Night Lizard Research Articles

Comparative approaches to understanding speciation: a case study in Xantusia lizards

Abstract The diversity of life forms that surround us formed through a variety of processes. Speciation researchers use a suite of comparative approaches to understand both the generalities and the variance underpinning this diversification. Here, we summarize these approaches and what they have taught us, and we then apply them to understand speciation in the night lizards Xantusia, a genus of small lizards found in the arid regions of western North America. Although Xantusia species span both a range of phenotypic and genetic divergence, we find that speciation in Xantusia appears to be a predictable consequence of divergence in extended periods of allopatry. We conclude by identifying possible areas of growth for comparative studies of speciation.

Parsing variance by marker type: Testing biogeographic hypotheses and differential contribution of historical processes to population structure in a desert lizard.

A fundamental goal of population genetic studies is to identify historical biogeographic patterns and understand the processes that generate them. However, localized demographic events can skew population genetic inference. Assessing populations with multiple types of genetic markers, each with unique mutation rates and responses to changes in population size, can help to identify potentially confounding population-specific demographic processes. Here, we compared population structure and connectivity inferred from microsatellites and restriction site-associated DNA loci among 17 populations of an arid-specialist lizard, the desert night lizard, Xantusia vigilis, in central California to test among historical processes structuring population genetic diversity. We found that both marker types yielded generally concordant insights into population genetic structure including a major phylogenetic break maintained between two populations separated by less than 10 km, suggesting that either marker type could be used to understand generalized demographic patterns across the region for management purposes. However, we also found that the effects of demography on marker discordance could be used to elucidate population histories and distinguish among competing biogeographic hypotheses. Our results suggest that comparisons of within-population diversity across marker types provide powerful opportunities for leveraging marker discordance, particularly for understanding the creation and maintenance of contact zones among clades.

ZZ/ZW Sex Chromosomes in the Madagascar Girdled Lizard, Zonosaurus madagascariensis (Squamata: Gerrhosauridae).

Scincoidea, the reptilian clade that includes girdled lizards, night lizards, plated lizards and skinks, are considered as a lineage with diversity in sex-determining systems. Recently, the hypothesis on the variability in sex determination in skinks and even more the absence of sex chromosomes in some of them has been rivalling. Homologous, evolutionary stable XX/XY sex chromosomes were documented to be widespread across skinks. However, sex determination in the other scincoidean families is highly understudied. ZZ/ZW sex chromosomes have been identified only in night lizards and a single species of plated lizards. It seems that although there are different sex chromosome systems among scincoidean lineages, they share one common trait: they are mostly poorly differentiated and often undetectable by cytogenetic methods. Here, we report one of the exceptions, demonstrating for the first time ZZ/ZW sex chromosomes in the plated lizard Zonosaurus madagascariensis. Its sex chromosomes are morphologically similar, but the W is clearly detectable by comparative genomic hybridization (CGH), suggesting that the Z and W chromosomes highly differ in sequence content. Our findings confirm the presence of female heterogamety in plated lizards and provides novel insights to expand our understanding of sex chromosome evolution in scincoidean lizards.

Evolutionary origins of the prolonged extant squamate radiation

Squamata is the most diverse clade of terrestrial vertebrates. Although the origin of pan-squamates lies in the Triassic, the oldest undisputed members of extant clades known from nearly complete, uncrushed material come from the Cretaceous. Here, we describe three-dimensionally preserved partial skulls of two new crown lizards from the Late Jurassic of North America. Both species are placed at the base of the skink, girdled, and night lizard clade Pan-Scincoidea, which consistently occupies a position deep inside the squamate crown in both morphological and molecular phylogenies. The new lizards show that several features uniting pan-scincoids with another major lizard clade, the pan-lacertoids, in trees using morphology were convergently acquired as predicted by molecular analyses. Further, the palate of one new lizard bears a handful of ancestral saurian characteristics lost in nearly all extant squamates, revealing an underappreciated degree of complex morphological evolution in the early squamate crown. We find strong evidence for close relationships between the two new species and Cretaceous taxa from Eurasia. Together, these results suggest that early crown squamates had a wide geographic distribution and experienced complicated morphological evolution even while the Rhynchocephalia, now solely represented by the tuatara, was the dominant clade of lepidosaurs.

A statistical reanalysis of morphological differentiation among island night lizards (Xantusia riversiana) from the California Channel Islands

This study re-analyzes morphometric and meristic data among island night lizards, Xantusia riversiana, from the California Channel Islands of San Clemente, Santa Barbara, and San Nicolas in order to ascertain whether the implementation of different statistical methods can recover different results that could potentially alter biological interpretations. Our results concur with a recent previous study demonstrating that the three island populations differ morphologically from one another and that the San Nicolas Island population is the most divergent. Several important aspects, however, of the previous study depart significantly from those recovered here. Our analyses found sexual dimorphism within each population for both morphometric and meristic characters to be relatively uncommon whereas the previous study found nearly all characters to be sexually dimorphic for all island populations. The previous study also recovered significant differences among the three island populations for all morphometric characters whereas far fewer differences were recovered in the present study. Both studies found few significant inter-island differences among the meristic characters. The discordances between these two studies stem from differences in the a priori treatment of the raw character data and the different downstream statistical analyses and visualization techniques used on those data. This was particularly relevant with the use here of an allometric growth algorithm for size-correcting the morphometric data not used in the previous study and by treating all three populations as independently evolving groups. We did not conduct analyses where data from the San Clemente and Santa Barbara island populations were conflated based on their subspecific designation (X. r. reticulata) and then compared to data from the independently evolving San Nicolas Island population. This imprudent use of taxonomy violates the assumptions of statistical independence. We emphasize that explicit justification for the use of particular statistical analyses should occur in all studies—especially if the results bear on the implementation of effective and efficient resource management programs.

A New Species of Night Lizard of the Genus Lepidophyma (Xantusiidae) from Southern Mexico

Here, we describe a new species of the genus Lepidophyma (Xantusiidae) from the Veracruzan biotic province of western Chiapas and adjacent Tabasco. The new species was discovered in a phylogenetic study performed by previous workers, who found that this species was the sister taxon to a clade composed of Lepidophyma lipetzi as the sister taxon to Lepidophyma reticulatum and Lepidophyma flavimaculatum. However, the new species is morphologically most similar to L. flavimaculatum, a widely distributed taxon with which the new species was previously confused. The new species inhabits tropical deciduous and tropical evergreen forest, montane cloud forest, and anthropic environments such as pasture–tropical forest borders and agroecosystems between 70 and 1100 m of elevation. The new species increases the number of species described in the genus to 22.

Comparative ecomorphology of the sandstone night lizard (Xantusia gracilis) and the granite night lizard (Xantusia henshawi)

Abstract It is hypothesized that shape differences between the closely related sandstone night lizard (Xantusia gracilis) and the granite night lizard (X. henshawi) may be correlated with structual differences in their respective microhabitats. Multivariate and univariate analyses of 22 morphometric characters taken from the head, body, and limbs of both saxicolus specialists recovered statistically significant differences between them with X. gracilis having a wider head, longer snout, larger eyes, wider sternum, higher and wider pelvis, thinner limbs, longer forearms and thighs, and longer hind limbs. Many of these same proportional differences have been reported among very closely related saxicolus species in other lizard families (i.e. Eublepharidae, Gekkonidae, Phrynosomatidae) that also live on different rocky substrates. This supports the inference that morphometric differences between X. gracilis and X. henshawi are ecomorphological adaptations for navigating the substantially different substrates of their respective microhabitats. Xantusia gracilis is restricted to a loose, heterogeneous, sandstone microhabitat composed of large boulders, small rocks, and cliff faces where cracks, crevices, holes, and exfoliations are used as retreats versus the compact, more homogeneous, granite boulder microhabitat of X. henshawi where narrow spaces beneath exfoliations and cap-rocks are the preferred retreats.

Mixed-sex offspring produced via cryptic parthenogenesis in a lizard.

Facultative parthenogenesis in vertebrates is believed to be exceptional, and wherever documented, it always led to single-sex progeny with genome-wide homozygosity. We report the first challenge to this paradigm: frequent facultative parthenogenesis in the previously assumed sexually reproducing tropical night lizard Lepidophyma smithii results in offspring of both sexes and preserves heterozygosity in many loci polymorphic in their mothers. Moreover, we documented a mixture of sexually and parthenogenetically produced progeny in a single clutch, which documents how cryptic a facultative parthenogenesis can be. Next, we show that in the studied species, 1) parthenogenetically produced females can further reproduce parthenogenetically, 2) a sexually produced female can reproduce parthenogenetically, 3) a parthenogenetically produced female can reproduce sexually, and 4) a parthenogenetically produced male is fully fertile. We suggest that facultative parthenogenesis should be considered even in vertebrates with frequent males and genetically variable, heterozygous offspring.

First Report of Sex Chromosomes in Night Lizards (Scincoidea: Xantusiidae).

Squamate reptiles (lizards, snakes, and amphibians) are an outstanding group for studying sex chromosome evolution-they are old, speciose, geographically widespread, and exhibit myriad sex-determining modes. Yet, the vast majority of squamate species lack heteromorphic sex chromosomes. Cataloging the sex chromosome systems of species lacking easily identifiable, heteromorphic sex chromosomes, therefore, is essential before we are to fully understand the evolution of vertebrate sex chromosomes. Here, we use restriction site-associated DNA sequencing (RADseq) to classify the sex chromosome system of the granite night lizard, Xantusia henshawi. RADseq is an effective alternative to traditional cytogenetic methods for determining a species' sex chromosome system (i.e., XX/XY or ZZ/ZW), particularly in taxa with non-differentiated sex chromosomes. Although many xantusiid lineages have been karyotyped, none possess heteromorphic sex chromosomes. We identified a ZZ/ZW sex chromosome system in X. henshawi-the first such data for this family. Furthermore, we report that the X. henshawi sex chromosome contains fragments of genes found on Gallus gallus chromosomes 7, 12, and 18 (which are homologous to Anolis carolinensis chromosome 2), the first vertebrate sex chromosomes to utilize this linkage group.

Precipitation and prey abundance influence food habits of an invasive carnivore

AbstractInvasive predators threaten biodiversity worldwide, and generalist invasive predators are often more successful due to their broad diets. Predation patterns can be influenced by prey abundance, prey preference, and climate, and understanding these relationships is integral to conserving native prey species. We examined stomach contents of 2882 feral cats Felis catus from San Clemente Island, California, to assess how their diets varied annually and seasonally, and how precipitation and prey abundance influenced predation patterns. Rodents were found in 95% (n = 2589) of stomachs containing prey. The endemic San Clemente deer mouse Peromyscus maniculatus clementis was the most prevalent prey species and was found in 85% (n = 2589) of stomachs containing prey. Consumption of rodents, lizards, and birds varied annually. In years following dry winters, consumption of rodents decreased and consumption of lizards increased. This had a particularly strong effect on endemic night lizards Xantusia riversiana reticulata with 20.4% (n = 1952) of non‐empty cat stomachs containing night lizards following normal years, and 43.7% (n = 602) following dry years. Consumption of rodents peaked in fall, while consumption of lizards and birds peaked in spring. Using rodenticide removed from bait stations as an index of rodent abundance, we found a positive correlation between bait removal and the number of rodents consumed by cats, and a negative correlation between bait removal and the number of lizards consumed by cats. These results suggest that feral cats use rodents as primary prey and lizards as secondary prey, particularly during droughts when rodent abundance is low. Understanding how weather patterns affect invasive species predation patterns will help conservation biologists predict and manage for the effects of invasive species as climate change continues. Furthermore, identifying and quantifying diet pattern seasonality can help managers identify times when sensitive species are vulnerable and plan interventions accordingly.

Morphological Divergence among Populations ofXantusia riversiana,a Night Lizard Endemic to the Channel Islands of California

Morphological variation between closely related island endemics offers a unique system to study ecological and evolutionary processes. The Island Night Lizard, Xantusia riversiana (Cope, 1883), is endemic to three of the Southern Channel Islands off the coast of Southern California: Santa Barbara, San Clemente, and San Nicolas. Some authors treat the species as polytypic with the night lizards on San Nicolas (X. r. riversiana) distinct from those on Santa Barbara and San Clemente (X. r. reticulata). Previous studies failed to find strong morphological divergence, but it remains uncertain if those studies were hampered by a combination of small sample size, small number of characters, and/or the lack of modern morphometric techniques. Here we examined 172 Island Night Lizards from the three islands for nine morphometric and five meristic characters, increasing the number and types of morphological characters examined over previous studies and applying modern morphometric techniques to test for divergence a...

Distribution, Habitat, and Population Size of Island Night Lizards on San Nicolas Island, California

The Island Night Lizard (Xantusia riversiana) was removed from the federal list of threatened species in May 2014. This strongly differentiated species is endemic to 3 of the southern California Channel Islands—San Clemente, San Nicolas, and Santa Barbara. Suitable habitat for Island Night Lizards is extensive on San Clemente Island, and the species is abundant there. Habitat is limited and fragmented, however, on San Nicolas Island and small Santa Barbara Island. Bringing together extensive field surveys and mark-recapture sampling, we synthesize available data for Island Night Lizards on San Nicolas Island and calculate population and density estimates for the species in major habitats on the island. Island Night Lizards are widely distributed across most of the eastern half of San Nicolas Island. In contrast, they are nearly absent over the western third of the island except for isolated populations in boulder beach habitats. We combined mark-recapture population estimates with comprehensive measurements of the extent of cactus, boxthorn, and other habitat types on the island to arrive at a more accurate assessment of the status of Island Night Lizards on San Nicolas Island. High densities of Island Night Lizards on the island are found in small areas of cholla cactus (Cylindropuntia prolifera; mean of 4100 lizards/ha), boulder beach habitat (mean of 3400 lizards/ha), and prickly pear cactus (Opuntia spp.; mean of 1700 lizards/ha); low numbers are found in more extensive mixed-shrub habitat (mean of 250 lizards/ha). The U.S. Fish and Wildlife Service requires a post-delisting program for “monitoring the overall health of the Island Night Lizard” to assure the continued long-term viability of the species in its restricted distribution. The information on population size and habitat presented here will inform and guide conservation and management efforts by the U.S. Navy on San Nicolas Island over the coming years.

Thermal ecology and activity patterns of six species of tropical night lizards (Squamata: Xantusiidae: Lepidophyma) from Mexico

Activity patterns in ectotherms rely on the structure of the thermal environment and thermoregulatory opportunities during activity periods. A dichotomy between diurnal and nocturnal ectotherms is not clear in every case, and temperature can directly affect the daily activity period in these organisms during both photophase and scotophase. In the present study we evaluate the thermal ecology of six tropical night lizards (genus Lepidophyma) from Mexico. Our results indicate a thermoconformer strategy in most of the studied species. In these species, thermal tolerances are associated with environmental temperatures to which they are exposed. Furthermore, thermal quality of the environment directly determines the daily activity period. Therefore, we argue that diurnal activity in Lepidophyma species is determined by local thermal conditions.

Rare long-distance dispersal of the Island Night Lizard, Xantusia riversiana, maintains high diversity in a fragmented environment

The Island Night Lizard (Xantusia riversiana) is endemic to three of the Channel Islands off the coast of California, USA. Introduced species such as goats, sheep, and cats have profoundly affected the fauna and flora of the islands for over 150 years, but most of these non-native species have been recently removed. We measured the distribution of genetic diversity in Island Night Lizards across San Nicolas Island using DNA microsatellites to assess the impacts of historical habitat change on effective population size, gene flow, and population divergence; to provide baseline data for future monitoring of genetic diversity; and to provide recommendations to inform the restoration of degraded habitat. Despite a history of profound anthropogenic habitat disturbance, genetic diversity was high within sites, and there was no evidence of population bottlenecks. Divergence between sites was extraordinarily high, as expected for this sedentary species. Landscape resistance modeling using circuit theory showed that unsuitable habitat is relatively permeable to gene flow compared to suitable habitat, and yet populations separated by very short geographic distances remain genetically distinct. We found no evidence of a need for short-term intervention such as artificial translocations to maintain genetic diversity. Instead, we suggest that management should focus on maintaining, improving, and increasing habitat, especially in creating patches of habitat to link existing sites.

The Use of Chemical Cues by Granite Night Lizards (Xantusia henshawi) to Evaluate Potential Predation Risk

Squamate reptiles have highly developed chemosensory systems used to detect both predators and prey. Although the general ability of squamates to assess predation risk using chemical cues is well known, the detail to which squamates can make discriminations concerning risk is largely unexamined. Granite Night Lizards (Xantusia henshawi) are habitat specialists that live in exfoliations of granite boulders in dense populations. We measured the responses of Granite Night Lizards to the scent of a sympatric predator, the Lyre Snake (Trimorphodon lyrophanes), maintained on two different diets (lizard-fed and mouse-fed), as well as a non-predatory snake (the Shovelnose Snake, Chionactis occipitalis) and a blank control. We also evaluated the potential use of conspecific chemical cues to assess predation risk by quantifying the response of lizards to the scent of both calm and stressed conspecifics. We collected scents for both experiments on paper pads, which we then placed at the entrance of a shelter within a testing arena containing a focal lizard. We then used video cameras to record the behavior of focal lizards over a 60-minute period. We found that, compared to the blank control, Night Lizards in the presence of chemical cues from snakes took longer to enter the shelter, spent longer investigating chemical cues, and traveled further before entering the shelter. Lizards also spent longer investigating chemical cues from Lyre Snakes than Shovelnose Snakes. However, there were no significant differences between responses to lizard-fed and mouse-fed Lyre Snake chemical cues. We also found no evidence that lizards use conspecific chemical cues to evaluate predation risk. This study demonstrates that Granite Night Lizards can use chemical cues from their predators to assess predation risk, but further research is needed to assess whether these responses differ based on the diet of the predator.

Historical Environment Is Reflected in Modern Population Genetics and Biogeography of an Island Endemic Lizard (Xantusia riversiana reticulata).

The restricted distribution and isolation of island endemics often produces unique genetic and phenotypic diversity of conservation interest to management agencies. However, these isolated species, especially those with sensitive life history traits, are at high risk for the adverse effects of genetic drift and habitat degradation by non-native wildlife. Here, we study the population genetic diversity, structure, and stability of a classic “island giant” (Xantusia riversiana, the Island Night Lizard) on San Clemente Island, California following the removal of feral goats. Using DNA microsatellites, we found that this population is reasonably genetically robust despite historical grazing, with similar effective population sizes and genetic diversity metrics across all sampling locations irrespective of habitat type and degree of degradation. However, we also found strong site-specific patterns of genetic variation and low genetic diversity compared to mainland congeners, warranting continued special management as an island endemic. We identify both high and low elevation areas that remain valuable repositories of genetic diversity and provide a case study for other low-dispersal coastal organisms in the face of future climate change.

Threatened San Clemente Bell's Sparrow Nest Depredated by Island Night Lizard

We used remote video monitoring systems to document nest predators at San Clemente Bell's Sparrow (Artemisiospiza belli clementeae) nests and recorded an unexpected depredation by an island night lizard (Xantusia riversiana) on 22 May 2013. This record is the first documented case of a San Clemente Bell’s Sparrow being depredated by any reptile and is also the first documentation of any night lizard species (genus Xantusia) depredating a bird's nest. Additionally, we found that night lizards are among the smallest lizard species ever observed depredating a bird's nest.

Development and characterization of 12 microsatellite markers for the Island Night Lizard (Xantusia riversiana), a threatened species endemic to the Channel Islands, California, USA

The Island Night Lizard is a federally threatened species endemic to the Channel Islands of California. Twelve microsatellite loci were developed for use in this species and screened in 197 individuals from across San Nicolas Island, California. The number of alleles per locus ranged from 6 to 21. Observed heterozygosities ranged from 0.520 to 0.843. These microsatellite loci will be used to investigate population structure, effective population size, and gene flow across the island, to inform protection and management of this species.

Early Eocene Lizards of the Wasatch Formation near Bitter Creek, Wyoming: Diversity and Paleoenvironment during an Interval of Global Warming

Lizards (nonophidian squamates) from a vertical series of localities in the early Eocene Wasatch Formation (Washakie Basin, Wyoming, USA) deposited during an interval of global warming are described on the basis of isolated cranial and some postcranial bones. At least 24 species are present. New material supports a close relationship of the iguanid Paranolis to Anolis (to the exclusion of Anolbanolis). Records of Tinosaurus and Scincoideus are the earliest in North America; a potential affinity of the latter, a new species, with Lacertidae is explored. A new species of Palaeoxan tusia and two species related to Neotropical Night Lizards, Lepidophyma, are named. A rhineurid amphisbaenian is present. New material of Apodosauriscus minutus further bolsters the case for its relationship to living Anniella. Glyptosaurine anguids are also present, including new species referred to Xestops, Arpadosaurus, and Glyptosaurus, the last with distinctive crushing posterior teeth. A distinctive new anguimorph lineage, Entomophontes, may be related to Xenosaurus. Considerable cranial material is referred to a new species of Provaranosaurus; we argue that this lineage is closely related to extant Shinisaurus. Restes-like remains are smaller and rare. Helodermatidae is represented by a single osteoderm. The varanid Saniwa is present. The four localities examined here record an interval of warming in the Rocky Mountain interior, when temperatures rose toward their Cenozoic acme in the Eocene Climatic Optimum. Faunal composition shows only two major deviations at a higher taxonomic level, suggesting a prevailing stability. Maximal within-locality species diversity (richness), based on cranial material (18 species), is seen at the top of the section. The diversity difference between the upper and lower part of the section is statistically significant. There is an underlying component of noise to the diversity data with regard to rarer taxa. Diversity changes primarily as a result of dispersal on a local level.

Phylogenetic relationships within the lizard clade Xantusiidae: Using trees and divergence times to address evolutionary questions at multiple levels

Xantusiidae (night lizards) is a clade of small-bodied, cryptic lizards endemic to the New World. The clade is characterized by several features that would benefit from interpretation in a phylogenetic context, including: (1) monophyletic status of extant taxa Cricosaura, Lepidophyma, and Xantusia; (2) a species endemic to Cuba (Cricosaura typica) of disputed age; (3) origins of the parthenogenetic species of Lepidophyma; (4) pronounced micro-habitat differences accompanied by distinct morphologies in both Xantusia and Lepidophyma; and (5) placement of Xantusia riversiana, the only vertebrate species endemic to the California Channel Islands, which is highly divergent from its mainland relatives. This study incorporates extensive new character data from multiple gene regions to investigate the phylogeny of Xantusiidae using the most comprehensive taxonomic sampling available to date. Parsimony and partitioned Bayesian analyses of more than 7kb of mitochondrial and nuclear sequence data from 11 loci all confirm that Xantusiidae is monophyletic, and comprises three well-supported clades: Cricosaura, Xantusia, and Lepidophyma. The Cuban endemic Cricosaura typica is well supported as the sister to all other xantusiids. Estimates of divergence time indicate that Cricosaura diverged from the (Lepidophyma+Xantusia) clade ∼81million years ago (Ma), a time frame consistent with the separation of the Antilles from North America. Our results also confirm and extend an earlier study suggesting that parthenogenesis has arisen at least twice within Lepidophyma without hybridization, that rock-crevice ecomorphs evolved numerous times (>9) within Xantusia and Lepidophyma, and that the large-bodied Channel Island endemic X. riversiana is a distinct, early lineage that may form the sister group to the small-bodied congeners of the mainland.