Yarrow's Spiny Research Articles

Brain transcriptomic responses of Yarrow's spiny lizard, Sceloporus jarrovii, to conspecific visual or chemical signals.

Species with multimodal communication integrate information from social cues in different modalities into behavioral responses that are mediated by changes in gene expression in the brain. Differences in patterns of gene expression between signal modalities may shed light on the neuromolecular mechanisms underlying multisensory processing. Here, we use RNA-Seq to analyze brain transcriptome responses to either chemical or visual social signals in a territorial lizard with multimodal communication. Using an intruder challenge paradigm, we exposed 18 wild-caught, adult, male Sceloporus jarrovii to either male conspecific scents (femoral gland secretions placed on a small pebble), the species-specific push-up display (a programmed robotic model), or a control (an unscented pebble). We conducted differential expression analysis with both a de novo S. jarrovii transcriptome assembly and the reference genome of a closely related species, Sceloporus undulatus. Despite some inter-individual variation, we found significant differences in gene expression in the brain across signal modalities and the control in both analyses. The most notable differences occurred between chemical and visual stimulus treatments, closely followed by visual stimulus versus the control. Altered expression profiles could explain documented aggression differences in the immediate behavioral response to conspecific signals from different sensory modalities. Shared differentially expressed genes between visually- or chemically-stimulated males are involved in neural activity and neurodevelopment and several other differentially expressed genes in stimulus-challenged males are involved in conserved signal-transduction pathways associated with the social stress response, aggression and the response to territory intruders across vertebrates.

Predator-prey interactions and venom composition in a high elevation lizard specialist, Crotalus pricei (Twin-spotted Rattlesnake)

The Twin-spotted Rattlesnake (Crotalus pricei) is a small lizard specialist restricted to higher montane habitat in the Sky Islands of Arizona and México. Though this species is restricted to high elevations and dispersal between mountaintops is impossible, few studies have investigated venom composition or the predator-prey relationship between C. p. pricei and its primary prey source, Yarrow's Spiny Lizard (Sceloporus jarrovii). Because of current isolation of populations in disjunct mountain ranges, it is possible that populations show local adaptation to prey and/or environmental conditions, as reflected by distinct venom phenotypes. Here we characterize venom composition of C. pricei from several different Sky Island mountain ranges and its relationship with S. jarrovii by using various analytical techniques and comparative toxicity tests. Results of venom analyses indicate that there is limited geographic variation in venom composition, occurring primarily in venoms of C. pricei from Durango, México, which had unusual PLA2 isoforms that are lacking from venoms of U.S. populations. Toxicity assays reveal that S. jarrovii has not developed resistance specific to C. p. pricei venom but does display a general tolerance to venom of several snakes in the genus Crotalus. These results provide insight into the evolutionary relationship between a lizard specialist and its natural prey, in addition to novel information on the venom composition of a little-studied species with a narrow range in the United States.

Support for the thermal coadaptation hypothesis from the growth rates of Sceloporus jarrovii lizards

The thermal coadaptation hypothesis posits that ectotherms thermoregulate behaviorally to maintain body temperatures (Tb) that maximize performance, such as net energy gain. Huey's (1982) energetics model describes how food availability and Tb interact to affect net energy gain. We tested the thermal coadaptation hypothesis and Huey's energetics model with growth rates of juvenile Yarrow's spiny lizards (Sceloporus jarrovii). We compared the preferred (selected) Tb range (Tsel) of lizards in high and low energy states to their optimal temperature (To) for growth over nine weeks, and determined whether the To for growth depended on food availability. We also measured the same lizards’ resting metabolic rate at five Tbs to test the energetics model assumptions that metabolic cost increases exponentially with Tb and does not differ between energy states. The Tsel of lizards on both diets overlapped with the To for growth. The assumptions of the energetics model were verified, but the To for net energy gain did not depend on food availability. Therefore, we found support for the thermal coadaptation hypothesis. We did not find support for the energetics model, but this may have been due to low statistical power.

Ontogenetic Variation in the Thermal Biology of Yarrow's Spiny Lizard, Sceloporus jarrovii.

Climate change is rapidly altering the way current species interact with their environment to satisfy life-history demands. In areas anticipated to experience extreme warming, rising temperatures are expected to diminish population growth, due either to environmental degradation, or the inability to tolerate novel temperature regimes. Determining how at risk ectotherms, and lizards in particular, are to changes in climate traditionally emphasizes the thermal ecology and thermal sensitivity of physiology of adult members of a population. In this study, we reveal ontogenetic differences in thermal physiological and ecological traits that have been used to anticipate how ectotherms will respond to climate change. We show that the thermal biological traits of juvenile Yarrow’s Spiny Lizards (Sceloporus jarrovii) differ from the published estimates of the same traits for adult lizards. Juvenile S. jarrovii differ in their optimal performance temperature, field field-active body temperature, and critical thermal temperatures compared to adult S. jarrovii. Within juvenile S. jarrovii, males and females exhibit differences in field-active body temperature and desiccation tolerance. Given the observed age- and sex-related variation in thermal physiology, we argue that not including physiological differences in thermal biology throughout ontogeny may lead to misinterpretation of patterns of ecological or evolutionary change due to climate warming. Further characterizing the potential for ontogenetic changes in thermal biology would be useful for a more precise and accurate estimation of the role of thermal physiology in mediating population persistence in warmer environments.

Differences in the thermal physiology of adult Yarrow's spiny lizards (Sceloporus jarrovii) in relation to sex and body size.

Sexual size dimorphism (SSD) is often assumed to reflect the phenotypic consequences of differential selection operating on each sex. Species that exhibit SSD may also show intersexual differences in other traits, including field-active body temperatures, preferred temperatures, and locomotor performance. For these traits, differences may be correlated with differences in body size or reflect sex-specific trait optima. Male and female Yarrow's spiny lizards, Sceloporus jarrovii, in a population in southeastern Arizona exhibit a difference in body temperature that is unrelated to variation in body size. The observed sexual variation in body temperature may reflect divergence in thermal physiology between the sexes. To test this hypothesis, we measured the preferred body temperatures of male and female lizards when recently fed and fasted. We also estimated the thermal sensitivity of stamina at seven body temperatures. Variation in these traits provided an opportunity to determine whether body size or sex-specific variation unrelated to size shaped their thermal physiology. Female lizards, but not males, preferred a lower body temperature when fasted, and this pattern was unrelated to body size. Larger individuals exhibited greater stamina, but we detected no significant effect of sex on the shape or height of the thermal performance curves. The thermal preference of males and females in a thermal gradient exceeded the optimal temperature for performance in both sexes. Our findings suggest that differences in thermal physiology are both sex- and size-based and that peak performance at low body temperatures may be adaptive given the reproductive cycles of this viviparous species. We consider the implications of our findings for the persistence of S. jarrovii and other montane ectotherms in the face of climate warming.

Diet of the Yarrow's Spiny Lizard Sceloporus jarrovii in the Central Chihuahuan Desert

We studied seasonal dietary patterns of Sceloporus jarrovii from a desert environment northwest of Gomez Palacio, Durango, Mexico. Stomach contents were examined (n = 82) and relative abundance and volume were determined. Formicids (ants) were the most abundant prey in all seasons. Other abundant foods were coleopterans (summer, winter) and isopterans (autumn, winter). Based on relative abundance in all seasons, S. jarrovii had a narrow breadth of diet, but relative volume of foods was broader. Overlap between sexes for relative abundance and volume was high throughout the year. However, low overlap in relative volume in spring indicated variation in diet between sexes. Three of the most common prey throughout the year varied significantly between sexes in length, width, and volume. However, volumes of the three most abundant foods were not correlated with snout–vent length of lizards.

Food consumption does not affect the preferred body temperature of Yarrow's spiny lizard ( Sceloporus jarrovi)

When animals consume less food, they must reduce their body temperature to maximize growth. However, high temperatures enhance locomotion and other performances that determine survival and reproduction. Therefore, thermoregulatory behaviors during different metabolic states reveal the relative importance of conserving energy and sustaining performance. Using artificial thermal gradients, we measured preferred body temperatures of male spiny lizards ( Sceloporus jarrovi) in fed and fasted states. Both the mean and maximal body temperatures (33° and 35 °C, respectively) were unaffected by metabolic state. This finding suggests that the benefits of foraging effectively, evading predators, and defending territory outweigh the energetic cost of a high body temperature during fasting.

Infection of Yarrow's Spiny Lizards (Sceloporus jarrovii) by Chiggers and Malaria in the Chiricahua Mountains, Arizona

Abstract We measured prevalence of malaria infection and prevalence and intensity of chigger infection in Yarrow's spiny lizards (Sceloporus jarrovii) from three sites in the Chiricahua Mountains of southeastern Arizona. Our primary objective was to compare parasite load among sites, sexes, and reproductive classes. We also compared our findings to those of previous studies on malaria and chiggers in S. jarrovii from the same area. Of lizards examined, 85 and 93% were infected by malaria and chiggers, respectively. Prevalence of malaria was two times higher than previously reported for the same area, while prevalence of chiggers was similar to previous findings. Intensity of chigger infection was variable among sites, but not among reproductive classes. The site with the highest intensity of chigger infection also had the most vegetative cover, suggesting that this habitat was more favorable for non-parasitic adult chiggers.

Testosterone stimulates the expression of a social color signal in Yarrow's Spiny Lizard, Sceloporus jarrovii

The sex steroid testosterone has been shown to regulate the development of male-specific coloration in many organisms that exhibit sexual dichromatism, but the role of testosterone is less certain for species in which both sexes express bright coloration. Lizards in the genus Sceloporus possess bright blue patches on their throats and abdomens. These patches, which are used in social signaling, are often regulated by testosterone and are consequently expressed only in males of most species. However, Yarrow's Spiny Lizard (Sceloporus jarrovii, Cope 1875) exhibits a derived condition in which both sexes express bright blue ventral patches despite dramatic sexual differences in circulating testosterone levels throughout postnatal ontogeny. In this study, we used surgical castration and hormone replacement in juvenile males to test the hypothesis that testosterone stimulates the expression of blue ventral coloration in S. jarrovii. In two separate experiments conducted in captivity and the natural field environment, we found that surgical castration decreased the hue and saturation while increasing the brightness of blue throat and abdominal patches. Castration also decreased the amount of black pigment bordering the blue throat patch. Treatment of castrated males with exogenous testosterone restored all aspects of ventral coloration to values similar to those of intact control males. Early organizational effects of testosterone during prenatal development may lead to the expression of blue coloration in both sexes, but the results of our present experiments indicate that subsequent effects of testosterone during sexual maturation further enhance the coloration of males.

Demography of the Yarrow's Spiny Lizard, Sceloporus jarrovii, from the Central Chihuahuan Desert

The demography of a population of Yarrow's spiny lizard, Sceloporus jarrovii, was examined from 2004 to 2006 in the canyon Las Piedras Encimadas, located in Gomez Palacio, Durango, México. Lizards were studied using a mark-recapture technique. Reproduction in females occurred between November and May, coinciding with dry conditions. Reproductive activity was highest (percent of females with vitellogenic follicles or embryos) in the middle of the dry season (November and December). Thirteen percent of females reached sexual maturity at an average age of 8.5 months. The population structure was similar in spring and fall, but not in summer. A notable feature of summer, coinciding with the wet season, was the greater number of hatchlings and juveniles. The overall sex ratio did not differ from 1:1. The density of adults varied from 12 to 62 animals ·0.5 ha−1. Temperate and arid-adapted populations of S. jarrovii exhibited broad similarity in timing of the reproductive season, whereas factors such as density, growth, age at sexual maturity, and survivorship differed.

A test of the reproductive cost hypothesis for sexual size dimorphism in Yarrow's spiny lizard Sceloporus jarrovii

1. Trade-offs between reproduction and growth are central assumptions of life-history theory, but their implications for sexual size dimorphism (SSD) are poorly understood. 2. Adult male Yarrow's spiny lizards Sceloporus jarrovii average 10% larger than adult females. In a low-altitude (1700 m) population, this SSD develops because males grow more quickly than females during the first year of life, particularly during the first female reproductive season. This study tests the hypothesis that SSD develops because female growth is constrained by energetic costs of reproduction. 3. To test for a growth cost of reproduction, I compared growth rates of free-living females that differed, either naturally or experimentally, in reproductive status. Females that naturally delayed reproduction until their second year grew more quickly than females that reproduced as yearlings, and ovariectomized yearlings grew more quickly and to larger sizes than reproductive controls. 4. To determine whether SSD develops in the absence of this inferred reproductive cost, I also studied a high-altitude (2500 m) population in which all females delay reproduction until their second year. Sex differences in growth trajectories were similar to those observed at low altitude, such that males averaged 10% larger than females even prior to female reproduction. 5. Although female growth may be constrained by reproduction, multiple lines of evidence indicate that this cost is insufficient to explain the full magnitude of SSD in S. jarrovii. First, differences in growth of reproductive and nonreproductive females are not observed until the final month of gestation, by which time SSD is already well developed. Second, the growth benefit accruing from experimental inhibition of reproduction accounts for only 32% of the natural sex difference in body size. Finally, SSD develops well in advance of female reproduction in a high-altitude population with delayed maturation.

Environmental sensitivity of sexual size dimorphism: laboratory common garden removes effects of sex and castration on lizard growth

Summary Adult males average 10% larger than females in natural populations of Yarrow's Spiny Lizard (Sceloporus jarrovii). In two previous studies of free‐living animals, we found that (1) this sexual size dimorphism (SSD) develops because yearling males grow more quickly than females and (2) the sex steroid testosterone (T) may regulate this sex difference in growth: castrated males (CAST) grow more slowly than either intact control males (CON) or castrated males treated with exogenous T (TEST). In the present study, we tested the environmental sensitivity of these sex and treatment effects on growth by raising captive males (CAST, CON, TEST) and females under identical ‘common garden’ conditions. Sex and treatment effects on growth rate were absent in captivity. The development of SSD was suppressed because captive males grew more slowly than free‐living males of equal size, while experimental treatments failed to affect male growth because CAST grew more quickly in the laboratory common garden than in the field. Individual growth rates were strongly related to food consumption, but feeding rate did not differ between sexes or among male treatments. Our results call attention to the environmental sensitivity of sex‐specific endocrine growth regulation and illustrate the importance of combining laboratory and field studies of growth and SSD.

Responses of Kit Foxes (Vulpes macrotis) to Antipredator Blood-Squirting and Blood of Texas Horned Lizards (Phrynosoma cornutum)

Six related studies were conducted with four captive juvenile Kit Foxes (Vulpes macrotis) to test the hypothesis that blood-squirting from eye-socket tissues by Texas Horned Lizards (Phrynosoma cornutum) is a canid antipredator defense. In 16 trials, naive “hungry” foxes killed and ate adult Yarrow's Spiny Lizards (Sceloporus jarrovii; eight of eight trials) slightly more frequently than adult P. cornutum (six of eight trials). Adverse responses by foxes (head shaking) were seen in five of six trials in which Phrynosoma squirted blood. Later these experienced foxes, fed ad libitum, killed and ate mice (eight of eight trials) while largely ignoring P. cornutum (one killed and eaten in eight trials), suggesting a learned aversion to horned lizards as prey. During attacks on mice smeared with horned-lizard blood, foxes displayed behaviors typical of predatory encounters with horned lizard prey (head shaking and prey tearing). These prey-handling behaviors were in striking contrast to those elicited by untreated mice and by mice treated with mouse blood, demonstrating that horned-lizard blood (and its chemical constituents) altered normal behaviors toward mouse prey. Prey-handling times for mice treated with horned lizard blood were significantly longer than mouse-only treatments. Responses of foxes to mice coated with horned lizard Harderian- and lacrimal-gland tissues coupled with responses to mice coated with systemic horned-lizard blood, mouse blood, and untreated mice suggest that (1) no defensive chemicals are added to the blood by orbital glands before blood ejection, and (2) active antipredator chemicals are carried in the circulating blood as well as in squirted blood. In four trials, foxes attacked “de-horned” horned lizards; a role for cranial horns in facilitating predator hesitancy prior to blood squirting is proposed. Evidence is presented that horned lizards visually identify and categorize foxes as appropriate predators for a blood-squirting defense. We conclude that, in many predator-prey encounters with wild canids, blood-squirting by Texas Horned Lizards is an effective chemical defense. We propose a scenario for the evolution of this unique defense and suggest that the defensive compounds found in the blood may be sequestered from the seed-harvester ant prey of horned lizards.

NOCTURNAL ACTIVITY BY DIURNAL LIZARDS (SCELOPORUS JARROVI, S. VIRGATUS) EATEN BY SMALL OWLS (GLAUCIDIUM GNOMA, OTUS TRICHOPSIS)

Whiskered screech-owls (Otus trichopsis) and northern pygmy-owls (Glaucidium gnoma) delivered freshly caught Yarrow's spiny lizards (Sceloporus jarrovi) and striped plateau lizards (S. virgatus) to nestlings from dusk to dark in southeastern Arizona. This observation stimulated studies of the prey deliveries by the owls and lizard activity patterns, because the lizards are not known to be nocturnal. Lizards were more frequent prey of both owls than endothermic vertebrates but infrequent compared to arthropods, a pattern in the pygmy-owl that differs from its northern populations. Yarrow's spiny lizard, the most abundant and frequently captured lizard, was most active in the morning but also active in the evening. Striped plateau lizard, the second most abundant and depredated species, had morning and evening peaks of activity. Few lizards, including S. clarki and Urosaurus ornatus, but not Cnemidophorus exsanguis and C. sonorae, were active at or after dark, when relatively few were captured by the owls.

Molecular Phylogenetics and Evolution of Sexual Dichromatism among Populations of the Yarrow's Spiny Lizard (Sceloporus jarrovii)

Molecular Phylogenetics and Evolution of Sexual Dichromatism among Populations of the Yarrow's Spiny Lizard (Sceloporus jarrovii)

MOLECULAR PHYLOGENETICS AND EVOLUTION OF SEXUAL DICHROMATISM AMONG POPULATIONS OF THE YARROW'S SPINY LIZARD (SCELOPORUS JARROVII).

Understanding evolution of geographic variation in sexually dimorphic traits is critical for understanding the role that sexual selection may play in speciation. We performed a phylogenetic analysis of geographic variation in sexual dichromatism in the Yarrow's spiny lizard (Sceloporus jarrovii), a taxon that exhibits remarkable diversity in male coloration among populations (e.g., black, red, green, yellow, blue, brown). An mtDNA phylogeny based on approximately 880 bp from the 12S ribosomal RNA gene and 890 bp from the ND4 gene was reconstructed for 30 populations of S. jarrovii and eight other species of the torquatus species group using maximum-likelihood and parsimony methods. The phylogeny suggests that S. jarrovii consists of at least five evolutionary species, none of which are sister taxa. Although intraspecific diversity in male coloration is less than indicated by previous taxonomy, two species formerly referred to as S. jarrovii exhibit impressive geographic variation in sexual dichromatism. In one of these species, the phylogeny shows the independent evolution of a distinctive blue color morph in different parts of the species range. This pattern suggests that sexual selection may lead to striking phenotypic divergence among conspecific populations and striking convergence. Results also demonstrate the importance of a phylogenetic perspective in studies of evolutionary processes within nominal species and the problematic nature of "polytypic" species recognized under the biological species concept.

Gastrointestinal Helminths of Yarrow's Spiny Lizard, Sceloporus jarrovii (Phrynosomatidae) in Mexico

-Three-hundred sixty-one Sceloporus jarrovii from 16 states in Mexico were examined for gastrointestinal helminths. Two species of cestodes, Oochoristica scelopori and Mesocestoides sp.; 14 species of nematodes, Abbreviata terrapenis, Macdonaldius grassi, Physaloptera retusa, Piratuba prolifica, Scatonema wulkeri, Skrjabinoptera phrynosoma, Spauligodon giganticus, Strongyluris similis, Thubunaea iguanae, Thubunaea intestinalis, Ascarops sp., Gongylonema sp., Mermis sp., Physocephalus sp. and one species of acanthocephalan, Centrorhynchus sp., were found. With the exception of Abbreviata terrapenis and Thubunaea intestinalis, these helminths have been found in other lizards. Throughout the range of S. jarrovii in Mexico, the predominant monoxenous (direct life cycle) helminth was Spauligodon giganticus (prevalence 68%); the predominant heteroxenous (indirect life cycle) helminth was Physaloptera retusa (prevalence 27%). Sceloporus jarrovii is a new host record for Macdonaldius grassi, Piratuba prolifica, Skrjabinoptera phrynosoma, Thubunaea iguanae, Ascarops sp., Gongylonema sp., Physocephalus sp. and Centrorhynchus sp.

Prevalence of ectoparasite infestation in neonate Yarrow's spiny lizards, Sceloporus jarrovii (Phrynosomatidae), from Arizona

Prevalence of ectoparasite infestation in neonate Yarrow's spiny lizards, Sceloporus jarrovii (Phrynosomatidae), from Arizona

Ectoparasite-induced lesions in mite pockets of the Yarrow's spiny lizard, Sceloporus jarrovii (Phrynosomatidae).

Histopathological effects of the chigger, Eutrombicula lipovskyana, on the mite pockets of neonatal, juvenile and adult Yarrow's spiny lizard, Sceloporus jarrovii, were investigated. Focal ulcerative dermatitis was noted in all age classes. This reaction was more diffuse in older animals in which penetration as deep as the panniculus occurred. Based on the occurrence of inflammatory reactions in neonatal lizards, S. jarrovii appears capable of recognizing foreign antigens shortly after birth. There was an increased inflammatory response in older lizards that may have been an augmented host sensitivity following repeated exposure to chiggers. Granulomas, which were interpreted as an attempt to isolate the effects of chigger bites, were noted in juveniles and adults. We propose that S. jarrovii does not develop resistance after repeated exposures to E. lipovskyana.

Lizard homing behavior: the role of the parietal eye during displacement and radio-tracking, and time-compensated celestial orientation in the lizard Sceloporus jarrovi

The role of the parietal eye was investigated in Yarrow's spiny lizard, Sceloporus jarrovi. Three groups of lizards were displaced approximately 150 m from previously determined home ranges: (1) normal lizards, (2) sham-treated lizards (paint placed alongside the parietal eye), and (3) experimental lizards (parietal eye covered with a layer of paint). Significantly fewer experimental lizards returned home (20%) than either the normal (61%) or sham-treated lizards (57%). Control studies indicated that the parietal eye treatment did not affect the daily activity patterns, home range size, or survivorship of the lizards. Radio-tracking of displaced S. jarrovi showed that $$\raise.5ex\hbox{$\scriptstyle 1$}\kern-.1em/ \kern-.15em\lower.25ex\hbox{$\scriptstyle 2$} $$ h after displacement, normal and sham-treated lizards moved in homeward pathways that were significantly non-random. Experimental lizards, however, were not significantly oriented, either $$\raise.5ex\hbox{$\scriptstyle 1$}\kern-.1em/ \kern-.15em\lower.25ex\hbox{$\scriptstyle 2$} $$ or 3 $$\raise.5ex\hbox{$\scriptstyle 1$}\kern-.1em/ \kern-.15em\lower.25ex\hbox{$\scriptstyle 2$} $$ h later, and all moved in random directions after their release. The use of celestial cues for homing orientation was also examined. One group of lizards was maintained on a natural light-dark cycle (no phase-shift:NPS) while a second group was subjected to a 6-h advanced phase-shift (APS). All lizards were released in the field approximately 150m from their home ranges and radio-tracked. The NPL lizards were oriented towards home 30 min after release while the APS lizards shifted their orientation in a counterclockwise direction. Both NPS and APS lizards improved their orientation after 3 h.