Species Of Whiptail Lizards Research Articles

Patterns of diet composition of a whiptail lizard species conforms to the Shared Preferences Model of interindividual variation in prey consumption

Abstract We analysed the interindividual variation in diet, patterns of food resource use and topology of the trophic networks of juvenile, male, and female Ameivula ocellifera (Spix, 1825) during one year, covering wet and dry seasons. Using a network-based approach, we evaluated the degree of variation in the diet of individuals, and the degree of nestedness and clustering to identify patterns of resource use and the topology of individuals food webs. We found a high degree of interindividual variation in the diet of juveniles, males, and females during the study period, which seems to be related to nested patterns of resource use of males and females. These results also suggest that males and females seem to have both generalist and specialist individuals, of which the diets of specialists are nested within the diets of generalists. For juveniles, we found evidence of interindividual variation in diet in both seasons, although patterns of food resource partition that may cause it could not be identified. Insect larvae of several groups were the main food resource in all three lizard groups during the wet season, while termites were the dominant food item during the dry season. Our results conform to the Shared Preferences Model where individuals should consume the same top-ranked prey when they are abundant in the environment, replacing it with suboptimal items as preferred ones become scarce.

The Second Known Tetraploid Species of Parthenogenetic Tetrapod (Reptilia: Squamata: Teiidae): Description, Reproduction, Comparisons With Ancestral Taxa, And Origins Of Multiple Clones

We describe the second known tetraploid amniote that reproduces by parthenogenetic cloning. This all-female species of whiptail lizard originated in the laboratory from hybridization between Aspidoscelis uniparens (triploid parthenogen) and Aspidoscelis inornatus (diploid bisexual species). Similar clonal lineages of tetraploids arose from at least 44 F1 hybrid females. These were produced by at least 15 A. uniparens that mated with several different males of A. inornatus from both New Mexico and Arizona stock.Inheritance of alleles at eight microsatellite deoxyribonucleic acid (msDNA) loci in the tetraploid species confirms its parentage, whereas DNA quantification and behavior of chromosomes in meiosis demonstrate that tetraploidy and heterozygosity are maintained generation after generation.We compared univariate and multivariate variation in scalation between the tetraploids, their parental taxa, and four museum specimens from New Mexico that were reported as putative hybrids. Two of the putative hybrids are confirmed as such, but the other two are A. inornatus. The similarities of A. uniparens and the tetraploids suggest that tetraploid females may exist in old samples misidentified as A. uniparens. Clones of the tetraploid species are so similar to each other in morphology and msDNA that we have been unable to distinguish most individuals or separate lineages from the P1 through multiple generations (up to F7) on the basis of the 12 msDNA loci analyzed in this study.We discuss taxonomic aspects of the multiple hybrid origins of similar clones and apply one specific name. For some systematists, depending on the species concept preferred, these lizards represent a complex of multiple cryptic species that cannot be reliably identified or diagnosed (one species for each F1 hybrid female that cloned a lineage). These specimens of known parentage provide valuable insights for taxonomic treatment of natural parthenogenetic clones. In addition, we show that the degree of morphological variation in clonal parthenogens and bisexual A. inornatus can be similar to each other.

Widespread failure to complete meiosis does not impair fecundity in parthenogenetic whiptail lizards.

Parthenogenetic species of whiptail lizards in the genus Aspidoscelis constitute a striking example of speciation by hybridization, in which first-generation hybrids instantly attain reproductive isolation and procreate as clonal all-female lineages. Production of eggs containing a full complement of chromosomes in the absence of fertilization involves genome duplication prior to the meiotic divisions. In these pseudo-tetraploid oocytes, pairing and recombination occur exclusively between identical chromosomes instead of homologs; a deviation from the normal meiotic program that maintains heterozygosity. Whether pseudo-tetraploid cells arise early in germ cell development or just prior to meiosis has remained unclear. We now show that in the obligate parthenogenetic species A. neomexicana the vast majority of oocytes enter meiosis as diploid cells. Telomere bouquet formation is normal, but synapsis fails and oocytes accumulate in large numbers at the pairing stage. Pseudo-tetraploid cells are exceedingly rare in early meiotic prophase, but they are the only cells that progress into diplotene. Despite the widespread failure to increase ploidy prior to entering meiosis, the fecundity of parthenogenetic A. neomexicana is similar to that of A. inornata, one of its bisexual ancestors.

Extreme variant of the triploid parthenogenetic lizardAspidoscelis exsanguis(Squamata: Teiidae) from New Mexico

Abstract Parthenogenetic reproduction in several all-female species of whiptail lizards (genus Aspidoscelis) does not preclude the occasional production of extreme variants. An adult lizard with a unique combination of dorsal color pattern, scutellation, and meristic characters captured 20 August 2013 approximately 200 m east of the Rio Grande in Bosque Farms, Valencia County, New Mexico, was inferred to be an extreme variant of triploid, hybrid-derived Aspidoscelis exsanguis which was also observed near the point of capture. There was no basis for identifying the specimen as a tetraploid hybrid because morphology did not reflect that origin and no gonochoristic species (e.g., Aspidoscelis marmorata or Aspidoscelis inornata) was known to occur at the site. Morphological analyses also ruled out the possibility that it could be an extreme variant of diploid parthenogenetic Aspidoscelis neomexicana, which is syntopic with A. exsanguis in Bosque Farms.

Gastrointestinal Helminths from Eight Species ofAspidoscelis(Squamata: Teiidae) from Mexico

Seventy-four representatives of 8 species of whiptail lizards (Aspidoscelis ssp.), from Mexico were examined for helminths: Aspidoscelis calidipes (n = 8), A. communis (n = 10), A. cozumelae (n = 9), A. gularis (n = 10), A. lineattissima (n = 9), A. motaguae (n = 11), A. parvisocia (n = 9), and A. sackii (n = 8). We found one species of Cestoda, Oochoristica scelopori, and 7 species of Nematoda, including Abbreviata terrapenis, Parapharyngodon alvarengai, Pharyngodon warneri, Spauligodon garciaprietoi, Spinicauda spinicauda, Thubunaea cnemidophorus, and Physaloptera sp. Mean helminth diversity per lizard species was 3.1 (SD 1.8). Spauligodon garciaprietoi was present in 6 of 8 (75%) of the lizard species. The specimens we examined were infected by an aggregate of helminths that were either characteristic of Aspidoscelis spp. from the United States (North America: O. scelopori, T. cnemidophorus, A. terrapenis, P. warneri) or characteristic of Aspidoscelis spp. from Mexico (Mesoamerica: S. garciaprietoi, P. alvarengai, S. spinicauda). Twentytwo new host records are reported.

Comparative Meristic Variability in Whiptail Lizards (Teiidae,Aspidoscelis): Samples of ParthenogeneticA. tesselataVersus Samples of Sexually ReproducingA. sexlineata, A. marmorata, andA. gularis septemvittata

ABSTRACT Is it correct, as is often assumed, that the clonal form of inheritance in parthenogenetic lizards results in less variability than occurs with genetic recombination in their sexually reproducing (gonochoristic) relatives? We tested this hypothesis by comparing morphological variability in samples of parthenogenetic Aspidoscelis tesselata and several gonochoristic species of whiptail lizards. To control for environmental factors that might differentially affect embryonic development of morphological characters, we compared samples obtained from the same or geographically adjacent localities. In addition, we compared apparently “uniclonal” and multiclonal samples from each of two color-pattern classes (C and E) of A. tesselata. For univariate meristic characters, parthenogenetic A. tesselata matched the variability of a sympatric gonochoristic species in 11 of 20 comparisons, had lower variability in six comparisons, and was more variable in three. For multivariate characters derived from principa...

Laboratory synthesis of an independently reproducing vertebrate species

Speciation in animals commonly involves an extrinsic barrier to genetic exchange followed by the accumulation of sufficient genetic variation to impede subsequent productive interbreeding. All-female species of whiptail lizards, which originated by interspecific hybridization between sexual progenitors, are an exception to this rule. Here, the arising species instantaneously acquires a novel genotype combining distinctive alleles from two different species, and reproduction by parthenogenesis constitutes an effective intrinsic barrier to genetic exchange. Fertilization of diploid parthenogenetic females by males of sexual species has produced several triploid species, but these instantaneous speciation events have neither been observed in nature nor have they been reconstituted in the laboratory. Here we report the generation of four self-sustaining clonal lineages of a tetraploid species resulting from fertilization of triploid oocytes from a parthenogenetic Aspidoscelis exsanguis with haploid sperm from Aspidoscelis inornata. Molecular and cytological analysis confirmed the genetic identity of the hybrids and revealed that the females retain the capability of parthenogenetic reproduction characteristic of their triploid mothers. The tetraploid females have established self-perpetuating clonal lineages which are now in the third generation. Our results confirm the hypothesis that secondary hybridization events can lead to asexual lineages of increased ploidy when favorable combinations of parental genomes are assembled. We anticipate that these animals will be a critical tool in understanding the mechanisms underlying the origin and subsequent evolution of asexual amniotes.

Two New Species of Cnemidophorus (Squamata: Teiidae) from Islands of the Northeastern Coast of Venezuela

We describe two new whiptail lizard species, previously assigned to Cnemidophorus lemniscatus, from islands of the state of Nueva Esparta and Los Frailes Archipelago, off the northeastern coast of Venezuela. The two new species differ from C. lemniscatus in color, pattern, and squamation. The species from the islands of Margarita and Cubagua can be distinguished from the one of Los Frailes Archipelago in having the circumorbital semicircles extending further anteriorly, more scales between supraocular and supraciliaries, and a larger number of scales of a smaller size between the preanal shield and anal spurs. The two new species also differ conspicuously in color and pattern of both sexes and all age classes. Additionally, we comment on the status of the population of Cnemidophorus of Los Testigos Archipelago, discuss the morphological and color variation observed in C. lemniscatus from northern Venezuela and restrict the distribution of the latter species in the country to the mainland.

Parthenogenetic Aspidoscelis neomexicana (Sauria: Teiidae) and Syntopic Congeners in Presidio County, Texas

Abstract Studies of distributional ecology of whiptail lizards near the Rio Grande in Presidio County, Texas, have resulted in discovery of Aspidoscelis neomexicana at three of >20 sites investigated. Records of A. neomexicana in Presidio County are >225 km southeast of sites inhabited by the species in El Paso, El Paso County. Observations made during 1988–2008 indicate that A. neomexicana in Presidio County inhabits only a few areas of floodplain where there is intermingling of several microhabitats characterized by loamy, gravelly alluvium with various combinations of trees, shrubs, Russian thistle (Salsola kali), Spanish dagger (Yucca torreyi), cacti, grasses, and forbs. Each species of whiptail lizard (i.e., A. exsanguis, A. tesselata, and A. tigris) that is syntopic with A. neomexicana is widely distributed in Presidio County and elsewhere in the United States and Mexico. Despite range maps to the contrary, A. neomexicana has not been recorded in Mexico; forays in 1993 to San Antonio, Chihuahua, acr...

PHYLOGEOGRAPHY AND GENETIC STRUCTURE IN THE CNEMIDOPHORUS LONGICAUDA COMPLEX (SQUAMATA, TEIIDAE)

Cnemidophorus longicauda is a poorly-studied species of whiptail lizard distributed in the Monte Desert region of Argentina. Some variation in dorsal color pattern has been observed between northern and southern populations along the latitudinal range of the species. Recently, a new species of Cnemidophorus (C. tergolaevigatus) previously considered as C. longicauda has been described, although no comparative morphological study has been conducted. In this study we use the mitochondrial ND4 gene region to examine the phylogeography and genetic structure of this species complex. Phylogenetic reconstruction, Nested Clade Phylogeographic Analysis, and AMOVA reveal deep genetic divergence between northern and southern populations that are geographically separated by the Famatina-Sanogasta Mountains. Because most of the localities of C. tergolaevigatus are from the general region of the ''northern group'' recovered in this study, there is general concordance between geographic patterns of mtDNA and morphological (color pattern) variation, and thus support for the recognition of this species. We discuss this genetic break and the phylogenetic/phylogeographic history of the Cnemidophorus in the context of other lizard species with similar distributions, and the implications for understanding the evolutionary history of the temperate South American biota.

The nitric oxide synthase inhibitor l-NAME suppresses androgen-induced male-like pseudocopulatory behavior in whiptail lizards

The synthesis of nitric oxide by the enzyme nitric oxide synthase (NOS) is involved in the androgen-dependent gating of male-typical copulatory behavior, both centrally, particularly in the preoptic area, and peripherally, notably through its role in penile erection. In the all-female whiptail lizard species Cnemidophorus uniparens, individuals display copulatory behaviors indistinguishable from males of similar species if gonadectomized and treated with testosterone. In this experiment, androgenized individuals were treated with a NOS inhibitor, which eliminated male-like behavior in half the individuals, suggesting that the central role of nitric oxide synthesis is conserved in this species. The deficit was principally in mounting, suggesting that sexual motivational systems were affected, rather than consummatory mechanisms.

A new species of Cnemidophorus (Squamata: Teiidae) from western Argentina

AbstractA new species of whiptail lizard of the genus Cnemidophorus (Teiidae) is described from La Rioja province, western Argentina. The species is characterized by a broad light brown-grayish middorsal pattern, the lack of vertebral and paravertebral stripes, alternating white and brown stripes from dorsolateral to flanks, pointed snout, postnasal scale usually longer than loreal scale, and 10 longitudinal rows of ventral scales. The previous and current states of knowledge on southern South American Cnemidophorus species are discussed.

Sex differences in estrogen-induced progesterone and estrogen receptor mRNA in the ventromedial hypothalamus of hatchling whiptail lizards

The ventromedial hypothalamus (VMH) is an important neural locus for the control of female-typical sexual behavior in vertebrates, and exogenous estrogen stimulates a strong increase in progesterone receptor (PR) in the VMH of adult females. Estrogen also regulates its own receptor (ER), though the direction of the response varies from species to species. In rodents and whiptail lizards, males either lack estrogen regulation of PR and ER mRNA in the VMH or display a greatly attenuated response. We examined hatchlings of two closely related species of whiptail lizards, one of which is parthenogenetic. Though normally all female, the parthenogens can be made to develop as gonadal males by treating with aromatase inhibitor early in development. Thus, we were able to ask whether the brain sex of these ‘created male’ parthenogens corresponded to their gonadal sex or their genetic sex. We injected 1- and 30-day-old animals of both species and sexes with estradiol benzoate (EB) and assayed for PR and ER mRNA using in situ hybridization. All animals given EB responded with a strong increase in PR mRNA in the VMH. However, females of the sexual species had higher EB-induced PR mRNA levels than did conspecific males; there was no sex difference between the normal parthenogens and the created males of the parthenogenetic species. EB also stimulated an increase in ER mRNA in the VMH, but the pattern of response was more complex. Normal parthenogens did not increase ER mRNA in response to EB in either age group, in contrast to the strong response of 1-day-old males and females of the sexual species and 30-day-old created males. The results indicate that hatchling whiptails show striking species and sexual differences in the regulation of sex steroid receptor mRNAs in an area of the brain important for adult sexual behavior. This variation may play a role in the development of species and sexual differences in the adult neuroendocrine phenotype.

Differential effects of testosterone and progesterone on the activation and retention of courtship behavior in sexual and parthenogenetic whiptail lizards

Both testosterone (T) and progesterone (P) facilitate the expression of male-typical sexual behavior in a variety of animals, including rodents and lizards. In two species of whiptail lizards, Cnemidophorus inornatus and C. uniparens, both hormones elicit the full repertoire of courtship behavior. However, the relative efficacy of the two hormones is unknown. In Experiments 1 and 2 we assessed differences in capacity of exogenous T and P to induce male-typical courtship behavior in gonadectomized whiptail lizards. In both species, individuals implanted with T showed more frequent courtship behavior relative to those implanted with P or cholesterol. In Experiments 3 and 4 we examined whether T and P differentially affected the retention of courtship behavior following implant removal. In both species, individuals implanted with T showed more courtship behavior following implant removal than those previously given P. In these experiments, implants were removed at a time when individuals in both groups were behaviorally similar; therefore, the differences in behavior following implant removal were not due to differences in the amount of courtship experience. Taken together, the hormone that was more effective at activating courtship behavior was also more effective at maintaining courtship behavior following implant removal. In summary, though both T and P can elicit identical sexual behaviors in both whiptail species, T has a greater and more lasting effect on courtship behavior and possibly on the neural circuits underlying courtship behavior.

Androgenic regulation of steroid hormone receptor mRNAs in the brain of whiptail lizards.

Sex and species differences in androgenic regulation of steroid hormone receptor mRNAs were examined in the diencephalon of two species of whiptail lizards: Cnemidophorus inornatus is a sexual species and the direct evolutionary ancestor to Cnemidophorus uniparens, an all-female parthenogenetic species. Lizards were gonadectomized and treated with different doses of either aromatizable testosterone or nonaromatizable dihydrotestosterone. The relative abundances of androgen-, oestrogen-, and progesterone-receptor mRNAs were compared in various nuclei following in situ hybridization with homologous riboprobes. A diversity of patterns in androgenic regulation was observed, with effects differing according to brain region, the steroid-receptor mRNA being considered and, in some cases, between androgens. In the ancestral sexual species, intact males had lower androgen-receptor mRNA abundances than castrated, blank-implanted males in the medial preoptic area. Testosterone significantly decreased androgen-receptor mRNA abundance in the medial preoptic area of castrated males. Males had higher androgen-receptor mRNA levels in the preoptic area than females generally and neither the sexual or parthenogenetic females showed a decrease in androgen-receptor mRNA with androgen treatment. Both testosterone and dihydrotestosterone increased oestrogen-receptor mRNA abundance in the ventromedial hypothalamus of C. inornatus, but no sex differences in this effect were observed. Gonadectomy decreased, whereas androgen treatment increased, progesterone-receptor mRNA abundance in the ventromedial hypothalamus. There was a sex difference in this response to androgen in the sexual species, with males having greater amounts than females in this brain area. The parthenogenetic species exhibited a similar pattern to females of the sexual species, but the levels were higher overall, possibly because Cnemidophorus uniparens is triploid. The periventricular preoptic area showed a different pattern, with testosterone treatment increasing progesterone-receptor mRNA abundance in both sexes of the sexual species and in the parthenogenetic species, while dihydrotestosterone did not. The diversity of patterns in androgen effects indicates that gonadal sex, aromatization of androgen, and perhaps gene dosage all influence the expression of steroid-receptor mRNAs in the lizard brain.

Progesterone Inhibits Female-Typical Receptive Behavior and Decreases Hypothalamic Estrogen and Progesterone Receptor Messenger Ribonucleic Acid Levels in Whiptail Lizards (GenusCnemidophorus)

Female-typical sexual behavior in tetrapods is mediated primarily by estrogen and progesterone acting through intracellular receptors at specific sites in the mediobasal hypothalamus. Progesterone exerts both faciliatory and inhibitory actions on female sexual behavior and in well-studied rodent models, the inhibitory actions are exerted through downregulation of progesterone and estrogen receptors. This study examined progesterone effects on both female-typical sexual behavior and hypothalamic estrogen and progesterone receptor mRNA expression (ER- and PR-mRNA) in a sexual and parthenogenetic species of whiptail lizard. Progesterone capsules administered to ovariectomized femaleCnemidophorus inornatusandCnemidophorus uniparensfollowing a receptivity-inducing dosage of estradiol benzoate (EB) strongly inhibited receptive behavior as compared to blank implanted controls. Progesterone capsules administered either before or after an EB injection also strongly downregulated ER- and PR-mRNA abundance in the ventromedial nucleus of the hypothalamus relative to blank implanted controls. The correlated decrease in both EB-induced receptive behavior and ER- and PR-mRNAs following progesterone administration are similar to findings in rats and guinea pigs, suggesting that this is an evolutionarily conserved mechanism in the regulation of female sexual behavior.

Making Males from Females: The Effects of Aromatase Inhibitors on a Parthenogenetic Species of Whiptail Lizard

The parthenogenetic whiptail lizard Cnemidophorus uniparens provides a good model for the study of sex determination and sexual differentation because genetic variation is minimal and all unmanipulated embryos will develop as females. Thus any deviation from the established course of development can be identified as a treatment effect. Previous work has shown that early prenatal treatment with CGSI6949A, a nonsteroidal aromatase inhibitor, causes hatchlings to develop as males. The present study explores more fully the effects of dosage and timing of application of CGS16949A and examines the sex-reversing potential of CGS20267, a new and reputedly more potent aromatase inhibitor. Eggs were treated with a range of dosages of the aromatase inhibitors. Hatchlings that received 1 μg or more of either inhibitor were all male, while those that received 0.1 μg or less were all female. No difference in potency between the two compounds was detected. Animals treated with 100 μg of CGS16949A on Day 20 of incubation or later were all female, while those treated on Day 5 were all male. Seven sex-reversed male parthenogens have been raised to sexual maturity. The animals appear similar morphologically and behaviorally to males of the sexually reproducing whiptail species. Spermatogenesis and spermiogenesis have been confirmed by histological examination of the testes and by postcopulatory cloacal swabs. Application of aromatase inhibitors has been shown to sex-reverse both avian and reptilian species. In mammals, the male determining gene of the Y chromosome (SRY) may code for an intrinsic aromatase inhibitor. Studies show the gene's product has a binding domain which recognizes regulatory elements in the promoter of the aromatase gene. These results suggest that the superficially different sex-determining processes of many amniotes may have underlying mechanisms in common.

Species differences in estrogen receptor and progesterone receptor-mRNA expression in the brain of sexual and unisexual whiptail lizards.

Circulating concentrations of gonadal steroid hormones and reproductive behavior in female vertebrates vary as a function of ovarian state. Steroids secreted by the ovary, specifically estrogen and progesterone, influence the expression of behaviors associated with reproduction by intracellular sex steroid receptors located in specific regions of the brain. Using in situ hybridization, we analyzed estrogen receptor and progesterone receptor messenger RNA expression in several brain regions of ovariectomized, vitellogenic, and postovulatory individuals from two species of whiptail lizards (Cnemidophorus uniparens and C. inornatus). Although these species are genetically very similar, they differ in two aspects of their reproductive biology: (i) the unisexual C. uniparens alternate between expressing female-typical and male-like pseudosexual behaviors while female C. inornatus normally express only female receptive behavior, and (ii) circulating estradiol concentrations in reproductively active female C. uniparens are approximately five-fold lower than in reproductively active female C. inornatus. We found that the regulation of sex steroid receptor gene expression was region specific, with receptor-mRNA expression being increased, unchanged, or decreased during vitellogenesis depending on the area. Furthermore, several species differences in the amount of sex steroid receptor-mRNA were found that may be relevant to the species differences in circulating estrogen concentrations and sexual behavior.

Cloning and in situ hybridization analysis of estrogen receptor, progesterone receptor, and androgen receptor expression in the brain of whiptail lizards (Cnemidophorus uniparens and C. inornatus).

Gonadal steroid hormones act upon specific areas of the vertebrate brain to affect the reproductive physiology and behavior of the animal. Steroid receptors are members of a superfamily of ligand-dependent transcription factors that mediate the effects of steroid hormones by modulating gene expression in the cells containing the receptors. The neuroanatomical distributions of steroid receptor-containing cells have been described for several species by using steroid autoradiography, immunocytochemistry, and more recently in situ hybridization. We have used the polymerase chain reaction to amplify and clone fragments of the estrogen receptor, progesterone receptor, and androgen receptor of whiptail lizards (genus Cnemidophorus). These clones were used to produce probes for use in in situ hybridization assays and to map the neuroanatomical distribution of all three sex steroid hormone receptors in the forebrains of unisexual (C. uniparens) and sexual (C. inornatus) species of whiptail lizards. The distribution of receptor-expressing cells reported here is in general agreement with previous reports in other species with receptor-containing cells concentrated in septal, amygdaloid, cortical, preoptic, and hypothalamic nuclei.

Sequences with the potential to form stem-and-loop structures are associated with coding-region duplications in animal mitochondrial DNA.

Tandem duplications of gene-encoding regions occur in the mitochondrial DNA (mt DNA) of some individuals belonging to several species of whiptail lizards (genus Cnemidophorus). All or part of the duplicated regions of the mtDNAs from five different species were sequenced. In all, the duplication endpoints were within or immediately adjacent to sequences in tRNA, rRNA or protein genes that are capable of forming energetically stable stem-and-loop structures. In two of these mtDNAs, the duplication endpoints were also associated with a direct sequence repeat of 13 bp. The consistent association of stem-and-loop structures with duplication endpoints suggests that these structures may play a role in the duplication process. These data, combined with the absence of direct or palindromic repeats at three of the pairs of duplication endpoints, also suggest the existence of a mechanism for generating de novo duplications that is qualitatively different from those previously modeled.