Foraging mode constrains the evolution of cephalic horns in lizards and snakes.

A phylogenetically diverse minority of snake and lizard species exhibit rostral and ocular appendages that substantially modify the shape of their heads. These cephalic horns have evolved multiple times in diverse squamate lineages, enabling comparative tests of hypotheses on the benefits and costs of these distinctive traits. Here, we demonstrate correlated evolution between the occurrence of horns and foraging mode. We argue that although horns may be beneficial for various functions (e.g. camouflage, defence) in animals that move infrequently, they make active foragers more conspicuous to prey and predators, and hence are maladaptive. We therefore expected horns to be more common in species that ambush prey (entailing low movement rates) rather than in actively searching (frequently moving) species. Consistent with that hypothesis, our phylogenetic comparative analysis of published data on 1939 species reveals that cephalic horns occur almost exclusively in sit-and-wait predators. This finding underlines how foraging mode constrains the morphology of squamates and provides a compelling starting point for similar studies in other animal groups.

Gender differences in animal cognition science.

Women's representation in science is increasing steadily, with some fields closing gender parity in terms of participation and scientific output. Animal cognition appears to fall into that category. Our current analysis of gender author balance (women versus men) in 600 animal cognition papers supported parity in many aspects, but also revealed some remaining disparities. Women animal cognition scientists often held first authorship positions (58% of the studies), received similar numbers of citations, and published in equally high impact factor journals as men. Women were still under represented in last-author position, which often reflects seniority status (37% of last authors were women). There were interesting results when we considered the gender of teams (of two or more authors): all-women author teams were the minority in our dataset and received on average fewer citations than all men or mixed author teams, regardless of the quality of the journal (as measured by the journal's impact factor). Women more often focussed on mammals, whereas men more often focussed on fish, both as first authors and as same-gender teams. Men, as first author or in men-only teams, restricted their research more often to organisms of a single sex, compared to women, as first author and as members of a team. Our study suggests that there are many indices of the significant contribution of both women and men scientists in animal cognition, although some gender biases may remain.

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.

How to behave when marooned: the behavioural component of the island syndrome remains underexplored.

Animals on islands typically depart from their mainland relatives in assorted aspects of their biology. Because they seem to occur in concert, and to some extent evolve convergently in disparate taxa, these changes are referred to as the 'island syndrome'. While morphological, physiological and life-history components of the island syndrome have received considerable attention, much less is known about how insularity affects behaviour. In this paper, we argue why changes in personality traits and cognitive abilities can be expected to form part of the island syndrome. We provide an overview of studies that have compared personality traits and cognitive abilities between island and mainland populations, or among islands. Overall, the pickings are remarkably slim. There is evidence that animals on islands tend to be bolder than on the mainland, but effects on other personality traits go either way. The evidence for effects of insularity on cognitive abilities or style is highly circumstantial and very mixed. Finally, we consider the ecological drivers that may induce such changes, and the mechanisms through which they might occur. We conclude that our knowledge of the behavioural and cognitive responses to island environments remains limited, and we encourage behavioural biologists to make more use of these 'natural laboratories for evolution'.

Trace element concentrations in caudal scutes from Crocodylus moreletii and Crocodylus acutus in Belize in relation to biological variables and land use.

Crocodylus moreletii (Morelet's crocodile) and Crocodylus acutus (American crocodile) are generalist, apex predators of subtropical aquatic habitats in Central America. As top predators, crocodiles may be exposed to high levels of micro pollutants, such as trace elements via bioaccumulation that enter the food web as a consequence of human activities. As such, the status of their population can be considered indicative of that of the entire ecosystem - i.e., crocodiles constitute as genuine indicator species. In this study, we report on the concentrations of trace elements found in the caudal scutes of 178 specimens of C. acutus and C. moreletii from Belize. Our objectives were three-fold: (1) to assess variation in trace element concentration between species, sexes, age classes and body index; (2) to identify areas with elevated exposure to trace elements by comparing concentrations in the scutes of crocodiles at various sites in Belize; and (3) to explore links between crocodile trace element load and local land use. All elements tested (Hg, Pb, Cd, As, Cu, Zn, Co) could be detected in at least some scutes. Many of the readings of As and Co were under or close to the detection limit and were not further analyzed. Relatively high Hg concentrations were observed in adults from Chiquibul Forest (median 3.170 µg/g) and Ambergris Caye (0.834 µg/g). Concentrations of Hg and Pb tended to be higher in adult animals than in juveniles, especially in C. acutus. On the other hand, concentrations of Cd, Cu and Zn were higher in juveniles than in subadult adult animals. Concentrations of Cu were higher in C. acutus than in C. moreletii, but otherwise no species-effects were found for the other trace elements. We found a negative correlation between Hg and Zn concentrations; correlations among Cd, Pb, Cu and Zn concentrations tended to be positive. In both juveniles and adults, animals with high concentrations of Zn had lower body-indices (a proxy for physiological condition). None of the other element concentrations correlated with the body-index. Specimens of C. acutus were more often sampled at coastal sites, while C. moreletii sampling points were typically closer to agricultural or forested areas. A canonical correlation analysis revealed a significant association between trace element load and habitat characteristics. Animals sampled inland, near submontane forests, contained higher levels of Hg, while animals sampled near agricultural, urban or lowland habitats tended to have higher concentrations of Cd, Pb, Cu and Zn. This study identifies the most prevalent trace element concentrations impacting Belizean watersheds while highlighting the exposure risk to non-essential trace elements in less-urbanised areas or protected areas.

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.

Convergent evolution of skin surface microarchitecture and increased skin hydrophobicity in semi-aquatic anole lizards.

Animals that habitually cross the boundary between water and land face specific challenges with respect to locomotion, respiration, insulation, fouling and waterproofing. Many semi-aquatic invertebrates and plants have developed complex surface microstructures with water-repellent properties to overcome these problems, but equivalent adaptations of the skin have not been reported for vertebrates that encounter similar environmental challenges. Here, we document the first evidence of evolutionary convergence of hydrophobic structured skin in a group of semi-aquatic tetrapods. We show that the skin surface of semi-aquatic species of Anolis lizards is characterized by a more elaborate microstructural architecture (i.e. longer spines and spinules) and a lower wettability relative to closely related terrestrial species. In addition, phylogenetic comparative models reveal repeated independent evolution of enhanced skin hydrophobicity associated with the transition to a semi-aquatic lifestyle, providing evidence of adaptation. Our findings invite a new and exciting line of inquiry into the ecological significance, evolutionary origin and developmental basis of hydrophobic skin surfaces in semi-aquatic lizards, which is essential for understanding why and how the observed skin adaptations evolved in some and not other semi-aquatic tetrapod lineages.

The Effect of Long Term Captivity on Stress Levels in Anolis carolinensis Lizards.

The effect of long term captivity is a factor that is important for all research utilizing wild caught animals. Despite the fact that it can be considered to be one of the most fundamental potential sources of stress in captivity, it has received a low amount of interest in recent research on lizards. Given the wide variety in ecology and life history among lizards species, it would make sense to investigate the effect of long term captivity on wild caught lizards on a broader scale. In this study we investigated the effect of long term captivity (four months) on the physiology and behavior of male and female Anolis carolinensis lizards. Our results showed no negative effects of four months of captivity on physiological and behavioral measurements in male A carolinensis lizards. Similar results for females were found for all measurements except body mass and tail width. Here our results indicated a potential negative effect of four months of captivity on body mass and tail width in females.

Toxin variation among salamander populations: discussing potential causes and future directions.

Amphibians produce defensive chemicals which provide protection against both predators and infections. Within species, populations can differ considerably in the composition and amount of these chemical defenses. Studying intraspecific variation in toxins and linking it to environmental variables may help us to identify the selective drivers of toxin evolution, such as predation pressure and infection risk. Recently, there has been a renewed interest in the unique toxins produced by salamanders from the genus Salamandra: the samandarines. Despite this attention, intraspecific variation has largely been ignored within Salamandra-species. The aim of this study was to investigate whether geographic variation in profiles of samandarines exists, by sampling 4 populations of Salamandra atra over its range in the Dinaric Alps. In addition, we preliminary explored whether potential variation could be explained by predation (counting the number of snake species) and infection risk (cultivation and genomic analyses of collected soil samples). Salamanders from the 4 populations differed in toxin composition and in the size of their poison glands, although not in overall toxin quantity. Nor predation nor infection risk could explain this variation, as populations barely differed in these variables. Sampling over a much broader geographic range, using better estimators for predation and infection risk, will contribute to an improved understanding of how environment may shape variation in chemical defenses. Nevertheless, as the 4 populations of S. atra did differ in their toxin profiles, we propose that this species provides an interesting opportunity for further ecological and evolutionary studies on amphibian toxins.

The island syndrome.

Simon Baeckens and Raoul Van Damme introduce the phenotypic changes animals and plants undergo when inhabiting islands.

The (dis)advantages of dominance in a multiple male group of Anolis carolinensis lizards.

Male Anolis carolinensis lizards will fight and form social dominance hierarchies when placed in habitats with limited resources. Dominance may procure benefits such as priority access to food, shelter or partners, but may also come with costs, such as a higher risk of injuries due to aggressive interaction, a higher risk of predation or a higher energetic cost, all of which may lead to an increase in stress. While most research looks at dominance by using dyadic interactions, in our study we investigated the effect of dominance in a multiple male group of A. carolinensis lizards. Our results showed that dominant males in a multiple male group had priority access to prey and potential sexual partners but may run a higher risk of predation. We could not confirm that dominant males in a multiple male group had a higher risk of injuries from aggressive interactions or a higher energetic cost by being dominant. Overall our results seem to indicate that dominant male A. carolinensis lizards in a multiple male group obtain clear benefits and that they outweigh the disadvantages.

Convergent Evolution of Claw Shape in a Transcontinental Lizard Radiation.

Species occupying similar selective environments often share similar phenotypes as the result of natural selection. Recent discoveries, however, have led to the understanding that phenotypes may also converge for other reasons than recurring selection. We argue that the vertebrate claw system constitutes a promising but understudied model system for testing the adaptive nature of phenotypic, functional, and genetic convergence. In this study, we combine basic morphometrics and advanced techniques in form analysis to examine claw shape divergence in a transcontinental lizard radiation (Lacertidae). We find substantial interspecific variation in claw morphology and phylogenetic comparative statistics reveal a strong correlation with structural habitat use: ground-dwelling species living in open areas are equipped with long, thick, weakly curved, slender-bodied claws, whereas climbing species carry high, short, strongly curved, full-bodied claws. Species occupying densely vegetated habitats tend to carry intermediately shaped claws. Evolutionary models suggest that claw shape evolves toward multiple adaptive peaks, with structural habitat use pulling species toward a specific selective optimum. Contrary to findings in several other vertebrate taxa, our analyses indicate that environmental pressures, not phylogenetic relatedness, drive convergent evolution of similarly shaped claws in lacertids. Overall, our study suggests that lacertids independently evolved similarly shaped claws as an adaptation to similar structural environments in order to cope with the specific locomotory challenges posed by the habitat. Future biomechanical studies that link form and function in combination with genomic and development research will prove valuable in better understanding the adaptive significance of claw shape divergence.

Where to do number two: Lizards prefer to defecate on the largest rock in the territory.

Many animals use their excrements to communicate with others. In order to increase signal efficacy, animals often behaviourally select for specific defecation sites that maximize the detectability of their faecal deposits, such as the tip of rocks by some lizard species. However, the field conditions in which these observations are made make it difficult to reject alternative explanations of defecation site preference; rock tips may also provide better opportunities for thermoregulation, foraging, or escaping predators, and not solely for increasing the detectability of excrements. In addition, we still know little on whether lizard defecation behaviour varies within-species. In this laboratory study, we take an experimental approach to test defecation site preference of Podarcis melisellensis lizards in a standardized setting, and assess whether preferences differ between sexes, and among populations. Our findings show that in an environment where all stones provide equal thermoregulatory advantage, prey availability, and predator pressure, lizards still select for the largest stone in their territory as preferred defecation site. Moreover, we demonstrate that lizards' defecation preference is a strong conservative behaviour, showing no significant intraspecific variation. Together, these findings corroborate the idea that lizards may defecate on prominent rocky substrates in order to increase (visual) detectability of the deposited faecal pellets.

Habitat use and vestibular system's dimensions in lacertid lizards.

The vestibular system is crucial for movement control during locomotion. As the dimensions of the vestibular system determine the fluid dynamics of the endolymph and, as such, the system's function, we investigate the interaction between vestibular system size, head size and microhabitat use in lizards. We grouped 24 lacertid species in three microhabitat types, we acquired three-dimensional models of the bony vestibular systems using micro-computer tomography scanning, and we performed linear and surface measurements. All vestibular measurements scale with a negative allometry with head size, suggesting that smaller heads house disproportionally large ears. As the sensitivity of the vestibular system is positively related to size, a sufficiently large vestibular system in small-headed animals may meet the sensitivity demands during challenged locomotion. We also found that the microhabitat affects the locomotor dynamics: lizards inhabiting open microhabitats run at higher dimensionless speeds. On the other hand, no statistical relationship exists between dimensionless speed and the vestibular system dimensions. Hence, if the vestibular size would differ between microhabitats, this would be a direct effect (i.e. imposed, for instance, by requirements for manoeuvring, balance control, etc.), rather than depending on the lizards' intrinsic running speed. However, we found no effect of the microhabitat on the allometric relationship between head and vestibular system size. The finding that microhabitat is not reflected in the vestibular system size (hence sensitivity) of the lacertids in this study is possibly due to spatial constraints of the skull.

On dangerous ground: the evolution of body armour in cordyline lizards.

Animal body armour is often considered an adaptation that protects prey against predatory attacks, yet comparative studies that link the diversification of these allegedly protective coverings to differential predation risk or pressure are scarce. Here, we examine the evolution of body armour, including spines and osteoderms, in Cordylinae, a radiation of southern African lizards. Using phylogenetic comparative methods, we attempt to identify the ecological and environmental correlates of body armour that may hint at the selective pressures responsible for defensive trait diversification. Our results show that species inhabiting arid environments are more likely to possess elaborated body armour, specifically osteoderms. We did not find any effect of estimated predation pressure or risk on the degree of body armour. These findings suggest that body armour might not necessarily evolve in response to direct interactions with predators, but rather as a result of increased habitat-mediated predation risk. Furthermore, we discuss the possibility that osteoderms might have been shaped by factors unrelated to predation.

The brown anole dewlap revisited: do predation pressure, sexual selection, and species recognition shape among-population signal diversity?

Animal signalling structures are amongst the most variable characteristics, as they are subjected to a diversity of selection pressures. A well-known example of a diverse signalling system in the animal kingdom is the dewlap of Anolis lizards. Dewlap characteristics can vary remarkably among and within species, and also between sexes. Although a considerable amount of studies have attempted to disentangle the functional significance of the staggering dewlap diversity in Anolis, the underlying evolutionary processes remain elusive. In this study, we focus on the contribution of biotic selective pressures in shaping geographic variation in dewlap design (size, colour, and pattern) and dewlap display behaviour at the intraspecific level. Notably, we have tried to replicate and extend previously reported results hereof in both sexes of the brown anole lizard (Anolis sagrei). To do this, we assembled a dataset consisting of 17 A. sagrei heterogeneous island populations from the Caribbean and specifically tested whether predation pressure, sexual selection, or species recognition could explain interpopulational variation in an array of dewlap characteristics. Our findings show that in neither males nor females estimates of predation pressure (island size, tail break frequency, model attack rate, presence of predatory Leiocephalus lizards) or sexual selection (sexual size dimorphism) could explain variation in dewlap design. We did find that A. sagrei males from larger islands showed higher dewlap display intensities than males from smaller islands, but the direct connection with predation pressure remains ambiguous and demands further investigation. Last, we could show indirect support for species recognition only in males, as they are more likely to have a 'spotted' dewlap pattern when co-occurring with a higher number of syntopic Anolis species. In conclusion, we found overall limited support for the idea that the extensive interpopulational variability in dewlap design and use in A. sagrei is mediated by variation in their biotic environment. We propose a variety of conceptual and methodological explanations for this unexpected finding.

Intraspecific Variation in the Information Content of an Ornament: Why Relative Dewlap Size Signals Bite Force in Some, But Not All Island Populations of Anolis sagrei.

In many animals, male secondary sexual traits advertise reliable information on fighting capacity in a male-male context. The iconic sexual signaling device of anole lizards, the dewlap, has been extensively studied in this respect. For several territorial anole species (experiencing strong intrasexual selection), there is evidence for a positive association between dewlap size and bite capacity, which is an important determinant of combat outcome in lizards. Intriguingly, earlier studies did not find this expected correlation (relative dewlap size-relative bite force) in the highly territorial brown anole lizard, Anolis sagrei. We hypothesize that the dewlap size-bite force relationship can differ among populations of the same species due to interpopulation variation in the degree of male-male competition. In line with this thought, we expect dewlap size to serve as a reliable predictor of bite performance only in those populations where the level of intrasexual selection is high. To tackle this hypothesis, we examined the relationship between male dewlap size and bite force on the intraspecific level in A. sagrei, using an extensive dataset encompassing information from 17 island populations distributed throughout the Caribbean. First, we assessed and compared the relationship between both variables in the 17 populations under study. Second, we linked the relative dewlap size-bite force relationship within each population to variation in the degree of intrasexual selection among populations, using sexual size dimorphism and dewlap display intensity as surrogate measures. Our results showed that absolute dewlap size is an excellent predictor of maximum bite force in nearly all A. sagrei populations. However, relative dewlap size is only an honest signal of bite performance in 4 out of the 17 populations. Surprisingly, the level of signal honesty did not correlate with the strength of intrasexual selection. We offer a number of conceptual and methodological explanations for this unexpected finding.

Author Correction: Evolutionary morphology of the lizard chemosensory system.

A correction to this article has been published and is linked from the HTML version of this paper. The error has not been fixed in the paper.

The Role of Diet in Shaping the Chemical Signal Design of Lacertid Lizards.

Lizards communicate with others via chemical signals, the composition of which may vary among species. Although the selective pressures and constraints affecting chemical signal diversity at the species level remain poorly understood, the possible role of diet has been largely neglected. The chemical signals of many lizards originate from the femoral glands that exude a mixture of semiochemicals, and may be used in a variety of contexts. We analyzed the lipophilic fraction of the glandular secretions of 45 species of lacertid lizard species by gas chromatography/mass spectrometry. The proportions of nine major chemical classes (alcohols, aldehydes, fatty acids, furanones, ketones, steroids, terpenoids, tocopherols and waxy esters), the relative contributions of these different classes ('chemical diversity'), and the total number of different lipophilic compounds ('chemical richness') varied greatly among species. We examined whether interspecific differences in these chemical variables could be coupled to interspecific variation in diet using data from the literature. In addition, we compared chemical signal composition among species that almost never, occasionally, or often eat plant material. We found little support for the hypothesis that the chemical profile of a given species' secretion depends on the type of food consumed. Diet breadth did not correlate with chemical diversity or richness. The amount of plants or ants consumed did not affect the relative contribution of any of the nine major chemical classes to the secretion. Chemical diversity did not differ among lizards with different levels of plant consumption; however, chemical richness was low in species with an exclusive arthropod diet, suggesting that incorporating plants in the diet enables lizards to increase the number of compounds allocated to secretions, likely because a (partly) herbivorous diet allows them to include compounds of plant origin that are unavailable in animal prey. Still, overall, diet appears a relatively poor predictor of interspecific differences in the broad chemical profiles of secretions of lacertid lizards.

Evolutionary morphology of the lizard chemosensory system.

Foraging mode plays a pivotal role in traditional reconstructions of squamate evolution. Transitions between modes are said to spark concerted changes in the morphology, physiology, behaviour, and life history of lizards. With respect to their sensory systems, species that adopt a sit-and-wait strategy are thought to rely on visual cues primarily, while actively hunting species would predominantly use chemical information. The morphology of the tongue and the vomeronasal-organs is believed to mirror this dichotomy. Still, support for this idea of concerted evolution of the morphology of the lizard sensory system merely originates from studies comparing only a few, distantly related taxa that differ in many aspects of their biology besides foraging mode. Hence, we compared vomeronasal-lingual morphology among closely related lizard species (Lacertidae). Our findings show considerable interspecific variation indicating that the chemosensory system of lacertids has undergone substantial change over a short evolutionary time. Although our results imply independent evolution of tongue and vomeronasal-organ form, we find evidence for co-variation between sampler and sensor, hinting towards an 'optimization' for efficient chemoreception. Furthermore, our findings suggest species' degree of investment in chemical signalling, and not foraging behaviour, as a leading factor driving the diversity in vomeronasal-lingual morphology among lacertid species.