Predation Risk, and Not Shelter or Food Availability, as the Main Determinant of Reproduction Investment in Island Lizards.

Reproductive investment, including the number of offspring produced, is one of the fundamental characteristics of a species. It is particularly important for island vertebrates, which face a disproportionate number of threats to their survival, because it predicts, among other things, a species' resilience to environmental disruption. Taxa producing more offspring recover more quickly from environmental perturbations and survive environmental change better. However, ecologists do not understand which primary drivers shape a species' reproductive investment well. Here, we compare the reproductive efforts of 14 island populations of the Aegean Wall Lizard (Podarcis erhardii), which lives across widely diverging environmental conditions. We test three hypotheses, namely that reproductive investment (measured as clutch size, clutch volume) is (1) positively associated with predation risk ['Predation Risk Hypothesis']; (2) positively associated with the presence of reliable vegetation cover that provides shelter ['Gravid Female Protection Hypothesis']; and (3) limited by (and hence positively correlated with) food availability ['Food Limitation Hypothesis']. Although field data are somewhat consistent with all three hypotheses, statistical analyses provide strong support for the Predation Risk Hypothesis. The results not only shed light on which fundamental forces shape reproductive investment in island vertebrates, but can also help shape conservation priorities.

Seasonal Variation in the Thermoregulation Pattern of an Insular Agamid Lizard.

Ectotherms, including lizards, rely on behavioral thermoregulation to maintain their body temperature within an optimal range. The benign climate of islands is expected to favor the thermoregulation efficiency of reptiles throughout their activity period. In this study, we investigated the seasonal variation in thermoregulation in an insular population of the roughtail rock agama (Laudakia stellio) on Naxos Island, Greece. We measured body, operative, and preferred temperatures across three seasons (spring, summer, and autumn), and we evaluated the effectiveness of thermoregulation, using the Hertz index (E). Our results revealed that the effectiveness of thermoregulation was significantly influenced by seasonality. E was quite high in summer (0.97) and spring (0.92), and lowest in autumn (0.81). Accordingly, the quality of the thermal environment was significantly low during autumn, and maximum during summer. However, despite the environmental temperature fluctuations, lizards exhibited remarkable stability in body temperatures. They also adjusted their preferred temperatures seasonally and doubled the thermal niche breadth they occupied during summer, thus enhancing thermoregulation efficiency. Whether or not these adjustments are plastic or fixed local adaptations remains to be explored in further research across multiple years and seasons, including additional insular populations.

The Evolution of Diet and Morphology in Insular Lizards: Insights from a Replicated Island Introduction Experiment.

Resource-limited environments may drive the rapid evolution of phenotypic traits and ecological preferences optimizing the exploitation of resources. Very small islands are often characterized by reduced food availability, seasonal fluctuations in resources and strong unpredictability. These features may drive the evolution of phenotypic traits such as high bite forces, allowing animals to exploit a wider variety of the available resources. They may also lead to more generalist dietary patterns in response to food scarcity. However, the lack of predators and competitors on such small islands often also leads to high densities and the evolution of strong sexual dimorphism, which may also drive the evolution of bite force. Here, we take advantage of a unique replicated introduction experiment to test whether lizards introduced into very small islands alter their feeding ecology and use different resources, resulting in the evolution of a large body size, large head size and large bite forces. Our results show that three years after their introduction, the island lizards were larger and had greater bite forces and more pronounced sexual dimorphism. However, the diets were only marginally different between animals from the source population on a very large nearby island and those on the islets. Moreover, distinct differences in diet between animals on the different islets were observed, suggesting that the local environment is a strong driver of resource use. Overall, lizards with absolutely and relatively (adjusted for body size) large bite forces did eat larger and harder prey. Taken together, our data suggest that intraspecific competition is an important driver of the rapid evolution of bite force, which may allow these lizards to exploit the scarce and fluctuating resources on the islets. Whether or not lizards will evolve to include other types of food such as plants in their diet, facilitated by their large bite forces, remains to be explored in future studies.

Small Island Effects on the Thermal Biology of the Endemic Mediterranean Lizard Podarcis gaigeae.

Ectotherms are vastly affected by climatic conditions as they rely on external sources of heat to regulate their body temperature, and changes in their habitat thermal quality could seriously affect their overall biology. To overcome the problems of a thermally unfavorable habitat, lizards need to either adjust their thermoregulatory behavior or respond to directional selection and shift their preferred body temperatures. To assess the impact of habitat thermal quality on the thermoregulatory profile, we studied multiple islet and 'mainland' populations of the Skyros wall lizard Podarcis gaigeae, an endemic lacertid to Skyros Archipelago, Greece. We evaluated the effectiveness of thermoregulation (E) using the three main thermal parameters: body (Tb), operative (Te), and preferred (Tpref) temperatures. We first hypothesized that the spatial homogeneity, the scarcity of thermal shelters, and the exposure to higher winds on islets would result in more demanding climate conditions. Second, we anticipated that islet lizards would achieve higher E in response to the lower thermal quality therein. As hypothesized, thermal parameters differed between populations but not in the expected manner. Skyros 'mainland' habitats reached higher temperatures, had more intense fluctuations, and were of lower thermal quality. As a result, lizards showed higher accuracy, precision, and effectiveness of thermoregulation. Noteworthy, we found that lizards from different populations have shifted their thermal profile and preferred body temperatures to cope with the particular conditions prevailing in their habitats. The latter supports the labile view on the evolution of thermoregulation.

Some like it hotter: Differential thermal preferences among lizard color morphs.

Temperature rules the lives of ectotherms. To perform basic biological functions, ectotherms must make behavioral adjustments to keep their body temperatures near a preferred temperature (Tpref). Many color polymorphic lizards are active thermoregulators and exhibit morph differences in traits related to thermoregulation, such as color, body size, and microhabitat use. The Aegean wall lizard, Podarcis erhardii, is a heliothermic lizard with orange, white, and yellow color morphs that differ in size, behavior, and microhabitat use. Here, we tested whether P. erhardii color morphs from the same population from Naxos island, Greece, differ in Tpref. We hypothesized that orange morphs would prefer lower temperatures than white and yellow morphs because orange morphs are often found on cooler substrates and in microhabitats with more vegetation cover. We obtained Tpref for 95 individuals using laboratory thermal gradient experiments of wild-caught lizards and found that orange morphs do, indeed, prefer cooler temperatures. Average orange morph Tpref was 2.85 °C lower than average white and yellow morph Tpref. Our results add support to the idea that P. erhardii color morphs have multivariate alternative phenotypes and present the possibility that thermally heterogeneous environments play a role in the maintenance of color polymorphism in this species.

Learning with lacertids: Studying the link between ecology and cognition within a comparative framework.

Cognition is an essential tool for animals to deal with environmental challenges. Nonetheless, the ecological forces driving the evolution of cognition throughout the animal kingdom remain enigmatic. Large-scale comparative studies on multiple species and cognitive traits have been advanced as the best way to facilitate our understanding of cognitive evolution, but such studies are rare. Here, we tested 13 species of lacertid lizards (Reptilia: Lacertidae) using a battery of cognitive tests measuring inhibitory control, problem-solving, and spatial and reversal learning. Next, we tested the relationship between species' performance and (a) resource availability (temperature and precipitation), habitat complexity (Normalized Difference Vegetation Index), and habitat variability (seasonality) in their natural habitat and (b) their life history (size at hatching and maturity, clutch size, and frequency). Although species differed markedly in their cognitive abilities, such variation was mostly unrelated to their ecology and life history. Yet, species living in more variable environments exhibited lower behavioral flexibility, likely due to energetic constrains in such habitats. Our standardized protocols provide opportunities for collaborative research, allowing increased sample sizes and replication, essential for moving forward in the field of comparative cognition. Follow-up studies could include more detailed measures of habitat structure and look at other potential selective drivers such as predation.

Bold and bright: shy and supple? The effect of habitat type on personality-cognition covariance in the Aegean wall lizard (Podarcis erhardii).

Animals exhibit considerable and consistent among-individual variation in cognitive abilities, even within a population. Recent studies have attempted to address this variation using insights from the field of animal personality. Generally, it is predicted that animals with "faster" personalities (bolder, explorative, and neophilic) should exhibit faster but less flexible learning. However, the empirical evidence for a link between cognitive style and personality is mixed. One possible reason for such conflicting results may be that personality-cognition covariance changes along ecological conditions, a hypothesis that has rarely been investigated so far. In this study, we tested the effect of habitat complexity on multiple aspects of animal personality and cognition, and how this influenced their relationship, in five populations of the Aegean wall lizard (Podarcis erhardii). Overall, lizards from both habitat types did not differ in average levels of personality or cognition, with the exception that lizards from more complex habitats performed better on a spatial learning task. Nevertheless, we found an intricate interplay between ecology, cognition, and personality, as behavioral associations were often habitat- but also year-dependent. In general, behavioral covariance was either independent of habitat, or found exclusively in the simple, open environments. Our results highlight that valuable insights may be gained by taking ecological variation into account while studying the link between personality and cognition.

Population Genomics of Wall Lizards Reflects the Dynamic History of the Mediterranean Basin.

The Mediterranean Basin has experienced extensive change in geology and climate over the past six million years. Yet, the relative importance of key geological events for the distribution and genetic structure of the Mediterranean fauna remains poorly understood. Here, we use population genomic and phylogenomic analyses to establish the evolutionary history and genetic structure of common wall lizards (Podarcis muralis). This species is particularly informative because, in contrast to other Mediterranean lizards, it is widespread across the Iberian, Italian, and Balkan Peninsulas, and in extra-Mediterranean regions. We found strong support for six major lineages within P. muralis, which were largely discordant with the phylogenetic relationship of mitochondrial DNA. The most recent common ancestor of extant P. muralis was likely distributed in the Italian Peninsula, and experienced an "Out-of-Italy" expansion following the Messinian salinity crisis (∼5 Mya), resulting in the differentiation into the extant lineages on the Iberian, Italian, and Balkan Peninsulas. Introgression analysis revealed that both inter- and intraspecific gene flows have been pervasive throughout the evolutionary history of P. muralis. For example, the Southern Italy lineage has a hybrid origin, formed through admixture between the Central Italy lineage and an ancient lineage that was the sister to all other P. muralis. More recent genetic differentiation is associated with the onset of the Quaternary glaciations, which influenced population dynamics and genetic diversity of contemporary lineages. These results demonstrate the pervasive role of Mediterranean geology and climate for the evolutionary history and population genetic structure of extant species.

Functional genomics of abiotic environmental adaptation in lacertid lizards and other vertebrates.

Understanding the genomic basis of adaptation to different abiotic environments is important in the context of climate change and resulting short-term environmental fluctuations. Using functional and comparative genomics approaches, we here investigated whether signatures of genomic adaptation to a set of environmental parameters are concentrated in specific subsets of genes and functions in lacertid lizards and other vertebrates. We first identify 200 genes with signatures of positive diversifying selection from transcriptomes of 24 species of lacertid lizards and demonstrate their involvement in physiological and morphological adaptations to climate. To understand how functionally similar these genes are to previously predicted candidate functions for climate adaptation and to compare them with other vertebrate species, we then performed a meta-analysis of 1,100 genes under selection obtained from -omics studies in vertebrate species adapted to different abiotic factors. We found that the vertebrate gene set formed a tightly connected interactome, which was to 23% enriched in previously predicted functions of adaptation to climate, and to a large part (18%) involved in organismal stress response. We found a much higher degree of identical genes being repeatedly selected among different animal groups (43.6%), and of functional similarity and post-translational modifications than expected by chance, and no clear functional division between genes used for ectotherm and endotherm physiological strategies. In total, 171 out of 200 genes of Lacertidae were part of this network. These results highlight an important role of a comparatively small set of genes and their functions in environmental adaptation and narrow the set of candidate pathways and markers to be used in future research on adaptation and stress response related to climate change.

Specialist versus Generalist at the Intraspecific Level: Functional Morphology and Substrate Preference of Mediodactylus kotschyi Geckos.

Populations of the same species occupying different microhabitats can either exhibit generalized traits across them or display intraspecific variability, adapting to each microhabitat in order to maximize performance. Intraspecific variability contributes to the generation of diversity, following selection and adaptation, and understanding such variability is important for comprehending how individuals choose their microhabitats. Compared with interspecific variability, however, intraspecific variability in functional morphology and its relationship with microhabitat preference and use have been relatively little studied. Here we examined whether populations of the gecko Mediodactylus kotschyi that differ in the substrates they occupy display habitat-specific behaviors and differing morphologies associated with functional adaptation to their microhabitats. We collected 207 geckos from under or on rocks or on trees from seven populations in Greece. On large islands individuals occupy both substrates; whereas small islets are devoid of trees and the geckos are restricted to rocks, while on the mainland they are only found on trees. We determined gecko substrate preferences in the laboratory, together with their clinging abilities to the different substrates. We measured their limbs, digits, and claws and assessed how these measurements relate to clinging ability. Geckos from all populations preferred the tree made available to them, but this preference was not statistically significant. Geckos from both large and small islands clung better to the tree than to the rock in the laboratory, while those from the mainland clung similarly to both substrates. Geckos collected from trees had longer manual digits and hind limbs. Geckos collected from large and small islands had taller (longer on the dorso-ventral axis; henceforth "deeper") claws. Longer digits and deeper but shorter claws were associated with a better ability to cling to rocks. Our findings suggest that while M. kotschyi is potentially preferentially arboreal, due to the great variation and plasticity it possesses, it can successfully also exploit the habitats available on the smallest, treeless islets in the Aegean Sea. Our study suggests that the dichotomous use of generalist versus specialist in describing species' habitat use is oversimplified, and we suggest the use of a generalist-specialist gradient instead.

Tail regeneration alters the digestive performance of lizards.

Tissue regeneration is a fundamental evolutionary adaptation, which is well known in lizards that can regenerate their entire tail. However, numerous parameters of this process remain poorly understood. Lizard tail serves many functions. Thus, tail autotomy comes with many disadvantages and the need for quick regeneration is imperative. To provide the required energy and materials for caudal tissue building, lizards are expected to undergo a number of physiological and biochemical adjustments. Previous research showed that tail regeneration induces changes in the digestive process. Here, we investigated if and how tail regeneration affects the digestive performance in five wall lizard species deriving from mainland and island sites and questioned whether the association of tail regeneration and digestion is affected by species relationships or environmental features, including predation pressure. We expected that lizards from high predation environments would regenerate their tail faster and modify accordingly their digestive efficiency, prioritizing the digestion of proteins; the main building blocks for tissue repair. Second, we anticipated that the general food shortage on islands would inhibit the process. Our findings showed that all species shifted their digestive efficiency, as predicted. Elongation rate was higher in sites with stronger predation regime and this was also applied to the rate with which protein digestion raised. Gut passage time increases during regeneration so as to improve the nutrient absorbance, but among the islanders, the pace was more intense. The deviations between species should be attributed to the different ecological conditions prevailing on islands rather than to their phylogenetic relationships.

Trait differences among discrete morphs of a color polymorphic lizard, Podarcis erhardii.

Color polymorphism defies evolutionary expectations as striking phenotypic variation is maintained within a single species. Color and other traits mediate social interactions, and stable polymorphism within a population is hypothesized to be related to correlational selection of other phenotypic traits among color morphs. Here, we report on a previously unknown throat color polymorphism in the Aegean Wall Lizard (Podarcis erhardii) and examine morph-correlated differences in traits important to social behavior and communication: maximum bite force capacity and chemical signal profile. We find that both sexes of P. erhardii have three color morphs: orange, yellow, and white. Moreover, orange males are significantly larger and tend to bite harder than yellow and white males. Although the established color polymorphism only partially matches the observed intraspecific variation in chemical signal signatures, the chemical profile of the secretions of orange males is significantly divergent from that of white males. Our findings suggest that morph colors are related to differences in traits that are crucial for social interactions and competitive ability, illustrating the need to look beyond color when studying polymorphism evolution.

Landscape Connectivity Limits the Predicted Impact of Fungal Pathogen Invasion.

Infectious diseases are major drivers of biodiversity loss. The risk of fungal diseases to the survival of threatened animals in nature is determined by a complex interplay between host, pathogen and environment. We here predict the risk of invasion of populations of threatened Mediterranean salamanders of the genus Lyciasalamandra by the pathogenic chytrid fungus Batrachochytrium salamandrivorans by combining field sampling and lab trials. In 494 samples across all seven species of Lyciasalamandra, B. salamandrivorans was found to be absent. Single exposure to a low (1000) number of fungal zoospores resulted in fast buildup of lethal infections in three L. helverseni. Thermal preference of the salamanders was well within the thermal envelope of the pathogen and body temperatures never exceeded the fungus' thermal critical maximum, limiting the salamanders' defense opportunities. The relatively low thermal host preference largely invalidates macroclimatic based habitat suitability predictions and, combined with current pathogen absence and high host densities, suggests a high probability of local salamander population declines upon invasion by B. salamandrivorans. However, the unfavorable landscape that shaped intraspecific host genetic diversity, lack of known alternative hosts and rapid host mortality after infection present barriers to further, natural pathogen dispersal between populations and thus species extinction. The risk of anthropogenic spread stresses the importance of biosecurity in amphibian habitats.

Evolutionary Variability of W-Linked Repetitive Content in Lacertid Lizards.

Lacertid lizards are a widely radiated group of squamate reptiles with long-term stable ZZ/ZW sex chromosomes. Despite their family-wide homology of Z-specific gene content, previous cytogenetic studies revealed significant variability in the size, morphology, and heterochromatin distribution of their W chromosome. However, there is little evidence about the accumulation and distribution of repetitive content on lacertid chromosomes, especially on their W chromosome. In order to expand our knowledge of the evolution of sex chromosome repetitive content, we examined the topology of telomeric and microsatellite motifs that tend to often accumulate on the sex chromosomes of reptiles in the karyotypes of 15 species of lacertids by fluorescence in situ hybridization (FISH). The topology of the above-mentioned motifs was compared to the pattern of heterochromatin distribution, as revealed by C-banding. Our results show that the topologies of the examined motifs on the W chromosome do not seem to follow a strong phylogenetic signal, indicating independent and species-specific accumulations. In addition, the degeneration of the W chromosome can also affect the Z chromosome and potentially also other parts of the genome. Our study provides solid evidence that the repetitive content of the degenerated sex chromosomes is one of the most evolutionary dynamic parts of the genome.

Rapid and repeated divergence of animal chemical signals in an island introduction experiment.

Studies of animal communication have documented myriad rapid, context-dependent changes in visual and acoustic signal design. In contrast, relatively little is known about the capacity of vertebrate chemical signals to rapidly respond, either plastically or deterministically, to changes in context. Four years following an experimental introduction of lizards to replicate experimental islets, we aimed to determine if chemical signal design of the experimental populations differed from that of the source population. In 2014, we translocated Podarcis erhardii lizards from a large, predator-rich island to each of five replicate predator-free islets. Mean population densities increased fivefold over the following 4 years and bite scars suggest significantly more intraspecific fighting among these experimental populations. In 2018, we analysed the chemical signal design of males in each of the experimental populations and compared it to the chemical signals of the source population. We found that males consistently presented a significantly more complex chemical signal compared to the source population. Moreover, their chemical signals were marked by high proportions of octadecanoic acid, oleic acid and α-tocopherol, the three compounds that are known to be associated with lizard territoriality and mate choice. Our island introduction experiment thus suggests that the chemical signal design of animals can shift rapidly and predictably in novel ecological contexts.

Environmental temperatures shape thermal physiology as well as diversification and genome-wide substitution rates in lizards.

Climatic conditions changing over time and space shape the evolution of organisms at multiple levels, including temperate lizards in the family Lacertidae. Here we reconstruct a dated phylogenetic tree of 262 lacertid species based on a supermatrix relying on novel phylogenomic datasets and fossil calibrations. Diversification of lacertids was accompanied by an increasing disparity among occupied bioclimatic niches, especially in the last 10 Ma, during a period of progressive global cooling. Temperate species also underwent a genome-wide slowdown in molecular substitution rates compared to tropical and desert-adapted lacertids. Evaporative water loss and preferred temperature are correlated with bioclimatic parameters, indicating physiological adaptations to climate. Tropical, but also some populations of cool-adapted species experience maximum temperatures close to their preferred temperatures. We hypothesize these species-specific physiological preferences may constitute a handicap to prevail under rapid global warming, and contribute to explaining local lizard extinctions in cool and humid climates.

Promoting evolution: the brand new Hellenic Evolutionary Society (HEVOS).

Herein we present the recently founded Hellenic Evolutionary Society (HEVOS) that has been recently instituted to promote evolution and scientific thinking among the Greek-speaking public. HEVOS is a timely initiative, given the low levels of acceptance of evolution by Greek society and the almost complete lack of evolution teaching in primary and secondary education in Greece. Herein, the main aims of the Society are presented.

Habitat shapes the thermoregulation of Mediterranean lizards introduced to replicate experimental islets.

Both environmental temperatures and spatial heterogeneity can profoundly affect the biology of ectotherms. In lizards, thermoregulation may show high plasticity and may respond to environmental shifts. In the context of global climate change, lizards showing plastic thermoregulatory responses may be favored. In this study, we designed an experiment to evaluate the extent to which lizard thermoregulation responds to introduction to a new environment in a snapshot of time. In 2014, we captured individuals of the Aegean Wall lizard (Podarcis erhardii) from Naxos Island (429.8 km2) and released them onto two small, lizard-free islets, Galiatsos (0.0073 km2) and Kampana (0.004 km2) (Aegean Sea, Greece). In 2017, we returned to the islets and estimated the effectiveness (E), accuracy and precision of thermoregulation measuring operative, preferred (Tpref) and body temperatures. We hypothesized that the three habitats would differ in thermal quality and investigated the extent to which lizards from Naxos demonstrate plasticity when introduced to the novel, islet habitats. Thermal parameters did not differ between Galiatsos and Naxos and this was reflected in the similar E and Tpref. However, lizards from Kampana deviated in all focal traits from Naxos, resulting in higher E and a preference for higher Tpref. In sum, Naxos lizards shifted their thermoregulatory profile due to the idiosyncratic features of their new islet habitat. Our results advocate a high plasticity in lizard thermoregulation and suggest that there is room for effective responses to environmental changes, at least for Podarcis lizards in insular habitats.

Partitioning thermal habitat on a vertical rock, a herculean task.

Species occurring in sympatry have to effectively segregate their niche in order to co-exist. In the case of ectotherms in particular, the very important parameter of thermal biology has to be taken into account. Here we investigated the thermoregulatory effectiveness (E) of two endemic Greek lizards (Hellenolacerta graeca and Podarcis peloponnesiacus) that live syntopically on a rocky cliff in the Peloponnese. We presumed that the two species would select different microhabitats, to avoid interspecific competition, and follow a similar thermoregulation pattern as they experience the same conditions. We also expected that E values for both species would differ depending on the season. Overall, we found that the two species had similar E values for each season but differentiated partial thermoregulatory attributes. Though they both occurred in the same types of microhabitat, H. graeca selected higher sites (average 99cm above ground) than P. peloponnesiacus (average 44cm). Also, the latter achieved higher preferred temperatures during summer and winter. Finally, the effectiveness of thermoregulation for both species varied interseasonally and received its highest values during summer, in response to the lowest thermal quality that was observed then. Similar studies stress the importance of thermal shifts for ectotherm co-existence.

Living in sympatry: The effect of habitat partitioning on the thermoregulation of three Mediterranean lizards.

The ability for effective, accurate and precise thermoregulation is of paramount importance for ectotherms. Sympatric lizards often partition their niche and select different microhabitats. These microhabitats, however, usually differ in their thermal conditions and lizards have to adapt their thermoregulation behavior accordingly. Here, we evaluated the impact of habitat partitioning on the thermal biology of three syntopic, congeneric lacertids (Podarcis peloponnesiacus, P. tauricus and P. muralis) from central Peloponnese, Greece. We assessed thermoregulation effectiveness (E) using the three standard thermal parameters: body (Tb), operative (Te) and preferred (Tpref) temperatures. We hypothesized that the microhabitats used by each species would differ in thermal quality. We also predicted that all species would effectively thermoregulate, as they inhabit a thermally challenging mountain habitat. As expected, the partition of the habitat had an effect on the thermoregulation of lizards since microhabitats had different thermal qualities. All three species were effective and accurate thermoregulators but one of them achieved smaller E values as a result of the lower Tb in the field. This discrepancy could be attributed to the cooler (but more benign) thermal microhabitats that this species occupies.