Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. II. The New Mexico whiptail (Cnemidophorus neomexicanus)

Twelve of 61 (20%) unisexual New Mexico whiptails (Cnemidophorus neomexicanus) from three counties of central New Mexico (USA) and two counties of extreme southwestern Texas (USA) were found to be infected with one or more endoparasites. These included a linstowiid cestode (Oochoristica bivitellobata) in seven (11%), a larval spirurid nematode (Physaloptera sp.) in three (5%), an oxyurid nematode (Pharyngodon warneri) in two (3%) and an unidentified acanthocephalan cystacanth in a single (2%) lizard. This report constitutes the first record of helminths from C. neomexicanus.     

Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. I. The Colorado checkered whiptail (Cnemidophorus tesselatus)

Eleven of 27 (41%) parthenogenetic Colorado checkered whiptails (Cnemidophorus tesselatus) from four counties of western and southwestern Texas were infected with one or more helminths. These included a linstowiid cestode (Oochoristica sp.), a larval spirurid nematode (Physaloptera sp.) and two species of oxyurid nematodes (Parathelandros texanus and Pharyngodon warneri). This note, the first in a series of reports on helminths of Cnemidophorus spp., represents the first record of parasites from C. tesselatus.     

Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. V. Mesocestoides sp. tetrathyridia (Cestoidea: Cyclophyllidea) from four species of Cnemidophorus

Two hundred and one whiptail lizards, Cnemidophorus spp., from Texas and Colorado (USA), were examined for Mesocestoides sp. tetrathyridia. Eleven (5%) were infected, including three of 58 (5%) C. dixoni, six of 70 (9%) C. gularis septemvittatus, one of 35 (3%) C. marmoratus, and one of 34 (3%) C. tesselatus; four C. inornatus heptagrammus were not infected. In addition, 41 non-cnemidophorine lizards from the same study area were not infected. Free tetrathyridia were found in the body cavity of lizards and encapsulated tetrathyridia were observed in the heart, liver, stomach, mesenteries, ovaries, intestines, and lungs. None of the Mesocestoides sp. exhibited any evidence of asexual proliferation such as multiple scoleces or buds. This note, the fifth in a series of reports on helminths of Cnemidophorus spp., represents the first time Mesocestoides sp. has been reported from these four taxa, and Colorado is a new geographic locality record for this parasite.     

Additional notes on requirements of captive whiptail lizards (Cnemidophorus), with emphasis on ultraviolet radiation

Since 1972 we have maintained a colony of parthenogenetic Cnemidophorus exsanguis, which has reached the seventh generation in our laboratory. This paper reports improved husbandry techniques that allow maintenance of healthy, reproducing colonies of this and additional species of Cnemidophorus. In addition, aspects of the physiology of calcium regulation and metabolic bone disease are discussed in relation to the captive rearing of lizards through many generations.     

The reproductive cycle of the western whiptail lizard (Cnemidophorus tigris) in Southern Arizona

Reproduction in Cnemidophorus tigris at Tucson, Arizona follows a seasonal cycle in which gonadal size is minimal in September-October. Male reproductive organs gradually recrudesce during the winter months spent underground. After the lizards emerge from hibernation in March-April the testis, seminiferous epithelial height and tubule diameter gradually increase in size through April and May, reaching maximum size in June-July followed by rapid regression in August. Mating is first observed in the field in May. The ovaries undergo a period of heavy yolk deposition from early April to May, and remain functional until August. A thick circumtesticular subtunic layer of equivalent interstitial material (Leydig cells) is reported and described for the testis of Cnemidophorus.     

Comparisons of physiological performance in sexual and asexual whiptail lizards (genus Cnemidophorus): implications for the role of heterozygosity

Many asexual animal species are of hybrid origin, with consequent high levels of heterozygosity. Data from some studies suggest that increased heterozygosity may be functionally correlated with superior performance in a variety of fitness-related traits. Thus, hybrid asexual species could be expected to exhibit some degree of heterosis. This spontaneous heterosis hypothesis is tested in a comparative study of asexual and sexual species of the lizard genus Cnemidophorus. Asexual species of the genus are parthenogenetically reproducing hybrids of the sexual species and as a result have high levels of heterozygosity that have persisted since their origins. Five whole-organism physiological traits (burst speed, endurance, maximal exertion, standard metabolic rate, and evaporative water loss rate) were examined in five asexual species and the sexual species that gave rise to them. Trait values for sexual and asexual species were compared using a nonphylogenetic approach and two phylogenetically controlled approaches capable of dealing with reticulate phylogenies. In contrast to the predictions of the heterosis hypothesis, performance for four of the traits in asexual Cnemidophorus was not statistically different than that in their sexual parental species, and asexuals had significantly worse endurance. On the whole, the overall trend appeared to be toward worse performance in asexuals. An obvious interpretation of these results is that heterozygosity and "vigor" need not be functionally related. However, other factors may be counterbalancing possible beneficial effects of heterozygosity, including detrimental epistatic effects resulting from the karyotypically mixed genome of these hybrids, and the accumulation of deleterious mutations in the asexual lineages via Muller's ratchet.     

Helminths of Cnemidophorus ruthveni (Squamata: Teiidae) from Bonaire, Netherlands Antilles, with description of a new species of Alaeuris (Nematoda: Pharyngodonidae)

Alaeuris rinconensis n. sp. (Oxyuroidea, Pharyngodonidae) from the large intestine of the Bonaire whiptail lizard, Cnemidophorus ruthveni, is described and illustrated. Alaeuris rinconensis n. sp. represents the 13th Neotropical species assigned to the genus. It is most similar to Alaeuris iguanae in that only these 2 Neotropical species have postbulbar excretory pores; in A. iguanae, a tail filament is absent; in A. rinconensis, a tail filament is present. Two additional helminth species were found, i.e., the cestode Oochoristica iguanae and a nematode, Ozolaimus megatyphlon. Cnemidoporus ruthveni represents a new host record for the latter 2 species.     

Helminths infecting the parthenogenetic whiptail lizard Cnemidophorus nativo in a restinga habitat of Bahia State, Brazil

A sample of 101 specimens of the unisexual whiptail lizard Cnemidophorus nativo (Squamata; Teiidae) from a coastal site in Bahia State, Brazil were examined for the presence of endoparasites. Of these, 35 (34.7%) harboured helminths. Six helminth species were recovered from C. nativo, including five nematodes (Physaloptera retusa, Physalopteroides venancioi, Subulura lacertilia, Skrjabinelazia intermedia and Parapharyngodon sp., and one cestode (Oochoristica ameivae), all representing new host records. Most lizards were infected by a single species of helminth and none by more than three. Infection rates were neither significantly influenced by host body size nor by environmental factors. The results are compared with data from studies on other whiptail species in both South and North America.     

Niche differences between two sympatric whiptail lizards (Cnemidophorus abaetensis and C. ocellifer, Teiidae) in the restinga habitat of northeastern Brazil.

Differences among sympatric lizard species usually result from differences in the use of three resources: space, time and food or some combination of these three. However, differences in resource utilization among sympatric species may simply reflect their specific ecological needs rather than competitive pressures. In this study, we analyzed the temporal, spatial and food niche of two congeneric teiids (Cnemidophorus abaetensis and C. ocellifer) living sympatrically in the "restinga" habitat of Abaeté in the Salvador Municipality, Bahia State, Brazil to assess the degree of niche differentiation among them. The whiptail species overlapped considerably in an hourly activity (Ojk = 0.93), in microhabitat use (Ojk = 0.97) and in the prey items consumed (Ojk = 0.89). Differences in amount of vegetation in the microhabitats used by both lizard species may have contributed to differences in the activity period and in the distribution of the main prey eaten by these lizards which may, in turn, facilitate their coexistence in Abaeté. Although sympatric C. ocellifer and C. abaetensis in Abaeté differed only slightly in their use of microhabitats, period of activity and diet, the most important niche dimension segregating the two species seemed to be the food niche.     

A comparative ultrastructural study of spermatozoa of the teiid lizards Cnemidophorus gularis gularis,Cnemidophorus ocellifer,and Kentropyx altamazonica (Reptilia,Squamata, Teiidae)

The ultrastructure of the spermatozoa of Cnemidophorus gularis gularis, Cnemidophorus ocellifer, and Kentropyx altamazonica is described for the first time. Mature spermatozoa of Cnemidophorus spp. and K. altamazonica differ in the occurrence of a perforatorial base plate, the enlargement of axonemal fibers 3 and 8, and shape of mitochondria. The comparisons of the ultrastructure sperm of Cnemidophorus spp. and K. altamazonica with Ameiva ameiva [J. Morphol. (2002) in press] suggest that Ameiva and Cnemidophorus are more similar to each other than either is to Kentropyx. Statistical analyses reveal that sperm of all three species studied are significantly different in the following dimensions: head, acrosome, distal centriole length, and nuclear shoulders width. There was no variable statistically different between the Cnemidophorus spp. only. The length of the tail, midpiece, entire sperm, and nuclear rostrum are significantly different between K. altamazonica and Cnemidophorus spp. Our results indicate that sperm ultrastructure presents intra and intergeneric variability.     

Diet and foraging of the endemic lizard Cnemidophorus littoralis (Squamata, Teiidae) in the restinga de Jurubatiba, Macaé, RJ.

We investigated the diet and foraging of the endemic teiid lizard Cnemidophorus littoralis in a restinga habitat in Jurubatiba, Macaé - RJ. The stomach contents were removed, analyzed and identified to the Order level. There was no relationship between C. littoralis morphological variables and number, length or volume of preys. Termites (48.7%) and larvae (35.5%) were the most important prey items which occurred in the examined lizards' stomachs. The diet did not differ between males and females. Cnemidophorus littoralis is an active forager and predominantly consumes relatively sedentary prey or prey that is aggregated in the environment. We also found an intact and undigested hatchling of the crepuscular/nocturnal gekkonid lizard Hemidactylus mabouia in the stomach of an adult male of C. littoralis, which indicates that C. littoralis is a potential source of mortality for individuals of H. mabouia in the restinga de Jurubatiba.     

First evidence of cryptic species diversity and significant population structure in a widespread freshwater nematode morphospecies (Tobrilus gracilis)

Free‐living nematodes are ubiquitous and highly abundant in terrestrial and aquatic environments, where they sustain ecosystem functioning by mineralization processes and nutrient cycling. Nevertheless, very little is known about their true diversity and intraspecific population structure. Recent molecular studies on marine nematodes indicated cryptic diversity and strong genetic differentiation of distinct populations, but for freshwater nematode species, analogous studies are lacking. Here, we present the first extensive molecular study exploring cryptic species diversity and genetic population structure of a widespread freshwater nematode morphospecies, Tobrilus gracilis, from nine postglacially formed European lakes. Taxonomic species status of individuals, analysed for fragments of the mitochondrial COI gene and for the large (LSU) and small (SSU) ribosomal subunits, were determined by morphological characteristics. Mitochondrial and nuclear markers strongly supported the existence of three distinct genetic lineages (Tg I–III) within Tobrilus gracilis, suggesting that this morphospecies indeed represents a complex of highly differentiated biological species. High genetic diversity was also observed at the population level. Across the nine lakes, 19 mitochondrial, and seven (LSU) and four (SSU) nuclear haplotypes were determined. A phylogeographical analysis revealed remarkable genetic differentiation even among neighbouring lake populations for one cryptic lineage. Priority and persistent founder effects are possible explanations for the observed population structure in the postglacially colonized lakes, but ask for future studies providing direct estimates of freshwater nematode dispersal rates. Our study suggests therefore that overall diversity of limnetic nematodes has been so far drastically underestimated and challenges the assumed ubiquitous distribution of other, single freshwater nematode morphospecies.     

Tracing the evolution of brain and behavior using two related species of whiptail lizards: Cnemidophorus uniparens and Cnemidophorus inornatus

Cnemidophorus whiptail lizards offer a unique opportunity to study behavioral and neural evolution because unlike most genera, ancestral and descendant species are still extant, and comparisons between species provide a window into correlated changes in biological organization through speciation. This review focuses on the all-female or parthenogenetic species Cnemidophorus uniparens (descendant species), which evolved through several hybridization events involving the sexually reproducing species Cnemidophorus inornatus (ancestral species). Data compiled over more than 2 decades include behavioral, endocrine, and neural differences between these two related species of whiptail lizards. For example, unlike females of the ancestral species, individuals of the descendant species display male-like mounting behavior (pseudocopulatory behavior) after ovulation. Pseudocopulatory behavior in the parthenogen is triggered by the progesterone surge after ovulation, and the behavioral capacity to respond to progesterone appears to be an ancestral trait that was inherited from C. inornatus males through the hybridization events. Interestingly, the regulation of sex steroid hormone receptor mRNA in brain areas critical for the expression of sociosexual behaviors differs between females of the two species and suggests that evolutionary changes in the regulation of gene expression could be a proximate mechanism that underlies the evolution of a novel social behavior in the parthenogen. Finally, because the sexual species is diploid, whereas the parthenogen is triploid, differences between the species could directly assess the effect of ploidy. The behavioral and neuroendocrinological data are pertinent for considering this possibility.     

Drilomermis leioderma n. gen., n. sp. (Mermithidae:Nematoda) parasitizing Cybister fimbriolatus (Say) (Dystiscidae-Coleoptera)

The nematode Drilomermis leioderma n. gen., n. sp. (Merrnithidae) is described from larvae of Cybister fimbriolatus (Say) (Dytiscidae: Coleoptera) in Louisiana. Diagnostic characters of the genus Drilomermis are: medium-sized nematodes with the cuticle appearing smooth (lacking cross fibers) under the light microscope, six cephalic papillae, without mouth papillae, six hypodermal cords at midbody, 2 extremely long spicules (longer than 10 times body width at anus) which are separate and parallel (not twisted), an S-shaped vagina, medium-sized amphids located near head papillae, and postparasitic juvenile with a tail appendage. D. leioderma possesses a ventrally displaced mouth, very long vagina, and male genital papillae arranged in 3 double rows in the vicinity of the cloacal opening. Even when containing multiple parasites, about 40% of the hosts sulwived emergence of the memithids and lived several more days. In nature, some of these hosts may be able to continue their development, which is unusual since most mermithid-parasitized hosts die soon after the nematode emerges.     

Species differences in the regulation of tyrosine hydroxylase in Cnemidophorus whiptail lizards

Evolution of behavioral phenotype involves changes in the underlying neural substrates. Cnemidophorus whiptail lizards enable the study of behavioral and neural evolution because ancestral species involved in producing unisexual, hybrid species still exist. Catecholaminergic systems modulate the expression of social behaviors in a number of vertebrates, including whiptails, and therefore we investigated how changes in catecholamine production correlated with evolutionary changes in behavioral phenotype by measuring the size and number of catecholamine producing (tyrosine hydroxylase-immunoreactive, or TH-ir) cells across the reproductive cycle in females from two related whiptail species. Cnemidophorusuniparens is a triploid, parthenogenetic species that arose from hybridization events involving the diploid, sexual species C. inornatus. Prior to ovulation, females from both species display femalelike receptive behaviors. However, after ovulation, only parthenogenetic individuals display malelike mounting behavior. In all nuclei measured, we found larger TH-ir cells in the parthenogen, a difference consistent with species differences in ploidy. In contrast, species differences in the number of TH-ir cells were nucleus specific. In the preoptic area and anterior hypothalamus, parthenogens had fewer TH-ir cells than females of the sexual species. Reproductive state only affected TH-ir cell number in the substantia nigra pars compacta (SNpc), and C. uniparens individuals had more TH-ir cells after ovulation than when previtellogenic. Thus, species differences over the reproductive cycle in the SNpc are correlated with species differences in behavior, and it appears that the process of speciation may have produced a novel neural and behavioral phenotype in the parthenogen.     

Psychobiology of sexual behavior in a whiptail lizard, Cnemidophorus inornatus

This study investigated the effects of social environment on gonadal recrudescence and sexual behavior in male and female Little Striped Whiptail lizards (Cnemidophorus inornatus). The presence of sexually active males facilitates ovarian recrudescence in conspecific females. Similarly, the presence of reproductively active females facilitates testicular recrudescence in conspecific males. Males housed with females, however, had lower average circulating concentrations of testosterone and dihydrotestosterone, and higher average concentrations of corticosterone compared to intact males housed in isolation. In other studies, the presence of reproductively active females partially restored courtship behavior in castrated males compared to castrated males housed in isolation. Despite the stimulatory effects of females on castrates, exogenous androgens are required for complete restoration of all components of sexual behavior in male C. inornatus. Females are receptive to male courtship and copulatory behavior only during the vitellogenic stages; females in previtellogenic or postovulatory ovarian stages aggressively reject male courtship advances. These findings demonstrate reciprocal effects of sexual behaviors of males and females upon each other's reproductive behavior and physiology.     

Selective breeding of Steinernema feltiae (Filipjev) (Nematoda: Steinernematidae) for improved efficacy in control of a mushroom fly,Lycoriella solani Winnertz (Diptera: Sciaridae)

A method of selecting a Steinernema feltiae strain that is effective against a mushroom fly, Lycoriella solani, is described in detail. The pest control efficacy of the selected nematode strain was evaluated and compared with the efficacy of two unselected strains. The selection procedure was designed to give preference to nematode individuals with the greatest ability (1) to search effectively for the target insect larvae in their natural habitat, (2) to infect them shortly after application and (3) to reproduce in their haemocoel. Thirty‐four rounds of selection achieved a 4‐fold improvement in nematode ability to find and parasitize third‐ and fourth‐instar larvae of the pest in the mushroom substrate. In 24‐h laboratory experiments, mortality of the insect caused by nematode juveniles rose from 22.5%, recorded for the original unselected isolate, to 92.5% for the selected strain. In a 51‐day experiment conducted on a mixed age mushroom house population of L. solani, the enhanced pest control ability of the selected strain was detected shortly after nematode application and remained high throughout the experimental period. During the first 4 weeks of the trial the selected nematode strain was significantly better than both unselected strains and caused 91.1–92.7% reduction of the fly emergence from the mushroom substrate. No difference was observed between the efficacy of the selected nematodes applied at 1 × 10⁶ and 3 ×10⁶ infective juveniles per m², while the unselected strains performed significantly better at the higher concentration. All the nematodes examined showed good persistence in the mushroom casing apparently due to recycling in the insect host.     

The effects of intracranial implantation of estrogen on receptivity in sexually and asexually reproducing female whiptail lizards, Cnemidophorus inornatus and Cnemidophorus uniparens

The ventromedial hypothalamus (VMH) is an important site in the neuroendocrine control of sexual receptivity in mammals. This study was conducted to determine if the VMH was also involved in estrogen induction of receptivity in whiptail lizards. Estradiol benzoate (EB) was implanted into the VMH of ovariectomized Cnemidophorus inornatus, a sexually reproducing species, and C. uniparens, a parthenogenetic species which displays "pseudosexual" behaviors similar to the sexual behaviors typical of both male and female C. inornatus. In both species, EB was significantly more effective in eliciting receptivity when implanted in the VMH than in other locations in the brain. These results support the idea that, as in mammals, the VMH is an important location of estrogen action in the control of receptive behaviors in both sexually and asexually reproducing whiptail lizards.     

Androgens coordinate neurotransmitter‐related gene expression in male whiptail lizards

Sex steroid hormones coordinate neurotransmitter systems in the male brain to facilitate sexual behavior. Although neurotransmitter release in the male brain has been well documented, little is known about how androgens orchestrate changes in gene expression of neurotransmitter receptors. We used male whiptail lizards (Cnemidophorus inornatus) to investigate how androgens alter neurotransmitter‐related gene expression in brain regions involved in social decision making. We focused on three neurotransmitter systems involved in male‐typical sexual behavior, including the N‐methyl‐d ‐aspartate (NMDA) glutamate receptor, nitric oxide and dopamine receptors. Here, we show that in androgen‐treated males, there are coordinated changes in neurotransmitter‐related gene expression. In androgen‐implanted castrates compared with blank‐implanted castrates (control group), we found associated increases in neuronal nitric oxide synthase gene expression in the nucleus accumbens (NAcc), preoptic area and ventromedial hypothalamus, a decrease of NR1 gene expression (obligate subunit of NMDA receptors) in the medial amygdaloid area and NAcc and a decrease in D1 and D2 dopamine receptor gene expression in the NAcc. Our results support and expand the current model of androgen‐mediated gene expression changes of neurotransmitter‐related systems that facilitate sexual behavior in males. This also suggests that the proposed evolutionarily ancient reward system that reinforces sexual behavior in amniote vertebrates extends to reptiles.     

Phylogeography of the endemic St. Lucia whiptail lizard Cnemidophorus vanzoi: Conservation genetics at the species boundary

Vicariance and isolation leading to speciation of reptiles on islands is well exemplified in a number of taxa in the Caribbean. The St. Lucia whiptail (Cnemidophorus vanzoi), considered a single species, is found on two small islets (Maria Major and Maria Minor) off the main island of St. Lucia. From lizards collected from both localities, we gathered morphological measurements and analysed the genetic divergence between populations, using a molecular survey of ∼ ∼2800 mtDNA base pairs and 8 microsatellites. There are significant differences in body size and general form and fixed but small mtDNA differences between island populations. Microsatellites reveal low diversity within populations but very high differentiation between islands with non-overlapping allele size ranges at all except one microsatellite and two loci exhibiting single-base polymorphism, fixed between islands. Based on these results, we examine published criteria to determine whether the studied island forms could be considered true species. According to the phylogenetic species concept and Moritz’s evolutionary significant unit (ESU) criteria, the two lizard populations can be considered separate entities. Crandall et al.’s (2000, Trends Ecol. Evol., 15, 290–295) broader categorization of population distinctiveness, based on concepts of ecological and genetic exchangeability, produces conflicting results depending on the interpretation of the observed ecological data. Following Fraser and Bernatchez’s (2001, Mol. Ecol., 10, 2741–2752) framework for management decisions when ecological data are not sufficient we propose that the lizard populations on the Maria islands are on differing evolutionary trajectories and thus at the species boundary. The populations are of high priority to conservation, thus meriting separate management.