Rock Lizards Research Articles

The farther, the closer: geographic proximity and niche overlap versus genetic divergence in Caucasian rock lizards

Abstract Caucasian rock lizards (Darevskia) are a speciose group with 42 described species from the Caucasus Mountain region. We selected 11 species from Georgia and adjacent territories to explore whether their distribution depends on the distribution of congeneric taxa. We estimated two measures for each species pair: (1) niche overlap between all pairs of the studied species; (2) the extent of contact between the ranges of individual species. We then calculated the correlation between these measurements and the time of divergence between the species. The results showed that in sympatric and parapatric (but not allopatric) species, there is a highly significant correlation between the divergence time and the extent of the contact, as well as between the divergence time and the overlap of suitable habitats. The ranges of the evolutionarily closest species have the smallest extent of contact. Species separated later have overlapping ranges, although are separated by altitude. The most distant species, irrespective of their phenotype, are commonly found in the same location. We suggest that a gradual increase in the contact extent is compensated for by increasing the effectiveness of other mechanisms of niche shift or behavioural isolation and hence the frequency of potentially deleterious interspecific contacts is kept low.

WESTERNMOST RECORD OF THE SHORT-NOSED ROCK LIZARD (Petrosaurus repens; SQUAMATA: PHRYNOSOMATIDAE) AND COMMENTS ON ITS DISTRIBUTION

Here we describe and confirm the westernmost record of the Short-nosed Rock Lizard (Petrosaurus repens) and provide comments about its distribution.

INVASION POTENTIAL OF DAREVSKIA ARMENIACA (MEHELY, 1909) IN UKRAINE: ASSESSMENT BASED ON GIS MODELING

The article is devoted to the actual problem of determining the invasive potential of the invader species, the Armenian rock lizard Darevskia armeniaca. A population of introduced parthenogenetic rock lizards Darevskia armeniaca has existed in the canyon of the Teteriv River (Zhytomyr region, Ukraine) for about 60 years. Their presence in the herpetofauna of Ukraine is the result of a scientific experiment aimed at studying the processes of acclimatization and the existence of a local population of clones in a limited area, the possibilities of hybridogenesis of parthenogenetic and bisexual species and other issues of population genetics.
 The invasive potential of rock lizards in this area was studied by the method of bioclimatic modeling of the ecological niche. The material was based on data from the Global Biodiversity Information System (GBIF.org (03 November 2021) GBIFOccurrenceDownload. To model the ecological niche, 19 bioclimatic variables, average monthly data on solar radiation intensity for the modern period (1970-2000), data on altitude from the WorldClim 2.1 database were used. Most of the significant parameters of the ecological niche for the introduced population are in the lower pessimum zone. The model built based on the entire collection of points of registration of the species shows that the territory where the species was introduced in Ukraine is one of the least suitable. Nevertheless, the population of introduced parthenogenetic rock lizards is now stable, thriving, numerous and slightly expanding its range by inhabiting new territories. Obviously, favorable conditions for the existence of D. armeniaca here are determined not by macroclimatic factors, but by microclimatic ones.
 The analysis of the model built on the basis of points of registration of the species in the introduced population shows that under existing climatic conditions, wide expansion of the species in this region of Ukraine is not possible, although a small expansion of its range is quite likely. There is also no reason to predict the transition of rock lizards to the number of invasive species.

New records of the rock lizards of the genus Darevskia Arribas, 1999 (Sauria: Lacertidae) in the Caucasus. Communication 2

Five new regional records of the rock lizards in Caucasus are described. The distribution of Darevskia alpina (Darevsky, 1967) on the northern slope of Mount Elbrus has been detailed: the species was found in the Emmanuel glade and in the gorge of the Kyzylkol River. The easternmost record of D. alpina is located in the upper stream of the Cherek Bezengi River in Kabardino-Balkaria. Darevskia caucasica vedenica (Darevsky et Roitberg, 1999) was first found on the territory of Dagestan in the area of the lake Kezenoyam and on the watershed of the Okholitlau and Khulhulau rivers. The existence of an isolated population of D. daghestanica (Darevsky, 1967) in the gorge of the Bolshaya Liakhvi River was confirmed, which is located in South Ossetia, on the southwestern border of the species range. When studying the collections of the Zoological Institute of the Russian Academy of Sciences, three specimens of D. dahli (Darevsky, 1957) were found from the village Alapars of the Kotayk region of Armenia collected in 1880. This locality is the southernmost and, moreover, the only record of the species in the Armenian volcanic highlands.

Diversification in the mountains: Evolutionary history and molecular phylogeny of Anatolian rock lizards

Mountains play a key role in forming biodiversity by acting both as barriers to gene flow among populations and as corridors for the migration of populations adapted to the conditions prevailing at high elevations. The Anatolian and the Zagros Mountains are located in the Alpine-Himalayan belt. The formation of these mountains has influenced the distribution and isolation of the animal population since the late Cenozoic. Apathya is a genus of lacertid lizards distributed along these mountains with two species, i.e., Apathya cappadocica and Apathya yassujica. The taxonomy status of lineages within the genus is complicated. In this study, we tried to collect extensive samples from throughout the distribution range, especially within the Zagros Mountains. Also, we used five genetic markers, two mitochondrial (COI and Cyt b) and three nuclear (C-mos, NKTR, and MCIR), to resolve the phylogenetic relationships within the genus and explain several possible scenarios that shaped multiple genetic structures. The combination of results in the current study indicated eight well-support monophyletic lineages that separated to two main groups; group 1 including A. c. cappadocica, A. c. muhtari and A. c. wolteri, group 2 contains four regional clades Turkey, Urmia, Baneh and Ilam, and finally a single clade belonging to the species A. yassujica. In contrast to previous studies, Apathya cappadocica urmiana was divided into four clades and three clades were recognized within Iranian boundaries. The clades have dispersed from Anatolia to adjacent regions in the south of Anatolia and the western Zagros Mountains. According to the evidence generated in this study this clade is paraphyletic. Based on our assumption, orogeny activities and also climate fluctuations in Middle Miocene and Pleistocene have influenced to formation of lineages. In this study we revisit the taxonomy of the genus and demonstrate that the species diversity was substantially underestimated. Our findings suggest that each of the eight clades corresponding to subspecies and distinct geographic regions deserve to be promoted to species level.

Reproductive effort of unisexual and bisexual rock lizards (genus Darevskia)

We compared the life history components of small and large-bodied unisexual (Darevskia dahli and Darevskia armeniaca) and bisexual (Darevskia portschinskii, Darevskia valentini, and Darevskia obscura) Caucasian rock lizard species. Research objectives were to determine whether reproductive mode (bisexual or parthenogenetic), female body size, altitude and landscape of the habitat, or interaction of these factors determine the relative investment of energy into a single reproduction, number, and relative size of eggs.The research revealed the differences between two parthenogenetic species and their paternal bisexual lizards. However, the pattern did not coincide for the two studied lineages i.e., parthenogenetic D. armeniaca invests relatively more resources into reproduction than its paternal D. valentini. Simultaneously, reproductive effort of parthenogenetic D. dahli did not differ from its paternal D. portschinskii. Instead, D. dahli tended to produce more but lighter eggs than D. portschinskii. In both cases, the parthenogenetic form tended to follow a r-reproductive strategy, typical for lizards occupying less stable environments than their parental species. However, other interspecific differences such as body size or evolutionary distance shade these differences, and determine the pattern of divergence between a parthenogen and its bisexual relative. In particular, smaller body size constrains increased the reproductive effort, and parthenogenetic species shifted to a balance between egg size and number rather than between resources invested into a single reproduction event and the probability to survive until the next season.

First Genome of Rock Lizard Darevskia valentini Involved in Formation of Several Parthenogenetic Species.

The extant reptiles are one of the most diverse clades among terrestrial vertebrates and one of a few groups with instances of parthenogenesis. Due to the hybrid origin of parthenogenetic species, reference genomes of the parental species as well as of the parthenogenetic progeny are indispensable to explore the genetic foundations of parthenogenetic reproduction. Here, we report on the first genome assembly of rock lizard Darevskia valentini, a paternal species for several parthenogenetic lineages. The novel genome was used in the reconstruction of the comprehensive phylogeny of Squamata inferred independently from 7369 trees of single-copy orthologs and a supermatrix of 378 conserved proteins. We also investigated Hox clusters, the loci that are often regarded as playing an important role in the speciation of animal groups with drastically diverse morphology. We demonstrated that Hox clusters of D. valentini are invaded with transposons and contain the HoxC1 gene that has been considered to be lost in the amniote ancestor. This study provides confirmation for previous works and releases new genomic data that will contribute to future discoveries on the mechanisms of parthenogenesis as well as support comparative studies among reptiles.

Ecological niche differentiation in the Anatolian rock lizards (Genus: Anatololacerta) (Reptilia: Lacertidae) of the Anatolian Peninsula and Aegean Islands

The genus Anatololacerta is distributed in the eastern Mediterranean region including Asia Minor and some east Aegean islands. Recent phylogenetic studies suggested that this genus displayed cryptic diversity and was divided into five species: A. anatolica, A. pelasgiana, A. ibrahimi, A. finikensis and A. danfordi. The ecological niche differentiations of these species have not been studied so far. Our aims for this study were to predict the potential suitable habitats for the species nested in genus Anatololacerta, and to examine the niche overlaps and differentiations via identity and background tests. The occurrence data were obtained from literature and our own field surveys. Occurrence records were rarefied and assessed in a 30 arc-second resolution layer, compatible with several bioclimatic and topographic variables. Species distribution analyses were performed using maximum entropy approach and pairwise niche comparisons were evaluated by identity and background tests. Our results demonstrated that the species delimitation among this genus was not only affected by geographic isolation but also that precipitation and temperature influenced the habitat suitability for these species. Predicted suitability usually well matched the actual species distributions. Moreover, the niche overlap (identity test) analyses verified that allopatric Anatololacerta species show clear ecological differentiations. However, a niche overlap between parapatric species A. pelasgiana and A. finikensis, was confirmed by identity and background tests. It has been suggested that these parapatric species could be more affected by microclimatological parameters than the others. The results of our study are in agreement with the latest phylogenetic study within this genus.

Multimodal female mate choice in a polymorphic flat rock lizard

Multimodal female mate choice in a polymorphic flat rock lizard

Evolution of parthenogenetic reproduction in Caucasian rock lizards: A review.

Despite numerous works devoted to hybrid origin of parthenogenesis in reptiles, the causes of hybridization between different species, resulting in the origin of parthenogenetic forms, remain uncertain. Recent studies demonstrate that sexual species considered parental to parthenogenetic rock lizards (Darevskia spp.) avoid interspecific mating in the secondary overlap areas. A specific combination of environmental factors during last glaciation period was critical for ectotherms, which led to a change in their distribution and sex ratio. Biased population structure (e.g., male bias) and limited available distributional range favored the deviation of reproductive behavior when species switched to interspecific mates. To date, at least 7 diploid parthenogenetic species of rock lizards (Darevskia, Lacertidae) originated through interspecific hybridization in the past. The cytogenetic specifics of meiosis, in particular the weak checkpoints of prophase I, may have allowed the formation of hybrid karyotypes in rock lizards. Hybridization and polyploidization are 2 important evolutionary forces in the genus Darevskia. At present, throughout backcrossing between parthenogenetic and parental species, the triploid and tetraploid hybrid individuals appear annually, but no triploid species found among Darevskia spp. on current stage of evolution. The speciation by hybridization with the long-term stage of diploid parthenogenetic species, non-distorted meiosis, together with the high ecological plasticity of Caucasian rock lizards provide us with a new model for considering the pathways and persistence of the evolution of parthenogenesis in vertebrates.

Precise paternal ancestry of hybrid unisexual ZW lizards (genus Darevskia: Lacertidae: Squamata) revealed by Z-linked genomic markers

Abstract We genotyped multiple populations of all seven parthenogenetic species of rock lizards, genus Darevskia, as well as their putative sexual parental populations, using double digest RAD-sequencing genomic markers. Taking advantage of the conserved homology of the ZW/ZZ sex chromosomes among lacertid lizards, we aligned our short sequence reads to a reference Z chromosome assembly of the common wall lizard Podarcis muralis. This provided unique insight into the origin of all-female hybrid populations, which inherited their single Z chromosome exclusively from a paternal ancestor. The mapped Z-linked loci were used to construct a robust time-calibrated phylogeny. In each parent–offspring species pair, the geographically nearest population of the paternal species was identified as the most likely ancestor of the respective parthenogen, mirroring the trend observed previously on the maternal side in mitochondrial DNA. The estimated splits between the sampled paternal sexual ancestors and their daughter species occurred much earlier than suggested previously and during two narrow time periods: (1) the parthenogenetic Darevskia armeniaca, D. dahli, D. uzzelli and D. rostombekowi dated back to ~0.5 or ~0.9 Mya, depending on the calibration point used, while (2) D. bendimahiensis, D. sapphirina and D. unisexualis appear to have diverged ~1 or ~2 Mya.

Parthenogenesis in Darevskia lizards: A rare outcome of common hybridization, not a common outcome of rare hybridization.

Hybridization is a common evolutionary process with multiple possible outcomes. In vertebrates, interspecific hybridization has repeatedly generated parthenogenetic hybrid species. However, it is unknown whether the generation of parthenogenetic hybrids is a rare outcome of frequent hybridization between sexual species within a genus or the typical outcome of rare hybridization events. Darevskia is a genus of rock lizards with both hybrid parthenogenetic and sexual species. Using capture sequencing, we estimate phylogenetic relationships and gene flow among the sexual species, to determine how introgressive hybridization relates to the origins of parthenogenetic hybrids. We find evidence for widespread hybridization with gene flow, both between recently diverged species and deep branches. Surprisingly, we find no signal of gene flow between parental species of the parthenogenetic hybrids, suggesting that the parental pairs were either reproductively or geographically isolated early in their divergence. The generation of parthenogenetic hybrids in Darevskia is, then, a rare outcome of the total occurrence of hybridization within the genus, but the typical outcome when specific species pairs hybridize. Our results question the conventional view that parthenogenetic lineages are generated by hybridization in a window of divergence. Instead, they suggest that some lineages possess specific properties that underpin successful parthenogenetic reproduction.

Molecular Structure and Polymorphism of Microsatellite Loci of Caucasian Rock Lizards Darevskia raddei of the “Yerevan” Population from Armenia

Molecular Structure and Polymorphism of Microsatellite Loci of Caucasian Rock Lizards Darevskia raddei of the “Yerevan” Population from Armenia

A review of mites and ticks parasitizing rock lizards (Lacertidae: Darevskia).

Rock lizards of the genus Darevskia are interesting research models due to their asexual reproduction. Ectoparasitic mites and ticks of these lizards are poorly known, despite some of these chelicerates being vector pathogens of humans and wildlife. Here we document and curate previously known data on ectoparasitic Acari of rock lizards and, based on our extensive survey, provide an annotated list of these ectoparasitic arthropods (six tick species, one macronyssid species, and seven chigger species). We also provide new host records (Ixodes ricinus on Darevskia caucasica, D. dryada, D. mixta, and D. szczerbaki; Haemaphysalis sulcata on D. rudis; Odontacarus saxicolis on D. brauneri); and new geographical records (O. saxicolis in Russia and Georgia).

Lichens and animal camouflage: some observations from central Asian ecoregions

Camouflage is a fitness-relevant trait that supports survival and fosters evolutionary adaptation by which animals match their body pattern to a background setting. Lichens are among the most common of these backgrounds that several animal species use for camouflage. Lichens are omnipresent and grow in wide arrays of colorations and compositions. Their composition and phenotypic diversity might facilitate cryptic coloration and habitat matching by various animal species. Here, we describe the role of lichens in providing camouflage to various animal species in central Asian and Caucasus mountain ecoregions, which are categorized as global biodiversity hotspots. Despite multiple ecological studies, no information is available on the role of this regions‘ lichen diversity in providing animal camouflage. Casual field observations of lichen camouflage are reported for four (one mammal and three reptile) species: the Persian Leopard’s Panthera pardus saxicolor body coat seems to closely match the colors and patterns of saxicolous lichens (Acarospora sp. and Circinaria sp.) in their habitat. A similar background matching pattern was observed in both morphs of the Caucasian Rock Agama Paralaudakia caucasia upon crustose lichens: Caloplaca spp., Circinaria spp., and the Radde’s Rock Lizard Darevskia raddei to the crustose lichens Acarospora sp. and Caloplaca sp. Likewise, the Horny-scaled Agama’s Trapelus ruderatus grey matches with the color of multiple lichens (Lecanora spp., Circinaria spp., Protoparmeliopsis spp., Rinodina spp., and Anaptychia spp.). Our observations preliminarily suggest that lichens play an important role for species of different trophic levels, ensuring adaptation and survival through camouflage. We call for more field-based empirical and experimental studies in various terrestrial ecosystems in other parts of the world to test the role of lichens in local adaption and evolutionary plasticity of regional species.

Hidden Diversity in a Narrow Valley: Description of New Endemic Palearctic Rock Lizard Darevskia (Squamata: Lacertidae) Species from Northeastern Turkey.

Darevskia is a particularly species-rich radiation of Palearctic rock lizards from the Caucasus region. Thanks to intense systematic and taxonomic research, the knowledge of species-level diversity within this genus has increased over the last quarter century. Here, we described a new species, Darevskia salihae sp. nov. from northeastern Turkey. The new taxon is differentiated from other nearby taxon by the low number of dorsal scales in the middle of the body, the shorter body length, and the absence of blue dots both on the lateral region above the forelimbs and on the margin of the ventral plates. In addition to their morphological differences, the new taxon is phylogenetically different from close groups. It is located in a separate subclade from the rudis-valentini-portschinskii subclade. This distinction is supported by both a high bootstrap value (100) and a high posterior probability value (1.00). These two subclades are separated from each other by a genetic distance of almost 4%. This separation is supported not only genetically and morphologically, but also geographically. Since the habitat of the new taxon is limited to a high mountain and a narrow valley, it does not provide an opportunity for a different Darevskia species to shelter because it creates geographical isolation. However, Darevskia parvula that live closest to the habitat of the new taxon live only at the habitat boundaries and do not enter areas where the new taxon is found. Therefore, it might be possible that while it was separated from the rudis-valentini-portschinskii group during the evolutionary transformation, it remained as a refuge and relict in a narrow area as a result of the collapse of the valleys and the partial uplift of the Kaçkar Mountains.

О границах ареала ящерицы Линдгольма (Sauria, Lacertidae) Darevskia lindholmi

New data on the boundaries of the distribution range of the Lindholm rock lizard (Darevskia lindholmi), an endemic of the Crimean Peninsula, are presented. This petrophilous lizard inhabit a wide range of biotopes in various landscape levels of the Mountainous Crimea. The upper boundary of D. lindholmi distribution in the southwest of the Main Range of the Crimean Mountains reaches an elevation of 1,520 m a.s.l. (Ai-Petrinskaya Yayla, KemalEgerek Mountain), while on the other high uplands with altitudes above 1.5 km and colder climate (Babugan and Chatyrdag), the species was traced only up to 1,250–1,320 m a.s.l. The northern border of D. lindholmi range in the western part of the Crimean Mountains runs along the Outer Foothill Range (the right bank of the Alma River), while in the eastern part it corresponds the northernmost rocky massifs of the Inner Foothill Range to the north of 45º N latitude. Isolated marginal populations found in the forest-steppe or phrygana-steppe landscapes of the Foothills and arid Southeastern Coast differs significantly in their distance from the main habitat of the species, lizards’ abundance and density. A hypothetical history of the formation of the current range of the Lindholm lizard is discussed.

Reproductive Characteristics of the Kulzer’s Rock Lizard Phoenicolacerta kulzeri (Reptilia: Lacertidae)

The present study aims to determine, by histological examination, the female reproductive cycle of specimens of Kulzer’s rock lizards collected in a mountainous region in Lebanon. Females of Phoenicolacerta kulzeri followed a seasonal reproductive pattern. Winter hibernation period lasted for 5 months. Females of P. Kulzeri exhibited a reproductive activity during spring characterized by the presence of vitellogenic follicles in the ovaries and eggs in the oviducts. Oviposition occurred throughout the springtime. Up to two clutches were produced with an average clutch size of 2.9 eggs. Clutch size was significantly correlated to female body size. The attainment of sexual maturity was at a minimum size of 46 mm snout-vent length. The mean body size of adult females was 55.0 mm and did not differ significantly from that of adult males. Females showed a period of sexual rest in summer and none of them showed a reproductive activity in autumn. The female reproductive activity of P. kulzeri was well-synchronized with that of the males in spring; however, an autumnal asynchrony was observed between the female and male reproductive cycles, since males continued to exhibit a spermatogenetic activity.

The mitochondrial phylogeography of the Crimean endemic lizard Darevskia lindholmi (Sauria, Lacertidae): Hidden diversity in an isolated mountain system

AbstractThe Lindholm rock lizard,Darevskia lindholmi, is the only member of the genusDarevskiawhose range is restricted solely to Europe, representing a local endemism found only in the Crimean Mountains. In our study, we investigated the cytochromebgene (mtDNA) of 101D. lindholmisequences from 65 Crimean localities, representing its entire range. We found thatD. lindholmiis highly genetically structured, and its range is divided into populations belonging to three mitochondrial lineages. The Lindholm rock lizard populations inhabiting the middle part of the Crimean Mountains (further referred to as the Central lineage) are sharply differentiated from the other two lineages (the Common and the Southwestern lineages), which are present in most of the species range. The genetic distance between the Central lineage and the other two taken together is 4.6%, according to our results, suggesting that the divergence occurred during the Early Pleistocene. The narrowly distributed Southwestern lineage and the widespread Common lineage, on the other hand, are differentiated by 1%. Field observations on the representatives of the main evolutionary groups show that their ecology is also different: the Central lineage is a mesophilic and cold-resistant form, while the other two closely related lineages are more xerophilic and thermophilic. Results of the potential ranges modeling and ecological niche analysis confirm that the genetic lineages occupy different niches of the Crimea. Furthermore, the area of inhabitation of the Central lineage splits the western and eastern parts of the Common lineage range, while the Southwestern lineage is restricted along the coast of the southwestern coast of the peninsula. The long-term co-existence of deeply divergent sister mitochondrial lineages in a relatively small (circa 7,000 km2) isolated mountain system serves as a mesocosm for understanding the speciation process. Our data suggest that the Central lineage warrants further taxonomic investigation.

Foraging decisions of rock lizards may be dependent both on current rival assessment and dear enemy recognition

Foraging strategies aim to maximize the amount of food obtained while minimizing searching costs. To reduce these costs, animals use different strategies based on the use of personal or social information to exploit food patches. At the same time, the social attraction for food resources could increase competition intensity for them. Prior experiences of animals regarding social risk and the foreknowledge of the competitors might drive the foraging strategies. In this paper, we examined experimentally whether rock lizards used behavioural strategies to reduce the risks of foraging in presence of potential competitors. We measured the foraging behaviour of a lizard resident to a territory (i.e. terrarium), in the presence of both familiar and unfamiliar conspecifics (potential competitors). We considered whether foraging choices between two food sources of different value (i.e. quantity) are influenced by familiarity with the intruder and the evaluation of its competitive ability based on body size differences between lizards. We found differences in the number of attacks performed to the best food source, with more attacks when the intruder was unfamiliar. The results suggest evidence of both dear enemy recognition and current rival assessment modulate the foraging choices depending on the identity and the social relationship with the intruder.