Climatic niche differences among Zootoca vivipara clades with different parity modes: implications for the evolution and maintenance of viviparity

Parity mode (oviparity/viviparity) importantly affects the ecology, morphology, physiology, biogeography and evolution of organisms. The main hypotheses explaining the evolution and maintenance of viviparity are based on bioclimatic predictions and also state that the benefits of viviparity arise during the reproductive period. We identify the main climatic variables discriminating between viviparous and oviparous Eurasian common lizard (Zootoca vivipara) occurrence records during the reproductive period and over the entire year.Analyses based on the climates during the reproductive period show that viviparous clades inhabit sites with less variable temperature and precipitation. On the contrary, analyses based on the annual climates show that viviparous clades inhabit sites with more variable temperatures.Results from models using climates during reproduction are in line with the “selfish-mother hypothesis”, which can explain the success of viviparity, the maintenance of the two reproductive modes, and why viviparous individuals cannot colonize sites inhabited by oviparous ones (and vice versa). They suggest that during the reproductive period viviparity has an adaptive advantage over oviparity in less risky habitats thanks to the selfish behaviour of the mothers. Moreover, the results from both analyses stress that hypotheses about the evolution and maintenance of viviparity need to be tested during the reproductive period.

Global changes explain the long-term demographic trend of the Eurasian common lizard (Squamata: Lacertidae)

The demographic trend of a species depends on the dynamics of its local populations, which can be compromised by local or by global phenomena. However, the relevance of local and global phenomena has rarely been investigated simultaneously. Here we tested whether local phenomena compromised a species’ demographic trend using the Eurasian common lizard Zootoca vivipara, the terrestrial reptile exhibiting the widest geographic distribution, as a model species. We analysed the species’ ancient demographic trend using genetic data from its six allopatric genetic clades and tested whether its demographic trend mainly depended on single clades or on global phenomena. Zootoca vivipara’s effective population size increased since 2.3 million years ago and started to increase steeply and continuously from 0.531 Mya. Population growth rate exhibited two maxima, both occurring during global climatic changes and important vegetation changes on the northern hemisphere. Effective population size and growth rate were negatively correlated with global surface temperatures, in line with global parameters driving long-term demographic trends. Zootoca vivipara’s ancient demography was not driven by a single clade, nor by the two clades that colonized huge geographic areas after the last glaciation. The low importance of local phenomena, suggests that the experimentally demonstrated high sensitivity of this species to short-term ecological changes is a response in order to cope with short-term and local changes. This suggests that what affected its long-term demographic trend the most, were not these local changes/responses, but rather the important and prolonged global climatic changes and important vegetation changes on the northern hemisphere, including the opening up of the forest by humans.

The Allelic Variants in Microsatellite Loci and Phylogenetic Relationships of Darevskia rudis (Bedriaga, 1886) and D. bithynica (Méhely, 1909) Based on Mitochondrial DNA in Turkey

The spiny-tailed lizard, which has a series of taxonomic revisions, is one of the most common lizard species in Turkey. In this study, sequence data derived from three microsatellite loci (Du215, Du281, and Du323), two mitochondrial (16S rRNA and Cyt-b) genes and combined data were used to evaluate the taxonomic status of Darevskia rudis and Darevskia bithynica with new samples from all subspecies populations in Turkey. Our results indicated that the genetic variations of microsatellite loci were not specific to populations within species, and only minor differences separated D. rudis and D. bithynica populations. Furthermore, the markers we used for phylogenetic analyses (NJ, ML, MP, and BI) produced topologically similar trees based on 16S rRNA and Cyt-b while the combined data produced conflicting trees with the separate gene analyses. Finally, the basal relationships among the populations in Turkish populations D. rudis and D. bithynica were not resolved with this dataset, and we found a hard polytomy at the basis of the phylogeny.

Additive effects of temperature and water availability on pregnancy in a viviparous lizard

ABSTRACTOne of the greatest current threats to biodiversity is climate change. However, understanding of organismal responses to fluctuations in temperature and water availability is currently lacking, especially during fundamental life-history stages such as reproduction. To further explore how temperature and water availability impact maternal physiology and reproductive output, we used the viviparous form of the European common lizard (Zootoca vivipara) in a two-by-two factorial design manipulating both hydric and thermal conditions, for the first time. We collected blood samples and morphological measurements during early pregnancy and post-parturition to investigate how water availability, temperature and a combination of the two influence maternal phenology, morphology, physiology and reproductive output. We observed that dehydration during gestation negatively affects maternal physiological condition (lower mass gain, higher tail reserve mobilization) but has little effect on reproductive output. These effects are mainly additive to temperature regimes, with a proportional increase in maternal costs in warmer environments. Our study demonstrates the importance of considering combined effects of water and temperature when investigating organismal responses to climate changes, especially during periods crucial for species survival such as reproduction.

Chromosome-Level Assembly of the Common Lizard (Zootoca vivipara) Genome

Squamate reptiles exhibit high variation in their phenotypic traits and geographical distributions and are therefore fascinating taxa for evolutionary and ecological research. However, genomic resources are very limited for this group of species, consequently inhibiting research efforts. To address this gap, we assembled a high-quality genome of the common lizard, Zootoca vivipara (Lacertidae), using a combination of high coverage Illumina (shotgun and mate-pair) and PacBio sequencing data, coupled with RNAseq data and genetic linkage map generation. The 1.46-Gb genome assembly has a scaffold N50 of 11.52 Mb with N50 contig size of 220.4 kb and only 2.96% gaps. A BUSCO analysis indicates that 97.7% of the single-copy Tetrapoda orthologs were recovered in the assembly. In total, 19,829 gene models were annotated to the genome using a combination of ab initio and homology-based methods. To improve the chromosome-level assembly, we generated a high-density linkage map from wild-caught families and developed a novel analytical pipeline to accommodate multiple paternity and unknown father genotypes. We successfully anchored and oriented almost 90% of the genome on 19 linkage groups. This annotated and oriented chromosome-level reference genome represents a valuable resource to facilitate evolutionary studies in squamate reptiles.

Smooth snake population decline and its link with prey availability

The relationship between the numbers of smooth snakes, Coronella austriaca, and common lizards, Zootoca vivipara, was investigated in a 6.5 ha area of lowland heath within Wareham Forest in southern England. With the exception of 2002 the numbers of lizards, small mammals and individual smooth snakes captured, or observed, were recorded during each of 21 annual surveys between May and October 1997-2018. Smooth snake diet was investigated annually between 2004 and 2015 by analysing faecal samples and showed that lizards, particularly the common lizard, and pigmy shrews, Sorex minutus, were important prey species. There was no significant correlation between the occurrence of any small mammal species and either snake numbers or their presence in smooth snake diet. Over the study period there was an overall decline in the number of smooth snakes captured whilst there was an overall increase in the number of common lizard sightings. The frequency of common lizards found in the diet of smooth snakes was positively correlated with their abundance within the study area. There was a significant correlation between the decline of smooth snake numbers and the subsequent increase in the number of common lizard sightings suggesting that lizard abundance may be controlled by snake numbers. Conversely, we found no evidence indicating that smooth snake numbers were dependent on lizard numbers suggesting that factors other than prey availability e.g. habitat change due to cattle grazing, blocking ground water drainage ditches, or climatic variables, were impacting on snake numbers, particularly between 2012 and 2018.

Mother-offspring conflict for water and its mitigation in the oviparous form of the reproductively bimodal lizard, Zootoca vivipara

Parent-offspring conflicts are widespread given that resources are often limited. Recent evidence has shown that availability of water can trigger such conflict during pregnancy in viviparous squamate species (lizards and snakes) and thus questions the role of water in the evolution of reproductive modes. Here, we examined the impact of water restriction during gravidity in the oviparous form of the bimodal common lizard (Zootoca vivipara), using a protocol previously used on the viviparous form. Females were captured in early gravidity from six populations along a 600 m altitudinal gradient to investigate whether environmental conditions (altitude, water access and temperature) exacerbate responses to water restriction. Females were significantly dehydrated after water restriction, irrespective of their reproductive status (gravid vs. non-reproductive), relative reproductive effort (relative clutch mass), and treatment timing (embryonic development stage). Female dehydration, together with reproductive performance, varied with altitude, probably due to long term acclimation or local adaptation. This moderate water-based intergenerational conflict in gravid females contrasts sharply with previous findings for the viviparous form, with implications to the evolutionary reversion from viviparity to oviparity. It is likely that oviparity constitutes a water-saving reproductive mode which might help mitigate intensive temperature-driven population extinctions at low altitudes.