Lacertid Research Articles

Walking or hanging: the role of habitat use for body shape evolution in lacertid lizards.

Differences in habitat use impose ecological constraints which in turn lead to functional and morphological differences through adaptation. In fact, a convergent evolutionary pattern is evident when species exhibit similar responses to similar environments. In this study we examine how habitat use influences the evolution of body shape in lizards from the family Lacertidae. We divided our species set into two categories: ground-dwellers and climbers, which encompasses the verticality and horizontality aspects of the habitat. We performed phylogenetic comparative analyses employing 186 species and seven linear morphological traits. Our results show contrasting patterns between head and limb shape, which are considered distinct functional blocks. We observed differences in forelimb proportions, but not in hindlimb length, contrary to what was documented in other lizard groups, demonstrating a novel axis in the limb-locomotion-habitat relationship in this family. In addition, a clear effect of habitat use on head shape was detected. We observed that climbing species present on average flatter heads than ground-dwelling species, as well as different evolutionary trajectories. These findings suggest the complex interplay between habitat use and morphological evolution in lizards, highlighting how distinct selective pressures drive divergent adaptations in different functional traits.

Comparing Preferred Temperatures and Evaporative Water Loss Rates in Two Syntopic Populations of Lacertid Lizard Species.

Many reptiles actively regulate their body temperature. During thermoregulation, they suffer evaporative water loss (EWL). Since evaporation increases with temperature, EWL could limit the activity of ectotherms when water is not available. In this study, we compared the preferred body temperatures (Tp) and EWL of two lacertid lizard species, Darevskia praticola and Podarcis muralis, at the western edge of D. praticola's range, where they live in syntopy. We hypothesized that D. praticola, a species that inhabits forested and humid environments, would have a higher EWL than the more widespread P. muralis. Our results show that D. praticola prefers lower temperatures (mean Tp = 28.1 °C) than P. muralis (mean Tp = 30.6 °C). Despite the differences in their thermal preferences, both species showed similar total EWL (2.76% for D. praticola and 2.67% for P. muralis), although their daily patterns of water loss differed. Our results suggest that D. praticola has developed mechanisms to control water loss and that its lower thermal preference may be due to both historical factors and local adaptations. These results contribute to the understanding of how environmental factors influence the physiology of lizards, which in turn has implications for predicting the effects of climate change on species distribution.

Spatiotemporal distribution of neural crest cells in the common wall lizard Podarcis muralis.

Neural crest cells (NCCs) are migratory embryonic stem cells that give rise to a diverse set of cell types. Here we describe the dynamic distribution of NCCs in developing embryos of the common wall lizard Podarcis muralis inferred from 10 markers. Our aim is to provide insights into the NCC development of lacertid lizards and to infer evolutionary modifications by comparisons to other tetrapods. NCC migration is ongoing at oviposition, following three streams in the head and multiple in the trunk. From 21ss, we observe expression patterns indicating the beginning of differentiation toward mesenchymal and neuronal fates. By 35ss, migration is restricted to caudal levels, and fully differentiated chromaffin cells are observed. We find that some markers show patterns that differ from other tetrapods. For example, the antibody HNK-1 labels three NCC streams from the hindbrain while some comparable reptile studies describe four. However, the information emerging from all markers combined shows that the overall spatiotemporal distribution of NCCs in the common wall lizard is largely conserved with that of other tetrapods. Our study highlights the dynamic nature of seemingly canonical marker genes and provides the first description of spatiotemporal NCC dynamics in a lacertid lizard.

The first lacertid and partly articulated snake from the Middle Miocene of the Devínska Kobyla Hill in Slovakia, from the type locality of the earliest known seal

I here describe lacertid and snake remains from the classic Middle Miocene (MN 6) locality Bonanza of the Devínska Kobyla Hill near Bratislava (Slovakia). The locality is famous for being a type locality of an early seal Devinophoca Koretsky & Holec, 2002. During the Middle Miocene, the area of Devínska Nová Ves was part of an archipelago in the western part of the Central Paratethys in the northern part of the Vienna basin. The fossils described here comprise an incomplete left maxilla of a lacertid lizard and an articulated portion of a vertebral column of a small colubrid snake with several ribs still attached. The maxilla is tentativelly allocated here to Lacerta Linnaeus, 1758 and is a rare instance of the occurrence of the clade Lacertidae Oppel, 1811 in this environment during the Middle Miocene. Moreover, it represents the oldest known occurence of this clade in Slovakia. Articulated snake specimens from the Cenozoic are rare and although only party articulated, the specimen from Bonanza is therefore exceptional. On the basis of vertebrae alone, determination of fossil colubrids is very difficult. The morphology of the Bonanza specimen is most similar to the extant Dolichophis Gistel, 1868, as also to other small fossil snakes assigned to ‘Coluber’ Linnaeus, 1758 when that genus was a catch-all grade taxon recognised from both Europe and North America, notably ‘Coluber’ dolnicensis Szyndlar, 1987 and ‘Coluber’ pouchetii (Rochebrune, 1880). Because the potentially closest living relative of the European Miocene ‘Coluber’ is Dolichophis, I assigned tentatively the material from Bonanza to cf. Dolichophis, rather than to the wastebasket taxon ‘Coluber’.

Analysis of subcellular energy metabolism in five Lacertidae lizards across varied environmental conditions

Aerobic respiration is the main energy source for most eukaryotes, and efficient mitochondrial energy transfer greatly influences organismal fitness. To survive environmental changes, cells have evolved to adjust their biochemistry. Thus, measuring energy metabolism at the subcellular level can enhance our understanding of individual performance, population dynamics, and species distribution ranges. We investigated three important metabolic traits at the subcellular level in five lacertid lizard species sampled from different elevations, from sea level up to 2000 m. We examined hemoglobin concentration, two markers of oxidative stress (catalase activity and carbonyl concentration) and maximum rate of metabolic respiration at the subcellular level (potential metabolic activity at the electron transport system). The traits were analysed in laboratory acclimated adult male lizards to investigate the adaptive metabolic responses to the variable environmental conditions at the local sampling sites. Potential metabolic activity at the cellular level was measured at four temperatures – 28 °C, 30 °C, 32 °C and 34 °C – covering the range of preferred body temperatures of the species studied. Hemoglobin content, carbonyl concentration and potential metabolic activity did not differ significantly among species. Interspecific differences were found in the catalase activity, Potential metabolic activity increased with temperature in parallel in all five species. The highest response of the metabolic rate with temperature (Q10) and Arrhenius activation energy (Ea) was recorded in the high-mountain species Iberolacerta monticola.

Microplastic accumulation in a lizard species: Observations from the terrestrial environments

Microplastics are a global environmental problem, polluting both aquatic and terrestrial environments. Terrestrial lizards are suitable model organisms to study human-induced pollution in these areas, as they can live in urbanized areas where microplastics are most abundant. Therefore, we analyzed the prevalence of microplastics (MPs) in a common Lacertid lizard, the snake-eyed lizard, Ophisops elegans. We detected MPs in the gastrointestinal tract (GIT) of 33 of 152 specimens from 18 populations. The detected MPs had six distinct polymer compositions, namely Polyethylene terephthalate, Polyacrylonitrile, Polypropylene, Polyethylene, Poly methyl methacrylate and Polyamide. The majority of these MPs were fiber-type and the dominant color was navy blue. The lengths of MPs varied from 37 to 563 μm, with an average length of 175 μm. MPs were detected in the GITs of 43% of juveniles (n = 7), 30% of males (n = 105), and 18% of females (n = 40), with a mean of 0.27 per specimen. Furthermore, we found that microplastic densities varied with habitat distance from human settlements, supporting the theory that high levels of microplastic contamination are associated with extensive anthropogenic activity.

Variability in personalities at sex, population, and taxon-levels in two European lacertid lizards

Variability in personalities at sex, population, and taxon-levels in two European lacertid lizards

Initial orientation and homing performances in the lacertid lizard Podarcis siculus

Homing abilities of lizards after experimental dislocations have been found to be well developed in several species. Following our preliminary findings in Podarcis siculus, the present paper reports a new series of experiments on homing performances and initial orientation behaviour upon release. For this purpose, three series of releases were performed at increasing distances from the home areas in which the lizards were captured (range 85–245 m). In each series, two groups of lizards were released: the route-based visual cues during displacement were denied to one of them (NVIS), but allowed for the other (YVIS). The results of initial orientation showed that both are significantly homeward oriented at all three distances tested. Male and female YVIS and female NVIS are similarly homeward oriented, while the male NVIS are not. All 74 lizards successfully returned to their respective home areas. Eleven lizards homed on the same day they were released, while most of them homed during the 1st day after release (n = 51) and the rest on the 2nd day (n = 12). The different transport treatments did not influence homing success at the different distances tested. These results seem to support the use of a geocentric pilotage strategy to re-enter home from the release spot. Alternatively, the possibility that P. siculus use a sun compass and a mosaic map to find their way home is also discussed.

Satellite DNA supports the monophyly of Lacertibaenia (Amphisbaenia and Lacertidae) in squamate phylogeny

Lacertid and amphisbaenian lizards are two squamate reptile lineages very divergent morphologically. In fact, adaptation to burrowing deeply modified amphisbaenian worm-like body. Lacertids instead have a typical reptile morphology with a long tail and four well-developed limbs. Despite so different in appearance, they are evolutionarily very close as evidenced by molecular phylogenetic approaches. Consistently, a slow-evolving satellite DNA (IMO-TaqI) described in lacertid lizards was isolated from the genome of the amphisbaenian Trogonophis wiegmanni too. Comparison with lacertid repeats evidenced great similarity, highlighting that molecular characters appeared very suitable especially when morphology is subjected to strong selective pressures.

Vertebrate Pollination of Angiosperms in the Mediterranean Area: A Review.

For a long time, it was considered that entomogamy was the only pollination mechanism in the Mediterranean area. However, data recorded in this review prove that ornithogamy and saurogamy also take place. With the exception of the nectarivorous Cinnyris osea (Nectariniidae) which pollinates the mistletoe Picosepalus acaciae in Israel, all birds responsible for the pollination of several plant species in this area are primarily insectivorous, sedentary, or migrating passerine birds, particularly Sylvia atricapilla, S. melanocephala, Phylloscopus collibita and Parus caeruleus. They contribute, together with insects, to the pollination of Anagyris foetida, three species of Scrophularia with big flowers, Rhamnus alaternus, Brassica oleracea, and some other plants. The lacertid lizard Podarcis lilfordi acts as a pollinating agent on several W Mediterranean islands, where it effectively pollinates Euphorbia dendroides, Cneorum tricocum, and presumably Rosmarinus officinalis and Chrithmum maritimum. The flowers of some other plant species are visited by birds or by Podarcis species in the Mediterranean area, where they could also contribute to their pollination.

Social display in the Curaçao Whiptail (Cnemidophorus murinus Laurenti)

Three teiid species (Squamata: Teiidae) are endemic to the ABC islands (Aruba, Bonaire, and Curaçao) of the former Netherlands Antilles: the Aruba Whiptail (Cnemidophorus arubensis) of Aruba, the Bonaire Whiptail (C. ruthveni) of Bonaire and Klein-Bonaire, and the Curaçao Whiptail (C. murinus) of Curaçao and Klein-Curaçao. Before now, social displays have been described only for one of these three species: C. ruthveni (Baird et al. 2003). All three species engage in an arm-waving display that involves forelimb circumduction (Baird et al. 2003; van Buurt 2005; van Buurt 2011), which conveys social signals to conspecifics in some iguanian and lacertid lizard species (Carpenter et al. 1970; Verbeek 1972; Mitchell 1973). However, this behavior in the ABC island species of Cnemidophorus has not been shown to have a social function (Baird et al. 2003). Instead, experimental evidence demonstrates that in C. ruthveni it functions as a pursuit deterrent display that is performed in response to approaching humans, whom the lizard may view as potential predators (Cooper et al. 2004), although there are not yet any published reports of C. ruthveni performing the display in response to the approach of a non-human predator. My observations and those of others (van Buurt 2011) also confirm that in C. arubensis the display is performed in response to approaching humans.

Climate-driven mitochondrial selection in lacertid lizards.

The mitochondrion, which is an intracellular organelle responsible for most of the energy-producing pathways, can have its genome targeted for climate-driven selection. However, climate-driven mitochondrial selection remains a sparsely studied area in reptiles. Here, we reported the complete mitochondrial genome sequence of a lacertid lizard (Takydromus intermedius) and used mitogenomes from 54 species of lacertid lizards to study their phylogenetic relationships and to identify the mitochondrial genes under positive selection by climate. The length of the complete mitochondrial genome sequence of T. intermedius was 17,713 bp, which was within the range of lengths (17,224-18,943) ever reported for Takydromus species. The arrangement of mitochondrial genes in T. intermedius was the same as in other congeneric species. The 54 lacertid species could be divided into three geographically and climatically different clades. We identified three mitochondrial genes (ATP6, ATP8, and ND3) under positive selection by climate, and found that isothermality, temperature seasonality, precipitation of wettest month, and precipitation seasonality were the most important climatic variables contributing to the gene selection.

Speciation in the Iranian plateau: Molecular phylogeny and evolutionary history of the Persian long‐tailed desert lizard

AbstractMesalina watsonana is a well‐known species of small lacertid lizards with an extensive species distribution that exhibits high genetic diversity. The species has a wide distribution range in Iran, some parts of Turkmenistan, Afghanistan, Pakistan, and northwest India. This study aims to generate phylogenetic and phylogeographic evidence to derive taxonomic recommendations supporting. Furthermore, this species can be used as a model for examining Iranian Platuea's historical biogeography. We conducted a very detailed sampling of its distribution and used genetic approaches. Phylogenetic analyses were done implementing two mitochondrial (Cytb and 16S) and one nuclear (C‐mos) gene fragments. Combination of these results indicated that seven well‐supported distinct clades exist within this species complex, i.e. Kerman clade, Esfarayen clade, Halil clade, Ardestan clade, M. watsonana clade, Bardaskan Clade, and Khuzestan Clade in Iran. Also, our results revealed that several distinct clades diverged due to geologic events when the Dasht‐e‐Kavir and the Zagros Mountains were formed. It seems that the ancestor of M. watsonana spread to Iranian Plateau before the formation of the Zagros Mountains. Orogenic activities of the Zagros Mountains and the formation of deserts have influenced the separation of these lineages from the Late Miocene by allopatric speciation. Generally, our findings suggest that each of the seven clades corresponding to distinct geographic regions deserves to be elevated to the species level.

Habitat turnover in Iberian and Italian lizards: Is it climatically, spatially, or phylogenetically determined?

AbstractThe Mediterranean peninsulas host rich assemblages of lizards, but little is known about the factors that limit their habitat use on large spatial scales. In this study, we investigated the variation in habitat use of 29 species of lacertid lizards on the Iberian and Italian peninsulas and the transitional region of southeastern France. We investigated whether the types of habitat used were phylogenetically determined or, in contrast, were more influenced by spatial or climatic effects. We characterized the vegetal composition of 483 habitats used by lacertids and estimated the contribution of each component to habitat variability using distance‐based redundancy analysis. We showed that overall turnover patterns were determined similarly in both peninsulas, despite differences in the composition of the lacertid assemblages. The aridity‐related component dominated over the phylogenetic one, which has a weak influence in both regions. The species showed different turnover patterns, being low in those present in cold alpine habitats and shrub‐steppe specialists. In some Iberian endemics, habitat turnover occurs within relatively homogeneous climatic bands. However, in the Italian species, habitat turnover has a comparatively stronger climatic component, suggesting lower climatic specialization. This study shows that species distributions across habitats provide information to assess community properties and can be applied to explore differences among faunal assemblages over large geographic areas. Our results provide evidence that beta diversity can play a key role in structuring patterns of habitat turnover.

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.

Chromosome evolution in Iberolacerta, a genus that deviates from the standard karyotype formula of Lacertidae

This paper describes the preparation of flow-sorted chromosome paints from the Iberian Rock lizard Iberolacerta monticola, exemplifying their subsequent use in cross-species comparisons of chromosome painting. We carried out comparative analyses of chromosome evolution in the congeneric species I. galani and I. bonnali, as well as in two other species of Lacertini (Lacerta schreiberi and Timon lepidus) whose sex chromosomes were also studied through comparative genomic hybridization. Most species of Lacertini possess a diplod number of 2n = 38, with 36 acrocentric macrochromosomes and 2 microchromosomes. However, the nine species included in the genus Iberolacerta do not possess microchromosomes. Furthermore, very conspicuous differences from the standard Lacertini karyotype were observed in the three Pyrenean species of this genus, which included several biarmed metacentrics and a Z1Z2W multiple sex-chromosome system. With the possible exception of L. schreiberi, all the species of the family Lacertidae described to date appear to share homologous Z chromosomes, which date back to the last common ancestor of the whole group. We provide conclusive evidence that L. schreiberi should no longer be considered an exception to this rule, and demonstrate that the loss of microchromosomes in Iberolacerta was produced by their fusion to a middle-sized chromosome. Furthermore, we show that the multiple sex-chromosome system of the Pyrenean species of Iberolacerta originated from the fusion of the ancestral W chromosome with one of the shortest autosomes, and provide additional evidence of the fast evolution of DNA sequences linked to the W chromosome in Lacertini.

Differential recovery ability from infections by two blood parasite genera in males of a Mediterranean lacertid lizard after an experimental translocation.

Different blood parasites can co-infect natural populations of lizards. However, our knowledge of the host's ability to recover from them (i.e., significantly reduce parasitemia levels) is scarce. This has interest from an ecological immunology perspective. Herein, we investigate the host recovery ability in males of the lizardPsammodromus algirus infected by parasite genera Schellackia and Karyolysus. The role of lizard hosts is dissimilar in the life cycle of these two parasites, and thus different immune control of the infections is expected by the vertebrate host. As Schellackia performs both sexual and asexual reproduction cycles in lizards, we expect a better immune control by its vertebrate hosts. On the contrary, Karyolysus performs sexual reproductive cycles in vectors, hence we expect lower immune control by the lizards. We carried out a reciprocal translocation experiment during the lizards' mating season to evaluate both parasitemia and leukocyte profiles in male lizards, being one of the sampling plots close to a road with moderate traffic. These circumstances provide a combination of extrinsic (environmental stress) and intrinsic factors (reproductive vs. immune trade-offs) that may influence host's recovery ability. We recaptured 33% of the lizards, with a similar proportion in control and translocated groups. Karyolysus infected 92.3% and Schellackia 38.5% of these lizards. Hosts demonstrated ability to significantly reduce parasitemia of Schellackia but not of Karyolysus. This suggests, in line with our predictions, a differential immune relationship of lizards with these parasites, at time that supports that parasites with different phylogenetic origins should be analyzed separately in investigations of their effects on hosts. Furthermore, lizards close to the road underwent a stronger upregulation of lymphocytes and monocytes when translocated far from the road, suggesting a putative greater exposure to pathogens in the latter area.

Sex-Linked Loci on the W Chromosome in the Multi-Ocellated Racerunner (Eremias multiocellata) Confirm Genetic Sex-Determination Stability in Lacertid Lizards.

The multi-ocellated racerunner, Eremias multiocellata, was considered to have temperature-dependent sex determination (TSD), as its sex ratio can be influenced at different temperatures. However, such an observation contrasts with recent findings that suggest TSD is less common than previously thought. Here, a genotyping-by-sequencing (GBS) approach was employed to identify sex-linked markers in the E. multiocellata, for which the mechanism choice of TSD or GSD is still controversial. We preliminarily identified 119 sex-linked markers based on sex-associated sex-specific sequences, 97% of which indicated female heterogamety. After eliminating the false positives, 38 sex-linked markers were recognized, all of which showed the ZW/ZZ system. Then, eight of the novel markers were verified by PCR amplification from 15 populations of E. multiocellata, which support the GSD in E. multiocellata without geographic variation. To test the conservation of sex chromosome in Eremias, the eight markers were further cross-tested by PCR amplification in 10 individuals of the Mongolian racerunner (Eremias argus), two of which exhibited cross-utility. The novel sex-linked markers could be mapped on the W chromosome of the sand lizard (Lacerta agilis). Our finding that the sex-linked markers are shared in closely related species, along with a conserved synteny of the W chromosome, further supports the homology and conservation of sex chromosomes in the lacertid lizards.

Sexual Selection and Proteinaceous Diversity in the Femoral Gland Secretions of Lacertid Lizards

Sexual selection contributes to the diversity of chemical signals in various animal groups. Lizards are good model species to study how sexual selection shapes signal diversity, as they are a chemically oriented taxonomic group with different levels of social interactions. Many lizard species bear epidermal glands secreting a waxy mixture of lipids and proteins, which are used in intraspecific communication. Previous among-species comparative analyses failed to find a relationship between the strength of sexual selection with the composition of the lipid blend in lizards. Here, we extend the investigation to the proteinaceous fraction. By using a phylogenetically informed approach, we correlated the average electrophoretic profiles of the protein from the femoral glands of 36 lacertid lizard species with the level of sexual dimorphism in size and shape, which are proxies for the strength of sexual selection. We found that as sexual size dimorphism advances, five distinct molecular weight regions in the protein profile increased their expression. Using tandem mass spectrometry, we successfully identified one of these five proteins: a carbonic anhydrase—an enzyme catalyzing the reversible hydration of carbon dioxide. Our findings suggest that proteins may be the target of sexual selection, as an active semiochemicals or as a dynamic support to other molecules: sexual selection may act indirectly on semiochemicals (namely lipids) by modifying the matrix (namely proteins).

Sexual selection and proteinaceous diversity in the femoral gland secretions of lacertid lizards

Sexual selection and proteinaceous diversity in the femoral gland secretions of lacertid lizards