Alligator Lizard Research Articles

Mandibular gland proteomics of the Mexican alligator lizard, Abronia graminea, and the red-lipped arboreal alligator lizard, Abronia lythrochila

A useful approach to deepen our knowledge about the origin and evolution of venom systems in Reptilia has been exploring the vast biodiversity of this clade of vertebrates in search of orally produced proteins with toxic actions, as well as their corresponding delivery systems. The occurrence of toxins in anguimorph lizards has been demonstrated experimentally or inferred from reports of the toxic effects of the oral secretions of taxa within the Varanidae and Helodermatidae families. In the present study, we have focused on two alligator lizards of the Anguidae family, the Mexican alligator lizard, Abronia graminea, and the red-lipped arboreal alligator lizard, A. lythrochila. In addition, the fine morphology of teeth of the latter species is described. The presence of a conserved set of proteins, including B-type natriuretic peptides, cysteine-rich secretory proteins, group III phospholipase A2, and kallikrein, in submandibular gland extracts was demonstrated for both Abronia species. These proteins belong to toxin families found in oral gland secretions of venomous reptile species. This finding, along with previous demonstration of toxin-producing taxa in both paleo- and neoanguimorpha clades, provides further support for the existence of a handful of conserved toxin families in oral secretions across the 100+ million years of Anguimorpha cladogenesis.

Ideas for collaborative social participation for the protection of charismatic species of the genus Abronia (alligator lizards, alicante lizards, abronias, tree scorpions)

A proposal for social participation is offered for the conservation of some populations of the genus Abronia (alicantes, dragonets) in urban-rural interface areas.

Bridging the gap: A new species of arboreal Abronia (Squamata: Anguidae) from the Northern Highlands of Chiapas, Mexico.

The mountain forests of Middle America are renowned for their endemic biodiversity, and arboreal alligator lizards (genus Abronia) are high-profile vertebrates endemic to this region. In this work, we describe a new species of arboreal Abronia that is known only from the type locality in the Northern Highlands of Chiapas, Mexico. The new species is diagnosed from all other members of the genus Abronia by the following combination of characters: lack of protuberant or spine-like supra-auricular scales, lack of protuberant or casque-like posterolateral head scales, dorsum of head pale yellow with distinct dark markings, 35-39 transverse dorsal scale rows, lateralmost row of ventral scales enlarged relative to adjacent medial row, and dorsum brown with darker crossbands that are sometimes reduced to rows of spots. We provisionally include the new species in the subgenus Lissabronia based on genomic and morphological evidence, but our results also suggest a close relationship to the subgenus Abaculabronia. The new species is geographically separated from the nearest Lissabronia and Abaculabronia species by the lowland Central Depression of Chiapas. Ongoing habitat loss and other factors imperil the new species, leading us to propose its listing under multiple threatened species frameworks. Because the Northern Highlands have poor coverage of protected areas, we briefly comment on the potential of this new species for stimulating conservation in the region.

Repeated patterns of reptile diversification in Western North America supported by the Northern Alligator Lizard (Elgaria coerulea).

Understanding the processes that shape genetic diversity by either promoting or preventing population divergence can help identify geographic areas that either facilitate or limit gene flow. Furthermore, broadly distributed species allow us to understand how biogeographic and ecogeographic transitions affect gene flow. We investigated these processes using genomic data in the Northern Alligator Lizard (Elgaria coerulea), which is widely distributed in Western North America across diverse ecoregions (California Floristic Province and Pacific Northwest) and mountain ranges (Sierra Nevada, Coastal Ranges, and Cascades). We collected single-nucleotide polymorphism data from 120 samples of E. coerulea. Biogeographic analyses of squamate reptiles with similar distributions have identified several shared diversification patterns that provide testable predictions for E. coerulea, including deep genetic divisions in the Sierra Nevada, demographic stability of southern populations, and recent post-Pleistocene expansion into the Pacific Northwest. We use genomic data to test these predictions by estimating the structure, connectivity, and phylogenetic history of populations. At least 10 distinct populations are supported, with mixed-ancestry individuals situated at most population boundaries. A species tree analysis provides strong support for the early divergence of populations in the Sierra Nevada Mountains and recent diversification into the Pacific Northwest. Admixture and migration analyses detect gene flow among populations in the Lower Cascades and Northern California, and a spatial analysis of gene flow identified significant barriers to gene flow across both the Sierra Nevada and Coast Ranges. The distribution of genetic diversity in E. coerulea is uneven, patchy, and interconnected at population boundaries. The biogeographic patterns seen in E. coerulea are consistent with predictions from co-distributed species.

Spatial Ecology of the Texas Alligator Lizard (Gerrhonotus infernalis) in Blanco County, Texas

Spatial Ecology of the Texas Alligator Lizard (Gerrhonotus infernalis) in Blanco County, Texas

Sustained force production by the jaw-adductor muscles of a megalophagous frog, Ceratophrys cranwelli.

Most frogs have weak jaws that play a relatively minor role in tongue-mediated prey capture. Horned frogs (Ceratophrys spp.), however, follow the projection of a large tongue with a vice-like grip of their jaws to hold and immobilize prey. Prey include relatively large vertebrates, which they may restrain for minutes to possibly hours. High endurance behaviors, such as prolonged biting, require that muscles be capable of sustained force production. The feeding behavior of Ceratophrys suggests that their jaw-adductor muscles may be capable of powering sustained bites for long periods. We examined the capacity for sustained bite force by conducting an in situ experiment during which we measured bite force while bilaterally and supramaximally stimulating the jaw-adductor muscles of euthanized Cranwell's horned frogs (C. cranwelli). Muscles were stimulated for at least 60 min with a series of tetanic trains, with one experiment lasting over 6 h. We found that a significant sustained force develops during the first few minutes of the experiment, and this force is present between tetanic trains when the muscles are not being stimulated. The sustained force persists long after tetanic forces are barely detectable. The observed sustained force phenomenon parallels that observed for the jaw-adductor muscles of alligator lizards (Elgaria), another animal capable of sustained biting. The ability to bite with sustained and significant force by C. cranwelli may be facilitated by a configuration of different muscle fiber types, such as slow tonic fibers, as well as specializations in the muscle fibers that mitigate the effects of fatigue.

Near‐shore island lizard fauna shaped by a combination of human‐mediated and natural dispersal

AbstractAimIsland biotas provide opportunities to study colonization and adaptation to novel environments. Islands, especially near‐shore islands, may have a long record of human habitation such that some lineages result from human‐assisted introductions. Here, we combine phylogenetic analyses with fossil data and historical specimen records to reconstruct colonization histories, characterize among‐island divergence and assess the role of humans in shaping the evolutionary history of lizards inhabiting a near‐shore island archipelago.LocationChannel Islands and adjacent mainland of California, United States.TaxaWestern fence lizard (Sceloporus occidentalis), southern alligator lizard (Elgaria multicarinata), common side‐blotched lizard (Uta stansburiana).MethodsWe sequenced mitochondrial DNA (ND1, cyt‐b) from each of three lizard species, covering their entire island distributions plus the adjacent mainland. For each, we estimated diversity within and among each island, obtained maximum likelihood bootstrapped phylogenies, constructed haplotype networks and tested for population expansion. We used museum specimen records and microfossil evidence to infer colonization scenarios.ResultsSceloporus occidentalis is characterized by a single island‐colonization event, and exhibits the deepest divergences from mainland relatives and the highest among‐island divergence. Elgaria multicarinata and Uta stansburiana each have at least three distinct colonization events, with fossil and historical data indicating that some of these occurred after humans arrived to the islands.Main ConclusionsThe evolution of Channel Island lineages for two lizard taxa has been mediated by ancient and contemporary anthropogenic activity, while the evolution of the third is shaped by natural dispersal and vicariance caused by sea‐level rise. Genetic divergence corroborates the treatment of S. occidentalis as an endemic island species, Sceloporus becki. The unique histories of these three taxa are synthesized with other Channel Island lineages highlighting that taxa inhabiting islands with long histories of human activity should be carefully studied to assess the role of people in facilitating colonization and subsequent gene flow.

Phylogenomics of arboreal alligator lizards shed light on the geographical diversification of cloud forest‐adapted biotas

AbstractAimThe proximate ecological and evolutionary processes underlying the high biodiversity of neotropical montane cloud forests are still very poorly understood. Climatic oscillations may have contributed to vicariance and cladogenesis, but also promoted secondary contact and erosion of genetic divergence. Here we tested whether geographical diversification – or its lack thereof – in a complex of arboreal alligator lizards is explained by range shifts during Quaternary climatic oscillations.LocationPine–oak and cloud forests, central Mexico.TaxonAbronia taeniata–gramineaspecies complex (Squamata: Anguidae: Gerrhonotinae).MethodsWe generated genomic data (ddRADseq) to infer patterns of geographical diversification in the complex, reconstruct its demographic history, estimate the timing of lineage split, and test for the presence of contemporary and/or historical hybridization. We evaluated whether the tempo and mode of diversification (i.e. strict isolation vs. secondary contact with introgression) are explained by the contemporary distribution of suitable habitats and/or range shifts experienced by the complex since the Last Glacial Maximum (LGM), as inferred from environmental niche modelling (ENM).ResultsGenomic data supported a marked genetic structure within the complex, and phylogenomic and dating analyses revealed cryptic lineage diversification starting at the onset of the Pleistocene followed by secondary contact with limited introgression. ENM pointed to considerable range expansions of the complex during the LGM and a marked fragmentation and scarce connectivity among contemporary populations, which was supported by genomic‐based demographic reconstructions.Main ConclusionsThe geographical diversification of the complex has been moulded by vicariant events promoted by Pleistocene geologic and climatic changes impacting the distribution of their pine–oak and cloud forest habitats. Our data supported a model of divergence with introgression, indicating that pulses of population fragmentation and expansion during the Quaternary have led to multiple opportunities for both allopatric isolation and secondary contact.

Correction to: Phylogenomics of alligator lizards elucidate diversification patterns across the Mexican Transition Zone and support the recognition of a new genus

Correction to: Phylogenomics of alligator lizards elucidate diversification patterns across the Mexican Transition Zone and support the recognition of a new genus

A strikingly ornamented fossil alligator lizard (Squamata:Abronia) from the Miocene of California

AbstractExtant alligator lizards of the genus Abronia are found in montane cloud forests and pine-oak forests of Mesoamerica and are iconic among the public and scientific communities. Here, we describe a fossilized partial skull from the Miocene of southern California (~12.5–11.0 Mya) that is the first definitive fossil and only recognized extinct species of Abronia. The locality of the fossil is substantially removed from the range of extant species of Abronia. This remarkable biogeographical discovery corroborates previous speculation that Abronia was distributed north of Mexico during the Neogene, a scenario that could not be inferred from the geographical ranges and phylogeny of the extant species alone. Additionally, the fossil preserves a distinctive morphology, osteoderm sails, that appears unique to the new taxon among alligator lizards. The finding emphasizes the importance of the fossil record for historical biogeography and could motivate new avenues of biogeographical research in Mesoamerica and the USA.

Phylogenomics of alligator lizards elucidate diversification patterns across the Mexican Transition Zone and support the recognition of a new genus

AbstractGenomic data continue to advance our understanding of species limits and biogeographic patterns. However, there is still no consensus regarding appropriate methods of phylogenomic analysis that make the best use of these heterogeneous data sets. In this study, we used thousands of ultraconserved element (UCE) loci from alligator lizards in the genus Gerrhonotus to compare and contrast species trees inferred using multiple contemporary methods and provide a time frame for biological diversification across the Mexican Transition Zone (MTZ). Concatenated maximum likelihood (ML) and Bayesian analyses provided highly congruent results, with differences limited to poorly supported nodes. Similar topologies were inferred from coalescent analyses in Bayesian Phylogenetics and Phylogeography and SVDquartets, albeit with lower support for some nodes. All divergence times fell within the Miocene, linking speciation to local Neogene vicariance and/or global cooling trends following the mid-Miocene Climatic Optimum. We detected a high level of genomic divergence for a morphologically distinct species restricted to the arid mountains of north-eastern Mexico, and erected a new genus to better reflect evolutionary history. In summary, our results further advocate leveraging the strengths and weaknesses of concatenation and coalescent methods, provide evidence for old divergences for alligator lizards, and indicate that the MTZ continues to harbour substantial unrecognized diversity.

A new extinct species of alligator lizard (Squamata: Elgaria) and an expanded perspective on the osteology and phylogeny of Gerrhonotinae

BackgroundAlligator lizards (Gerrhonotinae) are a well-known group of extant North American lizard. Although many fossils were previously referred to Gerrhonotinae, most of those fossils are isolated and fragmentary cranial elements that could not be placed in a precise phylogenetic context, and only a handful of known fossils are articulated skulls. The fossil record has provided limited information on the biogeography and phylogeny of Gerrhonotinae.ResultsWe redescribe a nearly complete articulated fossil skull from the Pliocene sediments of the Anza-Borrego Desert in southern California, and refer the specimen to the alligator lizard genus Elgaria. The fossil is a representative of a newly described species, Elgaria peludoverde. We created a morphological matrix to assess the phylogeny of alligator lizards and facilitate identifications of fossil gerrhonotines. The matrix contains a considerably expanded taxonomic sample relative to previous morphological studies of gerrhonotines, and we sampled two specimens for many species to partially account for intraspecific variation. Specimen-based phylogenetic analyses of our dataset using Bayesian inference and parsimony inferred that Elgaria peludoverde is part of crown Elgaria. The new species is potentially related to the extant species Elgaria kingii and Elgaria paucicarinata, but that relationship was not strongly supported, probably because of extensive variation among Elgaria. We explored several alternative biogeographic scenarios implied by the geographic and temporal occurrence of the new species and its potential phylogenetic placements.ConclusionsElgaria peludoverde is the first described extinct species of Elgaria and provides new information on the biogeographic history and diversification of Elgaria. Our research expands the understanding of phylogenetic relationships and biogeography of alligator lizards and strengthens the foundation of future investigations. The osteological data and phylogenetic matrix that we provided will be critical for future efforts to place fossil gerrhonotines. Despite limited intraspecific sampled sizes, we encountered substantial variation among gerrhonotines, demonstrating the value of exploring patterns of variation for morphological phylogenetics and for the phylogenetic placement of fossils. Future osteological investigations on the species we examined and on species we did not examine will continue to augment our knowledge of patterns of variation in alligator lizards and aid in phylogenetics and fossil placement.

The power of community science to quantify ecological interactions in cities

Studying animals in urban environments is especially challenging because much of the area is private property not easily accessible to professional scientists. In addition, collecting data on animals that are cryptic, secretive, or rare is also challenging due to the time and resources needed to amass an adequate dataset. Here, we show that community science can be a powerful tool to overcome these challenges. We used observations submitted to the community science platform iNaturalist to assess predation and parasitism across urbanization gradients in a secretive, ‘hard-to-study’ species, the Southern Alligator Lizard (Elgaria multicarinata). From photographs, we quantified predation risk by assessing tail injuries and quantified parasitism by counting tick loads on lizards. We found that tail injuries increased with age and with urbanization, suggesting that urban areas are risky habitats. Conversely, parasitism decreased with urbanization likely due to a loss of hosts and anti-tick medications used on human companion animals. This community science approach generated a large dataset on a secretive species rapidly and at an immense spatial scale that facilitated quantitative measures of urbanization (e.g. percent impervious surface cover) as opposed to qualitative measures (e.g. urban vs. rural). We therefore demonstrate that community science can help resolve ecological questions that otherwise would be difficult to address.

A new distributional record for the Martin del Campo’s Arboreal Alligator Lizard (Abronia martindelcampoi) with comments on the biogeography of arboreal Alligator-lizards in the Sierra Madre del Sur, Mexico

ABSTRACT Alligator lizards of the genus Abronia are a clade of arboreal and terrestrial squamates distributed throughout much of the highlands of Mexico and Central America. Here, we report a new record of the Mexican endemic A. martindelcampoi that represents the easternmost limit of the species and the lowest known elevational record. We briefly discuss the biogeographical hypotheses that have been proposed in the past concerning this and other related genera.

Fossil pigmy rattlesnake inside the mandible of an American mastodon and use of fossil reptiles for the paleoclimatic reconstruction of a Pleistocene locality in Puebla, Mexico

Records of Pleistocene reptiles are relatively well known in different countries. However, reptile fossil records of Pleistocene from Latin America are scarce and limited to presence data associated with records of megafauna remains. Taphonomic studies in Pleistocene reptiles are focused on finding out the origin of the paleontological remains; that is, if the remains found at a particular place correspond to organisms that lived and died there or if they were carried out and deposited there by water currents or predators. Pleistocene reptiles have been used as a proxy for qualitative paleoclimatic reconstructions of localities. In this study, we describe the fossil record of squamate reptiles from the Pleistocene of San José Buenavista (Puebla, Mexico), and the taphonomic relationship between them and the associated megafauna, as well as reconstruct the paleoclimate of the paleontological site in Central Mexico where the remains were found. We present the first Mexican Pleistocene record of Anolis and Storeria, the third fossil record of the alligator lizard Barisia sp. in Mexico, and the first North American Pleistocene record for the rattlesnake Crotalus triseriatus. The rattlesnake (C. triseriatus) was found inside the mandible of the American mastodon (Mammut americanum). This finding suggests that the mastodon remains were used as burrow by the rattlesnake during the Pleistocene. Paleoclimate was reconstructed using the Mutual Ecogeographic Range method, which uses the distribution and climate niche of the nearest extant representatives of the identified fossil taxa. A mean annual temperature of 13.91 ± 1.54 °C and an annual precipitation of 964.04 ± 316.82 mm were inferred for the locality. This suggests that the assemblage of fossil species found inhabited the locality during a glacial period.

Enduring muscular courtship

Physiology Several species of male amphibians and reptiles hold tight to their partners, possibly to prevent them mating with their rivals. The southern alligator lizard ( Elgaria multicarinata ) clamps its mate's head in its jaws for hours. This extreme muscular performance runs counter to expectations of reptilian muscle resilience. Nguyen et al. tested the sustained bite force of the adductor muscles of the lizard's jaw for fatigue. Muscle fibers can specialize, in terms of performance, into fast-acting twitch fibers and into slow-acting tonic fibers that are capable of fatigue-resistant contraction. Tonic fibers also exhibit slow calcium fluxes and relax slowly. The lizards' jaw muscle appears to have evolved to comprise fast-twitch fibers for eating and slow-tonic fibers that can sustain an extended courtship grip. Proc. R. Soc. London Ser. B 287 , 20201578 (2020).

Fatigue resistant jaw muscles facilitate long-lasting courtship behaviour in the southern alligator lizard (Elgaria multicarinata)

The southern alligator lizard (Elgaria multicarinata) exhibits a courtship behaviour during which the male firmly grips the female's head in his jaws for many hours at a time. This extreme behaviour counters the conventional wisdom that reptilian muscle is incapable of powering high-endurance behaviours. We conducted in situ experiments in which the jaw-adductor muscles of lizards were stimulated directly while bite force was measured simultaneously. Fatigue tests were performed by stimulating the muscles with a series of tetanic trains. Our results show that a substantial sustained force gradually develops during the fatigue test. This sustained force persists after peak tetanic forces have declined to a fraction of their initial magnitude. The observed sustained force during in situ fatigue tests is consistent with the courtship behaviour of these lizards and probably reflects physiological specialization. The results of molecular analysis reveal that the jaw muscles contain masticatory and tonic myosin fibres. We propose that the presence of tonic fibres may explain the unusual sustained force properties during mate-holding behaviour. The characterization of muscle properties that facilitate extreme performance during specialized behaviours may reveal general mechanisms of muscle function, especially when done in light of convergently evolved systems exhibiting similar performance characteristics.

Response behaviour of native lizards and invading wall lizard to interspecific scent: implications for invasion success

The human-assisted movement of species beyond their native range facilitates novel interactions between invaders and native species that can determine whether an introduced species becomes invasive and the nature of any consequences for native communities. Avoiding costly interactions through recognition and avoidance can be compromised by the naivety of native species to novel invaders and vice versa. We tested this hypothesis using the common wall lizard, Podarcis muralis, and the native lizard species with which it may now interact in Britain (common lizard, Zootoca vivipara, sand lizard, Lacerta agilis) and on Vancouver Island (northern alligator lizard, Elgaria coerulea) by exploring species' responses (tongue flicks, avoidance behaviour) to heterospecific scent cues in controlled experiments. The tongue flick response of P. muralis depended on the different species’ scent, with significantly more tongue flicks directed to E. coerulea scent than the other species and the control. This recognition did not result in any other behavioural response in P. muralis (i.e. attraction, aggression, avoidance). Lacerta agilis showed a strong recognition response to P. muralis scent, with more tongue flicks occurring close to the treatment stimuli than the control and aggressive behaviour directed towards the scent source. Conversely, Z. vivipara spent less time near P. muralis scent cues than the control but its tongue flick rate was higher towards this scent in this reduced time, consistent with an avoidance response. There was no evidence of E. coerulea recognition of P. muralis scent in terms of tongue flicks or time spent near the stimuli, although the native species did show a preference for P. muralis-scented refuges. Our results suggest a variable response of native species to the scent of P. muralis, from an avoidance response by Z. vivipara that mirrors patterns of exclusion observed in the field to direct aggression observed in L. agilis and an ambiguous reaction from E. coerulea which may reflect a diminished response to a cue with a low associated cost. These results have significant implications for the invasive success and potential impacts of introduced P. muralis populations on native lizards.

RECENT RAPID EXPANSION OF COMMON WALL LIZARDS (PODARCIS MURALIS) IN BRITISH COLUMBIA, CANADA

The Common Wall Lizard (Podarcis muralis) has existed in southwestern British Columbia since 1967, but expanded its range rapidly in the last decade. In 2006, P. muralis was thought restricted to 4 populations on southeastern Vancouver Island: 3 on the Saanich Peninsula and 1 in the Triangle Mountain area. However, increased reporting and exploration led to the recognition that these populations have merged. Further, P. muralis have also appeared along the eastern side of Vancouver Island north to Campbell River; and on Denman Island. In 2015, P. muralis was also reported from two BC mainland locations: Osoyoos in the southern Okanagan, and the city of Vancouver. Introduced lacertid populations are reported to spread from their points of origin at a relatively slow rate (∼1 km every 10 y), so given that P. muralis has been found at least 200 km north, 300 km west, and from Vancouver Island to Denman Island and the British Columbia mainland over the last 52 y, human-assisted dispersal likely contributed to its apparently rapid radial expansion in southwestern BC. As they expand into rural and protected areas on Vancouver Island, P. muralis may have increasing opportunities to interact with the native Northern Alligator Lizard (Elgaria coerulea). Where E. coerulea and P. muralis coexist on southern Vancouver Island, the latter seems more abundant, which raises concern and warrants study.

The skull of the gerrhonotine lizard Elgaria panamintina (Squamata: Anguidae).

We provide the first description of the skull, osteoderms, and hyoid apparatus of the poorly known alligator lizard Elgaria panamintina, and compare the cranial osteology of that species to the widespread and well-studied taxon Elgaria multicarinata. Patterns of morphological variation resulting from ontogenetic transformations and pathology are discussed. We employed x-ray computed tomography (CT) scans to examine two adult specimens of Elgaria panamintina and two adult specimens of Elgaria multicarinata, in addition to examining multiple traditionally prepared skeletal specimens of the latter species. CT scans provide simultaneous study of both articulated and disarticulated elements, allowing us to describe and document the morphology of the skull with exceptional precision and detail. The description of the skull of Elgaria panamintina serves as a generalization for all Elgaria; here we provide the first complete description of the skull of this genus for future uses in morphological and phylogenetic studies of both extant species and fossils.