded, sectioned (2 μm), stained, and examined via a light microscope to determine the spermatogenic developmental strategy of S. bicanthalis. In all months examined, the testes were spermiogenically active; based on this, plus the presence of sperm in the lumina of seminiferous tubules, we inferred that S. bicanthalis had year-round or continuous spermatogenesis, unlike most reptiles that occupy a temperate or montane habitat. It was recently reported that seasonally breeding reptiles had a temporal germ cell development strategy similar to amphibians, where germ cells progress through spermatogenesis as a single population, which leads to a single spermiation event. This was much different than spatial development within the testis of other derived amniotes. We hypothesized that germ cell development was temporal in S. bicanthalis. Therefore, we wanted to determine whether reptiles that practice continuous spermatogenesis have a mammalian-like spatial germ cell development, which is different than the typical temperate reptile exhibiting a temporal development. In the present study, S. bicanthalis had a temporal development strategy, despite its continuous spermatogenic cycle, making them similar to tropical anoles.     

Locomotor performance of hatchling fence lizards (Sceloporus occidentalis): Quantitative genetics and morphometric correlates

Summary We examined heritabilities and correlations among measures of locomotor performance (speed, stamina) and among possible morphometric determinants of performance (hindlimb span, tail length) in families of hatchling lizards (Sceloporus occidentalis). We were particularly interested in determining whether these traits were heritable and thus might potentially respond genetically to selection. Moreover, we wished to determine whether speed and stamina are negatively genetically correlated, as suggested bya priori physiological and empirical considerations. All four traits appeared to be significantly heritable. Broadsense heritabilities were 0.33–0.36 for speed, 0.35–0.36 for stamina, 0.45–0.51 for hindlimb span, and 0.46–0.47 for tail length. Contrary to expectations, speed and stamina were not negatively genetically correlated. Hindlimb span and tail length, however, were negatively genetically correlated (but not phenotypically correlated). Hindlimb span and stamina were positively phenotypically correlated. Thus, for example, selection for longer hindlimb span could potentially result in shorter tails, contrary to evolutionary predictions based only on phenotypic correlations.