Panayiotis Pafilis

Phylogeography of Balkan wall lizard (Podarcis taurica) and its relatives inferred from mitochondrial DNA sequences

Wall lizards of the genus Podarcis (Sauria, Lacertidae) comprise 17 currently recognized species in southern Europe, where they are the predominant reptile group. The taxonomy of Podarcis is complex and unstable. Based on DNA sequence data the species of Podarcis falls into four main groups that have substantial geographical conherence (western island group, southwestern group, Italian group and Balkan group). The Balkan species are divided in two subgroups: the subgroup of Podarcis taurica (P. taurica, P. milensis, P. gaigeae and perhaps P. melisellensis), and the subgroup of Podarcis erhardii (P. erhardii and P. peloponnesiaca). We addressed the question of phylogenetic relations among the species of the P. taurica subgroup encountered in Greece, as they can be inferred from partial mtDNA (cyt b and 16S) sequences. Our data support the monophyly of P. taurica subgroup and suggest that P. gaigeae, P. milensis and P. melisellensis form a clade, which thereinafter connects to P. taurica. Within the previous clade, P. gaigeae is more closely related to P. milensis than to P. melisellensis. However, the specimens of P. taurica were subdivided in two different groups. The first one includes the specimens from northeastern Greece, and the other group includes the specimens from the rest of continental Greece and Ionian islands. Because the molecular clock of the cyt b and 16 rRNA genes was not rejected in our model test, it is possible to estimate times of speciation events. Based on the splitting of the island of Crete from Peloponnisos [c. 5 million years ago (Ma)], the evolutionary rate for the cyt b is 1.55% per million years (Myr) and for the 16S rRNA is 0.46% per Myr. These results suggest that the evolutionary history of P. taurica in Greece is more complex than a single evolutionary invasion. The data analysed, stress the need for a reconsideration of the evolutionary history of Greek Podarcis species and help overcome difficulties that classical taxonomy has encountered at both the species level.

Intraspecific competition and high food availability are associated with insular gigantism in a lizard

Resource availability, competition, and predation commonly drive body size evolution. We assess the impact of high food availability and the consequent increased intraspecific competition, as expressed by tail injuries and cannibalism, on body size in Skyros wall lizards (Podarcis gaigeae). Lizard populations on islets surrounding Skyros (Aegean Sea) all have fewer predators and competitors than on Skyros but differ in the numbers of nesting seabirds. We predicted the following: (1) the presence of breeding seabirds (providing nutrients) will increase lizard population densities; (2) dense lizard populations will experience stronger intraspecific competition; and (3) such aggression, will be associated with larger average body size. We found a positive correlation between seabird and lizard densities. Cannibalism and tail injuries were considerably higher in dense populations. Increases in cannibalism and tail loss were associated with large body sizes. Adult cannibalism on juveniles may select for rapid growth, fuelled by high food abundance, setting thus the stage for the evolution of gigantism.

Island biology and morphological divergence of the Skyros wall lizard Podarcis gaigeae : a combined role for local selection and genetic drift on color morph frequency divergence?

BackgroundPatterns of spatial variation in discrete phenotypic traits can be used to draw inferences about the adaptive significance of traits and evolutionary processes, especially when compared to patterns of neutral genetic variation. Population divergence in adaptive traits such as color morphs can be influenced by both local ecology and stochastic factors such as genetic drift or founder events. Here, we use quantitative color measurements of males and females of Skyros wall lizard, Podarcis gaigeae, to demonstrate that this species is polymorphic with respect to throat color, and the morphs form discrete phenotypic clusters with limited overlap between categories. We use divergence in throat color morph frequencies and compare that to neutral genetic variation to infer the evolutionary processes acting on islet- and mainland populations.ResultsGeographically close islet- and mainland populations of the Skyros wall lizard exhibit strong divergence in throat color morph frequencies. Population variation in throat color morph frequencies between islets was higher than that between mainland populations, and the effective population sizes on the islets were small (Ne:s < 100). Population divergence (FST) for throat color morph frequencies fell within the neutral FST-distribution estimated from microsatellite markers, and genetic drift could thus not be rejected as an explanation for the pattern. Moreover, for both comparisons among mainland-mainland population pairs and between mainland-islet population pairs, morph frequency divergence was significantly correlated with neutral divergence, further pointing to some role for genetic drift in divergence also at the phenotypic level of throat color morphs.ConclusionsGenetic drift could not be rejected as an explanation for the pattern of population divergence in morph frequencies. In spite of an expected stabilising selection, throat color frequencies diverged in the islet populations. These results suggest that there is an interaction between selection and genetic drift causing divergence even at a phenotypic level in these small, subdivided populations.

Tail Shedding in Island Lizards [Lacertidae, Reptilia]: Decline of Antipredator Defenses in Relaxed Predation Environments

The ability of an animal to shed its tail is a widespread antipredator strategy among lizards. The degree of expression of this defense is expected to be shaped by prevailing environmental conditions including local predation pressure. We test these hypotheses by comparing several aspects of caudal autotomy in 15 Mediterranean lizard taxa existing across a swath of mainland and island localities that differ in the number and identity of predator species present. Autotomic ease varied substantially among the study populations, in a pattern that is best explained by the presence of vipers. Neither insularity nor the presence of other types of predators explain the observed autotomy rates. Final concentration of accumulated tail muscle lactate and duration of movement of a shed tail, two traits that were previously thought to relate to predation pressure, are in general not shaped by either predator diversity or insularity. Under conditions of relaxed predation selection, an uncoupling of different aspects of caudal autotomy exists, with some elements (ease of autotomy) declining faster than others (duration of movement, lactate concentration). We compared rates of shed tails in the field against rates of laboratory autotomies conducted under standardized conditions and found very high correlation values (r > 0.96). This suggests that field autotomy rates, rather than being a metric of predatory attacks, merely reflect the innate predisposition of a taxon to shed its tail.

Effects of fragmentation on genetic diversity in island populations of the Aegean wall lizard Podarcis erhardii (Lacertidae, Reptilia).

Landbridge islands offer unique opportunities for understanding the effects of fragmentation history on genetic variation in island taxa. The formation of islands by rising sea levels can be likened to a population bottleneck whose magnitude and duration is determined by island area and time since isolation, respectively. The Holocene landbridge islands of the Aegean Sea (Greece) were formed since the last glacial maximum and constitute an ideal system for disentangling the effects of island area, age and geographic isolation on genetic variability. Of the many reptile species inhabiting this island system, the Aegean wall lizard Podarcis erhardii is an excellent indicator of fragmentation history due to its widespread distribution and poor over-water dispersal abilities. In this study, we utilize a detailed record of Holocene fragmentation to investigate the effects of island history on wall lizard mitochondrial and nuclear microsatellite diversity. Findings show that the spatial distribution of mitochondrial haplotypes reflects historical patterns of fragmentation rather than geographic proximity per se. In keeping with neutral bottleneck theory, larger and younger islands retain more nuclear genetic variation than smaller, older islands. Conversely, there is no evidence of an effect of isolation by distance or effect of distance to the nearest larger landmass on genetic variability, indicating little gene flow between islands. Lastly, population-specific measures of genetic differentiation are inversely correlated with island area, suggesting that smaller islands exhibit greater divergence due to their greater susceptibility to drift. Taken together, these results suggest that both island area and time since isolation are important predictors of genetic variation and that these patterns likely arose through the progressive fragmentation of ancestral diversity and the ensuing cumulative effects of drift.

Reproductive Biology of Insular Reptiles: Marine Subsidies Modulate Expression of the “Island Syndrome”

Abstract Differences in ecological conditions can result in the evolution of dramatic inter-population shifts in whole suites of traits. We studied variation in reproductive output in three lizard populations of the Skyros Wall Lizard (Podarcis gaigeae, Lacertidae) endemic to the Skyros Archipelago (Greece), which live under similar climatic conditions but differ in predation pressure and food availability. Based on the “island syndrome” hypothesis, we predicted that females from island populations would produce larger, but fewer offspring. The study populations differ conspicuously in average body size, with males from the satellite Lakonissi and Diavates islets being respectively 20% and 39% larger than males from the main Skyros Island. Lizards from these predator-free islets produced eggs of larger size than the main Skyros population; however, they also produced significantly larger clutches than the Skyros population (2.31±0.83 and 2.73±1.0 vs. 1.97±0.58 eggs). All inter-population differences in clutch size, clutch volume, and egg size were explained by corresponding differences in average body size of the dams, revealing that across all populations, reproductive effort scaled similarly with maternal body size. There was no evidence of trade-offs between egg size and clutch size as generally encountered in many reptile taxa. The occurrence of this unusual pattern of reproductive investment among islet populations of giants is probably best explained by the occurrence of two underlying drivers: first, the substantial marine subsidies by resident seabird colonies and second, the existence of intense cannibalistic behaviors in the form of attacks to the tail and severe intraspecific predation on juveniles. This suggests that subsidies-driven gigantism in island endemics may free species from such trade-offs and allow a population to maximize reproductive output in multiple, normally conflicting dimensions.

Digestive performance in five Mediterranean lizard species: effects of temperature and insularity.

Temperature sensitivity of digestive processes has important ramifications for digestive performance in ectothermic vertebrates. We conducted a comparative analysis of temperature effects on digestive processes [gut passage times (GPTs) and apparent digestive efficiencies (ADEs)] in five lacertid lizards occurring in insular (Podarcis erhardii, P. gaigeae), and mainland (P. muralis, P. peloponnesiaca, Lacerta graeca) Mediterranean environments. GPTs were negatively correlated to temperature with mainland taxa having 10–20% longer GPTs than island taxa. In contrast to previous studies that estimate ADEs using bomb calorimetry, we compare ADEs by analyzing discrete efficiencies for lipids, sugars and proteins at three temperature regimes (20, 25, and 30°C); each of these categories produces different results. ADEs for lipids and sugars showed a monotonic increase with temperature whereas ADEs for proteins decreased with temperature. Island taxa had consistently higher ADEs than their mainland counterparts for lipids and for proteins but not for sugars. They are characterized by superior energy acquisition abilities despite significantly shorter GPTs. Their increased digestive performance relative to the mainland species appears to allow them to maximize energy acquisition in unproductive island environments where food availability is spatially and seasonally clustered.

Comparative Postautotomy Tail Activity in Six Mediterranean Lacertid Lizard Species

Tail autotomy, the self‐induced tail separation from the body, is a common and effective antipredator mechanism in lizards. In this study, we examine the muscle energetics of tail shedding in six lacertid lizard species (Podarcis erhardii, Podarcis peloponnesiaca, Podarcis muralis, Podarcis gaigeae, Podarcis milensis, and Lacerta graeca) from the northeast Mediterranean region. Very long periods of postautotomy tail movement were demonstrated for all species (range = 6–8 min), and differences among species were not statistically significant. Postautotomy tail movement, powered by anaerobic muscle activity, resulted in a strong increase in lactate concentrations and a concomitant depletion of muscle glycogen of exhausted tails relative to resting tails. No significant differences were found in either lactate or glycogen concentrations among the species examined. Duration of movement was negatively correlated with final lactate concentrations. The lack of differentiation in postautotomy energetic physiology in this group of species that have evolved under very different predation environments indicates that postautotomy muscle metabolism involves an overall conservative suite of characters.

Evolution of antipredator behavior in an island lizard species, Podarcis erhardii (Reptilia: Lacertidae): The sum of all fears?

Organisms generally have many defenses against predation, yet may lack effective defenses if from populations without predators. Evolutionary theory predicts that “costly” antipredator behaviors will be selected against when predation risk diminishes. We examined antipredator behaviors in Aegean wall lizards, Podarcis erhardii, across an archipelago of land‐bridge islands that vary in predator diversity and period of isolation. We examined two defenses, flight initiation distance and tail autotomy. Flight initiation distance generally decreased with declining predator diversity. All predator types had distinctive effects on flight initiation distance with mammals and birds having the largest estimated effects. Rates of autotomy observed in the field were highest on predator‐free islands, yet laboratory‐induced autotomy increased linearly with overall predator diversity. Against expectation from previous work, tail autotomy was not explained solely by the presence of vipers. Analyses of populations directly isolated from rich predator communities revealed that flight initiation distance decreased with increased duration of isolation in addition to the effects of current predator diversity, whereas tail autotomy could be explained simply by current predator diversity. Although selection against costly defenses should depend on time with reduced threats, different defenses may diminish along different trajectories even within the same predator–prey system.

The number of competitor species is unlinked to sexual dimorphism

Sexual size dimorphism (SSD) can allow males and females of the same species to specialize on different sized food items and therefore minimize intraspecific competition. Interspecific competition, however, is thought to limit sexual dimorphism, as larger competitors in the community will prevent the larger sex from evolving larger size, and smaller species may prevent the smaller sex from becoming even smaller. We tested this prediction using data on the sexual size dimorphism of lizards, and mammalian carnivores, on islands world-wide. Because insular communities are depauperate, and guilds are species-poor, it is often assumed that enhanced sexual size dimorphism is common on islands. The intensity of interspecific competition, hindering enhanced dimorphism, is thought to increase with competitor richness. We tested whether intraspecific sexual size dimorphism of mammalian carnivores and lizards decreases with increasing island species richness. We further computed the average sexual dimorphism of species on islands and tested whether species-rich islands are inhabited by relatively monomorphic species. Within families and guilds across carnivores and lizards, and with both intraspecific and interspecific approaches, we consistently failed to find support for the notion that species-poor islands harbour more sexually dimorphic individuals or species. We conclude that either interspecific competition does not affect the sexual size dimorphism of insular lizards and carnivores (i.e. character displacement and species sorting are rare in these taxa), or that the number of species in an assemblage or guild is a poor proxy for the intensity of interspecific competition in insular assemblages.