Squamate Reptiles Research Articles

Ecological factors and parity mode correlate with genome size variation in squamate reptiles

BackgroundEvidence of correlation between genome size, the nuclear haploid DNA content of a cell, environmental factors and life-history traits have been reported in many animal species. Genome size, however, spans over three orders of magnitude across taxa and such a correlation does not seem to follow a universal pattern. In squamate reptiles, the second most species-rich order of vertebrates, there are currently no studies investigating drivers of genome size variability. We run a series of phylogenetic generalized least-squares models on 227 species of squamates to test for possible relationships between genome size and ecological factors including latitudinal distribution, bioclimatic variables and microhabitat use. We also tested whether genome size variation can be associated with parity mode, a highly variable life history trait in this order of reptiles.ResultsThe best-fitting model showed that the interaction between microhabitat use and parity mode mainly accounted for genome size variation. Larger genome sizes were found in live-bearing species that live in rock/sand ecosystems and in egg-laying arboreal taxa. On the other hand, smaller genomes were found in fossorial live-bearing species.ConclusionsEnvironmental factors and species parity mode appear to be among the main parameters explaining genome size variation in squamates. Our results suggest that genome size may favour adaptation of some species to certain environments or could otherwise result from the interaction between environmental factors and parity mode. Integration of genome size and genome sequencing data could help understand the role of differential genome content in the evolutionary process of genome size variation in squamates.

Multiproxy approach to reconstruct the climate and environment of a new late Middle Pleistocene vertebrate site in northwestern Italy

The Moleto site (Ottiglio, AL, Piemonte, Italy) was discovered in the 1990s in an abandoned quarry carved into a Burdigalian–Langhian carbonate succession called Pietra da Cantoni. Sediment collection in three closely spaced fissures provided a rich vertebrate association whose age can be constrained to the late Middle Pleistocene on the basis of the presence of the extinct water vole Arvicola mosbachensis and its enamel characteristics (SDQ values ranging from 100 to 130). The very similar faunal content, evidenced by the common presence of Arvicola mosbachensis and its similar SDQ values, is indicative of a coeval deposition of the fillings of the three fissures. The vertebrate assemblage is represented by 30 taxa, including amphibians, squamate reptiles, birds, and mammals. Interestingly, a diverse fish assemblage from the embedded sediments of the Miocene Pietra da Cantoni has been found in the fissure fillings. We present here a multi-method approach using the small vertebrate assemblages (rodents, insectivores, amphibians, and squamate reptiles) from Moleto to characterize the environment and climate of the site. In order to reconstruct the palaeoenvironmental and palaeoclimatic conditions, we applied the Mutual Ecogeographic Range using UDA-ODA technique, the Bioclimatic Model, the Habitat Weightings, and the Quantified Ecology methods. The results revealed a landscape dominated by woodland habitats with presence of open humid meadows, under temperate and moist climatic conditions, although somewhat colder and drier than today. According to all evidence, the associations from Moleto would correspond to the interglacial MIS 7.

Corticosterone and immune responses to dehydration in squamate reptiles.

Many environments present some degree of seasonal water limitations; organisms that live in such environments must be adapted to survive periods without permanent water access. Often this involves the ability to tolerate dehydration, which can have adverse physiological effects and is typically considered a physiological stressor. While having many functions, the hormone corticosterone (CORT) is often released in response to stressors, yet increasing plasma CORT while dehydrated could be considered maladaptive, especially for species that experience predictable bouts of dehydration and have related coping mechanisms. Elevating CORT could reduce immunocompetence and have other negative physiological effects. Thus, such species likely have CORT and immune responses adapted to experiencing seasonal droughts. We evaluated how dehydration affects CORT and immune function in eight squamate species that naturally experience varied water limitation. We tested whether hydric state affected plasma CORT concentrations and aspects of immunocompetence (lysis, agglutination, bacterial killing ability and white blood cell counts) differently among species based on how seasonally water limited they are and whether this is constrained by phylogeny. The species represented four familial pairs, with one species of each pair inhabiting environments with frequent access to water and one naturally experiencing extended periods (>30 days) with no access to standing water. The effects of dehydration on CORT and immunity varied among species. Increases in CORT were generally not associated with reduced immunocompetence, indicating CORT and immunity might be decoupled in some species. Interspecies variations in responses to dehydration were more clearly grouped by phylogeny than by habitat type.

Design, Modeling, and Control of a Legless Squamate Reptiles Inspired Soft Crawling Robot

Design, Modeling, and Control of a Legless Squamate Reptiles Inspired Soft Crawling Robot

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.

Interspecific Comparison of Orthologous Short Interspersed Elements Loci Using Whole-Genome Data.

The polymorphism of SINE-containing loci reflects the evolutionary processes that occurred both during the period before the divergence of the taxa and after it. Orthologous loci containing SINE in two or more genomes indicate the relatedness of the taxa, while different copies may have a specific set of mutations and degree of difference. Polymorphic insertion can be interpreted with a high degree of confidence as a shared derived character in the phylogenetic reconstruction of the history of the taxon. The computational comparison of the entire set of SINE-containing loci between genomes is a challenging task, and we propose to consider it in detail using the genomes of representatives of squamate reptiles (lizards) as an example. Our approach allows us to extract copies of SINE from the genomes, find pairwise orthologous loci by using flanking genomic sequences, and analyze the resulting sets of loci for the presence or absence of SINE, the degree of similarity of the flanks, and the similarity of the SINE themselves. The workflow we propose allows us to efficiently extract and analyze orthologous SINE loci for the downstream analysis, as shown in our comparison of species- and genus-level taxa in lacertid lizards.

Squamate reptiles as indicators in fragments of Brazilian cerrado

ABSTRACT The data on the reptilian fauna of the state of Goiás are one-off and reveal a lack of information about this group. The aim of the research was to know the composition of the reptile fauna within the area of the Anglo American mining company, evaluating the relationship of the species with the years, the types of environments and the presence of indicator species. Fieldwork was carried out during seven years, from 2007 to 2013. Sampling was performed through active search, pitfall traps, occasional encounters, and third-party records. We recorded 36 reptile species: 15 lizards and 21 snakes. The most common lizards were Anolis meridionalis, Cnemidophorus sp, and the most abundant snakes were Apostolepis cerradoensis and Bothrops moojeni. There was no relationship between the species and the years. On the other hand, there was relationship between the species and the environments or between the species and the types of habitats. The lizard Ameivula ocellifera was found as an indicator species of Cerrado areas, as well as the snake Leptotyphlops dulcis We have seen that lizards are specific to their habitat, making it essential to preserve open and forested areas for the conservation of the species that live there.

Sexual dimorphism in skull size and shape of Laticauda colubrina (Serpentes: Elapidae).

Sexual dimorphism in size and shape is widespread among squamate reptiles. Sex differences in snake skull size and shape are often accompanied by intersexual feeding niche separation. However, allometric trajectories underlying these differences remain largely unstudied in several lineages. The sea krait Laticauda colubrina (Serpentes: Elapidae) exhibits very clear sexual dimorphism in body size, with previous studies having reported females to be larger and to have a relatively longer and wider head. The two sexes also differ in feeding habits: males tend to prey in shallow water on muraenid eels, whereas females prey in deeper water on congerid eels. I investigated sexual dimorphism in skull shape and size as well as the pattern of skull growth, to determine whether males and females follow the same ontogenetic trajectories. I studied skull characteristics and body length in 61 male and female sea kraits. The sexes differ in skull shape. Males and females follow distinct allometric trajectories. Structures associated with feeding performance are female-biased, whereas rostral and orbital regions are male-biased. The two sexes differ in allometric trajectories of feeding-related structures (female biased) that correspond to dietary divergence between the sexes. Sea kraits exhibit clear sexual dimorphism in the skull form that may be explained by intersexual differences in the feeding habits as well as reproductive roles. The overall skull growth pattern resembles the typical pattern observed in other tetrapods.

Dazzle: surface patterns that impede interception

Abstract ‘Dazzle coloration’ describes a wide variety of high-contrast patterns allegedly providing protection against attack during motion. Previous research falls into three broad groups. First, studies using humans demonstrate that certain surface patterns can cause significant misperceptions in controlled laboratory conditions, although the effects are inconsistent in both direction and magnitude. Second, experiments on target capture or tracking also show effects that are strongly dependent upon the test paradigm. It has not been established that these laboratory findings generalize to other species, or to the real world. Third, mainly comparative studies build a case for longitudinal striping being involved in escape strategies in some squamate reptiles. We suggest that: (1) the concept of dazzle conflates a description of appearance with presumed function; (2) some effects attributed to dazzle have not been distinguished clearly from other mechanisms of protective coloration; and (3) confusion persists over the evidence necessary to attribute a dazzle function to markings. We refine the definition of dazzle to exclude appearance: dazzle is coloration that interferes with target interception, as a result of misperception of its speed, trajectory and/or range. Our review clarifies discussion of dazzle, and sets out a coherent and practical framework for future research.

Geographical and ecological drivers of coexistence dynamics in squamate reptiles

AbstractAimSpecies richness varies widely across space and is determined by underlying factors that drive species coexistence. Such factors include the speciation process (sympatric vs. allopatric), time since divergence, geographic context and intrinsic properties of the organisms. We model for the first time the coexistence dynamics of lizards and snakes across broad temporal and spatial scales, investigating whether an increase in niche divergence, dispersal abilities and inhabiting islands or continents affect their probability of coexistence.LocationGlobal.Time periodCenozoic.Major taxa studiedSquamata.MethodsWe used 447 sister species pairs, their age since divergence, their level of spatial (sympatric or allopatric) and niche overlap and geographical setting (islands or continents) to fit probabilistic models of species coexistence. We measured morphological traits to quantify niche divergence and used range and body size as proxies for dispersal ability. We applied a model‐comparison framework in lizards and snakes separately to evaluate which factors best explained their coexistence dynamics.ResultsAllopatric speciation is the main speciation mode in snakes but we did not find evidence to favour one speciation mode in lizards. In snakes, sympatric pairs tend to occur on islands and to be more different in body size. On the contrary, dispersal ability shaped the coexistence of lizards, where species were more likely to coexist when they have higher dispersal abilities.Main conclusionsDistinct patterns and mechanisms underlie species coexistence within the order Squamata. Snake coexistence is preferentially produced by secondary sympatry favoured by niche divergence and is more likely to occur in more restricted geographical settings (islands vs. continents). Coexistence in lizards is strongly influenced only by dispersal abilities, but the high heterogeneity of processes simultaneously shaping the distribution of different lizard lineages might have masked specific coexistence signals, and future work should compare coexistence dynamics between clades (e.g. families).

Anatomy of the female reproductive tract organs of the brown anole (Anolis sagrei).

Female reproduction in squamate reptiles (lizards and snakes) is highly diverse and mode of reproduction, clutch size, and reproductive tract morphology all vary widely across this group of ~11,000 species. Recently, CRISPR genome editing techniques that require manipulation of the female reproductive anatomy have been developed in this group, making a more complete understanding of this anatomy essential. We describe the adult female reproductive anatomy of the model reptile the brown anole (Anolis sagrei). We show that the brown anole female reproductive tract has three distinct anterior-to-posterior regions, the infundibulum, the glandular uterus, and the nonglandular uterus. The infundibulum has a highly ciliated epithelial lip, a region where the epithelium is inverted so that cilia are present on the inside and outside of the tube. The glandular uterus has epithelial ducts that are patent with a lumen as well as acinar structures with a lumen. The nonglandular uterus has a heterogeneous morphology from anterior to posterior, with a highly folded, ciliated epithelium transitioning to a stratified squamous epithelium. This transition is accompanied by a loss of keratin-8 expression and together, these changes are similar to the morphological and gene expression changes that occur in the mammalian cervix. We recommend that description of the nonglandular uterus include the regional sub-specification of a "cervix" and "vagina" as this terminology change more accurately describes the morphology. Our data extend histological studies of reproductive organ morphology in reptiles and expand our understanding of the variation in reproductive system anatomy across squamates and vertebrates.

Efficient and highly continuous chromosome-level genome assembly of the first chameleon genome.

Most amniote genomes are diploid, moderate in size (approximately 1-6 Gbp), and contain a large proportion of repetitive sequences. The development of next-generation sequencing technology, especially the emergence of high-fidelity (HiFi) long-read data, has made it feasible to resolve high-quality genome assembly for non-model species efficiently. However, reference genomes for squamate reptiles has lagged behind other amniote lineages. Here we de novo assembled the first genome from the Chameleonidae family, the panther chameleon (Furcifer pardalis). We obtained telomere-to-telomere contigs using only HiFi data, reaching a contig N50 of 158.72 Mbp. The final chromosome-level assembly is 1.61 Gbp in size and 100% of primary contigs were placed to pseudochromosomes using Hi-C interaction data. We also found that sequencing depth > 30 folds can ensure both the integrity and accuracy of the genome, while insufficient depth led to false increase in genome size and proportion of duplicated genes. We provide a high-quality reference genome valuable for evolutionary and ecological studies in chameleons as well as providing comparative genomic resources for squamate reptiles.

Herpetological records from the Abujao basin, central Peruvian Amazon

The effort to uncover herpetofauna within the zone of influence of the Sierra del Divisor National Park has been focused on the northern reaches. The Abujao basin represents the Sierra del Divisor region well in an understudied area central to the Peruvian Amazon. We found 108 species of amphibians and squamate reptiles. Seven records extend ranges from the northern regions, while two records unite with southern regions (Madre De Dios and the Fitzcarrald Arc/Purus valley). There are higher levels of diversity attributable to land-cover units indicative of high terraces and hilly zones, as opposed to low hydromorphic habitats. Our new record for Pristimantis iiap Padial, Gagliardi-Urrutia, Chaparro & Gutiérrez, 2016 brings more resolution to this newly described species. We made observations of an unidentified species of blindsnake, which could represent a unique part of the fauna. Despite variations, we only uphold the presence of various subspecies of Micrurus annellatus Peters, 1871.

Squamates, rodents, and birds from Holocene deposits of the Illa Grossa Island (Columbretes Islands, Castellón, Spain): an unexpected diverse assemblage

The Columbretes Islands (eastern Spain) comprise a volcanic archipelago 50 km off the eastern Spanish coast. Illa Grossa is the main island of the archipelago. After the settlement of humans during the mid-19th century, strong modifications in biodiversity took place, including the reduction of the non-flying vertebrate fauna to a single taxon, Podarcis liolepis atratus (Boscá, 1916). The study of the fossils yielded at the COLT site (dated by AMC between 2780-2724 cal BP and 2600-2492 cal BP) from a loess deposit located at the south of Illa Grossa Island shows that this fauna was more diverse in the past. The assemblage was dominated by squamate reptiles, belonging to two lizards (Chalcides bedriagai (Boscá, 1880) and cf. Podarcis Wagler, 1830) and one snake (Vipera cf. latastei Boscá, 1878). The record in the late Holocene of Columbretes of Vipera cf. latastei settles the existing controversy about the identity of snakes in the archipelago. Regarding Chalcides bedriagai, this is the first record of its presence in the Columbretes Islands. Other faunal elements recovered from the site include at least six species of undetermined birds (passeriforms and procellariforms) and the anthropophilic Mus cf. musculus Linnaeus, 1758. The origin of the squamates taxa from Columbretes palaeontological site (COLT) is still unclear, but was probably related to the Late Pleistocene-Greenlandian (11 700 to 8300 BP, Early Holocene) sea transgression, natural passive colonization, and/or human introduction. We hypothesize implications for the conservation and management of the Natural Reserve.

Developmental regulation of conserved non-coding element evolution provides insights into limb loss in squamates.

Limb loss shows recurrent phenotypic evolution across squamate lineages. Here, based on three de novo-assembled genomes of limbless lizards from different lineages, we showed that divergence of conserved non-coding elements (CNEs) played an important role in limb development. These CNEs were associated with genes required for limb initiation and outgrowth, and with regulatory signals in the early stage of limb development. Importantly, we identified the extensive existence of insertions and deletions (InDels) in the CNEs, with the numbers ranging from 111 to 756. Most of these CNEs with InDels were lineage-specific in the limbless squamates. Nearby genes of these InDel CNEs were important to early limb formation, such as Tbx4, Fgf10, and Gli3. Based on functional experiments, we found that nucleotide mutations and InDels both affected the regulatory function of the CNEs. Our study provides molecular evidence underlying limb loss in squamate reptiles from a developmental perspective and sheds light on the importance of regulatory element InDels in phenotypic evolution.

Geographical and ecological drivers of coexistence dynamics in squamate reptiles

Geographical and ecological drivers of coexistence dynamics in squamate reptiles

Semicircular canal shape diversity among modern lepidosaurs: life habit, size, allometry

BackgroundThe shape of the semicircular canals of the inner ear of living squamate reptiles has been used to infer phylogenetic relationships, body size, and life habits. Often these inferences are made without controlling for the effects of the other ones. Here we examine the semicircular canals of 94 species of extant limbed lepidosaurs using three-dimensional landmark-based geometric morphometrics, and analyze them in phylogenetic context to evaluate the relative contributions of life habit, size, and phylogeny on canal shape.ResultsLife habit is not a strong predictor of semicircular canal shape across this broad sample. Instead, phylogeny plays a major role in predicting shape, with strong phylogenetic signal in shape as well as size. Allometry has a limited role in canal shape, but inner ear size and body mass are strongly correlated.ConclusionsOur wide sampling across limbed squamates suggests that semicircular canal shape and size are predominantly a factor of phylogenetic relatedness. Given the small proportion of variance in semicircular canal shape explained by life habit, it is unlikely that unknown life habit could be deduced from semicircular canal shape alone. Overall, semicircular canal size is a good estimator of body length and even better for body mass in limbed squamates. Semiaquatic taxa tend to be larger and heavier than non-aquatic taxa, but once body size and phylogeny are accounted for, they are hard to distinguish from their non-aquatic relatives based on bony labyrinth shape and morphology.

Adrenergic control of functional characteristics of the cardiovascular system in the South American rattlesnake, Crotalus durissus

In squamate reptiles, extensive innervation of the heart and vascular beds allows for continuous modulation of the cardiovascular system by the autonomic nervous system. The systemic vasculature is the main target of excitatory sympathetic adrenergic fibers, while the pulmonary circulation has been described as less responsive to both nervous and humoral modulators. However, histochemical evidence has demonstrated the presence of adrenergic fibers in pulmonary circulation. Besides, reduced responsiveness is intriguing since the balance of regulation between systemic and pulmonary vascular circuits has critical hemodynamic implications in animals with an undivided ventricle and consequent cardiovascular shunts. The present study investigated the role and functional relevance of α and β-adrenergic stimulation in regulating systemic and mainly the pulmonary circulations in a decerebrate, autonomically responsive rattlesnake preparation. The use of the decerebrate preparation allowed us to observe a new diverse functional modulation of vascular beds and the heart. In resting snakes, the pulmonary vasculature is less reactive to adrenergic agonists at 25 °C. However, the β-adrenergic tone is relevant for modulating resting peripheral pulmonary conductance, while both α- and β-adrenergic tones are relevant for the systemic circuit. Active dynamic modulation of both pulmonary compliance and conductance effectively counterbalances alterations in the systemic circulation to maintain the R-L shunt pattern. Furthermore, we suggest that despite the great attention given to cardiac adjustments, vascular modulation is sufficient to support the hemodynamic adjustments needed to control blood pressure.

Embryonic development of the skull in a parthenogenetic lizard, the mourning gecko (Lepidodactylus lugubris).

Gekkotans are one of the major clades of squamate reptiles. As one of the earliest-diverging lineages, they are crucial in studying deep-level squamate phylogeny and evolution. Developmental studies can shed light on the origin of many important morphological characters, yet our knowledge of cranial development in gekkotans is very incomplete. Here, we describe the embryonic development of the skull in a parthenogenetic gekkonid, the mourning gecko (Lepidodactylus lugubris), studied using non-acidic double staining and histological sectioning. Our analysis indicates that the pterygoid is the first ossifying bone in the skull, as in almost all other studied squamates, followed closely by the surangular and prearticular. The next to appear are the dentary, frontal, parietal and squamosal. The tooth-bearing upper jaw bones, the premaxilla and maxilla, develop relatively late. In contrast to previous reports, the premaxilla starts ossifying from two distinct centres, reminiscent of the condition observed in diplodactylids and eublepharids. Only a single ossification centre of the postorbitofrontal is observed. Some of the endochondral bones of the braincase (prootic, opisthotic, supraoccipital) and the dermal parasphenoid are the last bones to appear. The skull roof is relatively poorly ossified near the time of hatching, with a large frontoparietal fontanelle still present. Many bones begin ossifying relatively later in L. lugubris than in the phyllodactylid Tarentola annularis, which suggests that its ossification sequence is heterochronic with respect to T. annularis.

Scaling of erythrocyte shape and nucleus size among squamate reptiles: reanalysis points to constrained, proportional rather than adaptive changes.

Small erythrocytes might be beneficial for blood rheology, as they contribute less to blood viscosity than large erythrocytes. We predicted that rheological disadvantages of larger erythrocytes could be alleviated by relatively smaller nucleus size in larger cells allowing higher flexibility and by more elongated shape. Across squamate reptiles, we found that species with larger erythrocytes tend to have smaller ratio of nucleus size to cell size (N : C ratio), but that larger erythrocytes tend to be rounder, not more elongated. Nevertheless, we document that in fact nucleus area changes with erythrocyte area more or less linearly, which is also true for the relationship between cell length and cell width. These linear relationships suggest that nucleus size and cell size, and cell width and cell length, might be constrained to largely proportional mutual changes. The shifts in widely used N : C ratio and elongation ratio (cell length/cell width) with cell size might be misleading, as they do not reflect adaptive or maladaptive changes of erythrocytes, but rather mathematically trivial scaling of the ratios of two variables with a linear relationship with non-zero intercepts. We warn that ratio scaling without analyses of underlying patterns of evolutionary changes can lead to misinterpretation of evolutionary processes.