Repeated origin and loss of adhesive toepads in geckos

Geckos are well known for their extraordinary clinging abilities and many species easily scale vertical or even inverted surfaces. This ability is enabled by a complex digital adhesive mechanism (adhesive toepads) that employs van der Waals based adhesion, augmented by frictional forces. Numerous morphological traits and behaviors have evolved to facilitate deployment of the adhesive mechanism, maximize adhesive force and enable release from the substrate. The complex digital morphologies that result allow geckos to interact with their environment in a novel fashion quite differently from most other lizards. Details of toepad morphology suggest multiple gains and losses of the adhesive mechanism, but lack of a comprehensive phylogeny has hindered efforts to determine how frequently adhesive toepads have been gained and lost. Here we present a multigene phylogeny of geckos, including 107 of 118 recognized genera, and determine that adhesive toepads have been gained and lost multiple times, and remarkably, with approximately equal frequency. The most likely hypothesis suggests that adhesive toepads evolved 11 times and were lost nine times. The overall external morphology of the toepad is strikingly similar in many lineages in which it is independently derived, but lineage-specific differences are evident, particularly regarding internal anatomy, with unique morphological patterns defining each independent derivation.     

Whole-organism studies of adhesion in pad-bearing lizards: creative evolutionary solutions to functional problems

Understanding the evolution of complex functional traits is a challenge for evolutionary physiology. Here we investigate the evolution of subdigital toepads in lizards, which have arisen independently at least three times, although with subtle anatomical differences. Some designs (anole, gecko) appear functionally equivalent, whereas other designs (skink) are inferior. The functional equivalence of geckos and anoles highlights the creative aspect of the evolutionary process in that these two groups have arrived at the same functional endpoint along very different trajectories. However, this functional equivalence does not result in equivalence for performance at whole-organism tasks (e.g., running uphill), as the evolution of behavior (e.g., toe-furling) has enabled geckos to be superior climbers than anoles. We also show that adaptive increases in the toepad size within a closely related lizard genus (Anolis) has resulted in concomitant evolution of enhanced clinging ability and increased perch heights. A third insight is that pad-bearing geckos are capable of carrying tremendous loads (up to 250% of body weight) up smooth surfaces, and that the toepad itself does not appear limiting. This comparative and whole-organism approach to lizard toepads underscores how organisms can evolve multiple solutions to evolutionary problems.     

Key innovations and island colonization as engines of evolutionary diversification: a comparative test with the Australasian diplodactyloid geckos

The acquisition of key innovations and the invasion of new areas constitute two major processes that facilitate ecological opportunity and subsequent evolutionary diversification. Using a major lizard radiation as a model, the Australasian diplodactyloid geckos, we explored the effects of two key innovations (adhesive toepads and a snake‐like phenotype) and the invasion of new environments (island colonization) in promoting the evolution of phenotypic and species diversity. We found no evidence that toepads had significantly increased evolutionary diversification, which challenges the common assumption that the evolution of toepads has been responsible for the extensive radiation of geckos. In contrast, a snakelike phenotype was associated with increased rates of body size evolution and, to a lesser extent, species diversification. However, the clearest impact on evolutionary diversification has been the colonization of New Zealand and New Caledonia, which were associated with increased rates of both body size evolution and species diversification. This highlights that colonizing new environments can drive adaptive diversification in conjunction or independently of the evolution of a key innovation. Studies wishing to confirm the putative link between a key innovation and subsequent evolutionary diversification must therefore show that it has been the acquisition of an innovation specifically, not the colonization of new areas more generally, that has prompted diversification.     

The evolution of digit form in Gonatodes (Gekkota: Sphaerodactylidae) and its bearing on the transition from frictional to adhesive contact in gekkotans

Although the phenomenon of adhesion in geckos has been intensively studied for over 200 years, our understanding of how the morphological apparatus associated with this arose is less clear. Indeed, whether or not all of the intricate morphological hierarchy that is implicated in the attachment and removal of the adhesive setae originated at the same time is unknown. To explore whether setae may have arisen prior to the other parts of this structural hierarchy, we undertook morphological observations of Gonatodes, an ancestrally padless, sphaerodatyline genus known to exhibit the expression of incipient subdigital pads in some species. Focusing on this geographically and morphologically well‐circumscribed genus, for which intraspecific relationships are adequately known and ecology is quite well documented, allowed us to deduce trends in digit proportions, shape, scalation, and skeletal structure, and associate these with the micro‐ornamentation of the subdigital surfaces. Our findings indicate that in Gonatodes, setae capable of inducing adhesion are present without the modifications of the digital musculotendinous, circulatory and skeletal systems that are generally considered to be necessary for the operation of a functional adhesive apparatus. The acquisition of these latter characteristics (independently in many lineages of gekkotans, and incipiently so in Anolis) may have been preceded by a suite of modifications of the digits that enhanced static clinging in relation to sit‐and‐wait predation and the ability to take refuge on surfaces unavailable to other taxa. These possibilities await further testing. J. Morphol. 276:1311–1332, 2015. © 2015 Wiley Periodicals, Inc.     

Evolution of pedal digit orientation and morphology in relation to acquisition and secondary loss of the adhesive system in geckos

Among geckos, the acquisition of the adhesive system is associated with several morphological changes of the feet that are involved in the operation of the adhesive apparatus. However, analyses using a comparative framework are lacking. We applied traditional morphometrics and geometric morphometric analysis with phylogenetic comparative methods to morphological data, collected from X-ray scans, to examine patterns of morphological evolution of the pes in association with the gain and loss of adhesive capabilities, and with habitat occupancy among 102 species of gecko. Padbearing gecko lineages tend to have shorter digits and greater inter-digital angles than padless ones. Arboreal and saxicolous species have shorter digits than terrestrial species. Our results suggest repeated shifts that converge upon a similar padbearing morphology, with some modifications being associated with the habitat occupied. We demonstrate that functional innovation and habitat can operate on, and influence, different components of foot morphology.     

The relationship between habitat use and body shape in geckos

Geckos are a highly diverse group of lizards, with more than 1,700 species that exhibit a wide range of behaviors, ecologies, and sizes. However, no study has examined links between habitat use and body shape in pad-bearing geckos. We set out to answer a basic question using a data set of pad-bearing geckos (112 species, 103 pad-bearing, 9 padless, 42 genera): Do geckos that occur in different habitats also differ in body shape? Overall, we found that body shape was surprisingly similar among our sample of pad-bearing species, with the exception of the genus Uroplatus, which was clearly distinct from other geckos due to its depressed body and long limbs. However, the padless geckos differed in body shape from the pad-bearing geckos by having longer arms and legs and less rotund bodies. We found that about half of the pad-bearing species primarily inhabit trees, with the other half, divided approximately equally among rocks, the ground, and mixed habitats. We found no significant links between habitat use and body shape, nor any propensity for larger species to occupy different habitats than smaller species. Padless species tend to inhabit rock and ground substrates. Our results indicate that pad-bearing geckos have a relatively uniform body form, which contrasts with to their diversity in color, size, and behavior. Indeed, our data show that the general gecko body shape is suitable for a wide range of habitats, ranging from arboreal to terrestrial. This pattern is a departure from other ecomorphological studies and suggests that geckos may not easily fit into the mold of adaptive radiation, as suggested by prior studies.     

Sticky gecko feet: the role of temperature and humidity

Gecko adhesion is expected to be temperature insensitive over the range of temperatures typically experienced by geckos. Previous work is limited and equivocal on whether this expectation holds. We tested the temperature dependence of adhesion in Tokay and Day geckos and found that clinging ability at 12 degrees C was nearly double the clinging ability at 32 degrees C. However, rather than confirming a simple temperature effect, our data reveal a complex interaction between temperature and humidity that can drive differences in adhesion by as much as two-fold. Our findings have important implications for inferences about the mechanisms underlying the exceptional clinging capabilities of geckos, including whether performance of free-ranging animals is based solely on a dry adhesive model. An understanding of the relative contributions of van der Waals interactions and how humidity and temperature variation affects clinging capacities will be required to test hypotheses about the evolution of gecko toepads and is relevant to the design and manufacture of synthetic mimics.     

Information content in data sets for a nucleated-polymerization model

We illustrate the use of statistical tools (asymptotic theories of standard error quantification using appropriate statistical models, bootstrapping, and model comparison techniques) in addition to sensitivity analysis that may be employed to determine the information content in data sets. We do this in the context of recent models [S. Prigent, A. Ballesta, F. Charles, N. Lenuzza, P. Gabriel, L.M. Tine, H. Rezaei, and M. Doumic, An efficient kinetic model for assemblies of amyloid fibrils and its application to polyglutamine aggregation, PLoS ONE 7 (2012), e43273. doi:10.1371/journal.pone.0043273.] for nucleated polymerization in proteins, about which very little is known regarding the underlying mechanisms; thus, the methodology we develop here may be of great help to experimentalists. We conclude that the investigated data sets will support with reasonable levels of uncertainty only the estimation of the parameters related to the early steps of the aggregation process.     

Posture, speed, and habitat structure: three-dimensional hindlimb kinematics of two species of padless geckos

Differences in habitat use are often correlated with differences in morphology and behavior, while animals in similar habitats often exhibit similarities in form and function. However, this has not been tested extensively among lizards, especially geckos. Most studies of gecko locomotion have focused on the ability to adhere to surfaces. However, there are several species of geckos that have either secondarily lost adhesive capabilities or simply lack the capability. We quantified the three-dimensional locomotor kinematics for two desert-dwelling padless geckos, Teratoscincus scincus and Eublepharis macularius, on a level trackway over a range of speeds. Our results indicate that T. scincus landed with a high relative hip height of 48.7 ± 2.4% of total limb length at footfall, while E. macularius exhibited hip heights averaging only 36.0 ± 1.8% of total limb length for footfall. The three-dimensional knee angle of T. scincus averaged 120.6 ± 3.9° at footfall, while E. macularius averaged only 101.6 ± 1.8° at footfall. In addition, the femur of E. macularius was elevated to a much greater extent (i.e., was closer to being perpendicular to the long axis of the body) than that of T. scincus and every other lizard that has been studied, suggesting they move with a “hyper-sprawled” posture. Both of these gecko species live in deserts, but T. scincus is psammophilic while E. macularius inhabits a rocky, more densely vegetated environment. Benefits of the more upright posture of T. scincus on open sandy habitat may include a greater field of view and more efficient locomotion. The more sprawled posture of E. macularius may lower its center of gravity and aid in balance while climbing on rocks or shrubs.     

Identification of quantitative trait loci for productive tiller number and its relationship to agronomic traits in spring wheat

Productive tiller number (PTN), defined as the number of tillers that produce spikes and seeds, is a key component of grain yield in wheat. Spring wheat cultivars in the northern Great Plains of North America differ in PTN. The objectives of this study were (1) to determine the relationship of PTN to agronomic traits using recombinant inbred line (RIL) populations derived from crosses Reeder/Conan, McNeal/Thatcher and Reeder/McNeal grown under a range of environments, and (2) to identify and validate quantitative trait loci (QTL) associated with high PTN. Correlation between PTN and plot weight ranged from r = 0.4–0.6 among the populations based on combined means over years, and was positive in every environment for all crosses (P < 0.05). A genetic map generated for the Reeder/Conan RIL allowed identification of a QTL for PTN consistent over environments, located on chromosome 6B. The QTL on chromosome 6B (QTn.mst-6B) explained 9–17% of the variation of PTN and co-segregated with a QTL for yield in the Reeder/Conan RIL. QTn.mst-6B was validated by single marker analysis in the McNeal/Thatcher RIL, McNeal/Reeder RIL, and a set of near isogenic line (NIL) developed for QTn.mst-6B. The allele for high PTN significantly increased PTN by 8.7, 4, and 13% in the McNeal/Reeder RIL, McNeal/Thatcher RIL and Choteau/Reeder NIL, respectively. The allele for high PTN also had a significant positive effect on plot weight in the McNeal/Reeder RIL. Our results suggest that high PTN, controlled to a significant extent by QTn.mst-6B, contributed to increased yield potential over a range of environmental conditions. QTn.mst-6B may be useful for improving spring wheat in the northern Great Plains of North America and similar environments.     

Systematics of the Saharo‐Arabian clade of the Palearctic naked‐toed geckos with the description of a new species of Tropiocolotes endemic to Oman

Geckos are one of the most species‐rich, abundant, and widely distributed of all Squamata lineages and present several characteristics that have made them favorite model organisms for biogeographical, ecological, physiological, and evolutionary studies. One of the key aspects of any comparative study is to have a robust, comprehensive phylogeny, and an updated taxonomy. Recently, the Infraorder Gekkota has been the subject of several phylogenetic analyses and taxonomic revisions at different levels. Despite all these phylogenetic and taxonomic advances, there are still some groups whose systematics and taxonomy remain highly problematic. Maybe one of the most poorly resolved groups in spite of decades of intensive research by many herpetologists are the so‐called Palearctic naked‐toed geckos of the family Gekkonidae. This group of nocturnal geckos distributed from Mauritania across North Africa, Arabia, southwestern and central Asia to northern India, western China and southern Mongolia is characterized by the synapomorphy of lack of adhesive subdigital pads. Within the Palearctic naked‐toed geckos, the Saharo‐Arabian clade comprised by the genera Pseudoceramodactylus, Stenodactylus, and Tropiocolotes is the clade with the largest distribution range. At the same time, it is one of the problematic groups, presenting poorly supported phylogenetic relationships, with the genus Tropiocolotes being recovered non‐monophyletic in all analyses despite its morphological uniformity. To reassess the phylogeny of the Palearctic naked‐toed geckos with a special interest in the systematics of Tropiocolotes, we assembled a dataset comprising 298 gecko specimens from 283 different species (including all Tropiocolotes species but one) belonging to 122 of a total of 124 described gecko genera. This dataset included the nuclear c‐mos, ACM4, RAG1, RAG2, and PDC and the mitochondrial ND2 gene. To further investigate the relationships within Tropiocolotes and to revise the systematics of the south Arabian endemic species Tropiocolotes scorteccii, we used an integrative approach including information from the nuclear MC1R and c‐mos, the mitochondrial 12S, 16S, cytb genes, and morphological data from nine of the 10 described Tropiocolotes species. The phylogenetic analyses of the Gekkota dataset recovered a similar topology for the Palearctic naked‐toed geckos to previous studies, but in this case, Tropiocolotes was recovered monophyletic in all analyses, with high support in two of them. The results of the analyses of three datasets specifically assembled to test the effect of both gene sampling and taxon sampling in the monophyly of Tropiocolotes, and the internal relationships of the Palearctic naked‐toed geckos clearly showed that both the number and kind of characters (nuclear or mitochondrial data) and the number of taxa played a fundamental role in recovering the correct phylogenetic relationships. The phylogenetic analyses within Tropiocolotes suggested the existence of high levels of undescribed diversity in the south Arabian T. scorteccii, including a new genetically and morphologically distinct species endemic to Oman (Tropiocolotes confusus sp. nov. ). Our study using a large dataset, including several loci and a dense taxon sampling within Gekkota and especially within Tropiocolotes, has proved a valuable strategy to address the monophyly of Tropiocolotes and the relationships within the Saharo‐Arabian Palearctic naked‐toed geckos. The integrative systematic approach including several samples of south Arabian T. scorteccii based on many years of fieldwork has, once more, uncovered a new species endemic to this region. This highlights the importance of this area of Arabia as a reservoir of reptile endemicity and biodiversity, which is likely linked to the high degree of habitat heterogeneity and the effect of the monsoons. Obviously, based on this and previously published evidence, south Arabia represents an area with still high levels of undiscovered diversity.     

Social group composition modulates the role of last male sperm precedence in post-copulatory sexual selection

In many species, the order in which males mate with a female explains much of the variation in paternity arising from post-copulatory sexual selection. Research in Drosophila suggests that mating order may account for the majority of the variance in male reproductive success. However, the effects of mating order on paternity bias might not be static but could potentially vary with social or environmental factors. To test this idea, we used an existing dataset, collated from an experiment we previously published (Morimoto et al., PLoS One, 11, 2016, e0154468), with the addition of unpublished data from the same experiment. These previous experiments manipulated larval density in Drosophila melanogaster which generated variation in male and female body size, assembled groups of individuals of different sizes, and measured the mating success and paternity share of focal males. The data presented here provides information on each focal male's mating order and the frequency in which focal males remated with same females (‘repetitive matings’). We combined this information with our previously reported focal male reproductive success to partition variance in paternity into male mating order and repetitive matings across groups that differed in the body size composition of males and females. We found, as expected, that male mating order explained a considerable portion of the variance in male paternity. However, we also found that the impact of male mating order on male paternity was influenced by the body size composition of groups. Specifically, males that tended to mate last had a greater paternity advantage, and displayed lower variance, in groups containing a heterogenous mixture male body sizes than in groups with a single male body size. Repetitive mating only had a minor contribution to the variance in male paternity share across all experiments. Overall, our findings contribute to the growing body of research showing that post-copulatory sexual selection is subject to socio-ecological influences.     

The oncogenic transcription factor FOXM1 and anticancer therapy

Comment on: Halasi M,et al. PLoS One 2012; 7:e31761.     

Antipredator behaviour of invasive geckos in response to chemical cues from snakes

Antipredator behaviours and the ability to appropriately assess predation risk contribute to increased fitness. Predator avoidance can be costly; however, so we expect prey to most strongly avoid predators that pose the greatest risk (i.e., prey should show threat sensitivity). For invasive species, effectively assessing the relative risk posed by predators in the new environment may help them establish in new environments. We examined the antipredator behaviour of introduced Asian house geckos, Hemidactylus frenatus (Schlegel), by determining if they avoided shelters scented with the chemical cues of native predatory snakes (spotted pythons, Antaresia maculosa [Peters]; brown tree snakes, Boiga irregularis [Merrem]; common tree snakes, Dendrelaphis punctulata [Grey]; and carpet pythons, Morelia spilota [Lacépède]). We also tested if Asian house geckos collected from vegetation vs. anthropogenic substrates (buildings) responded differently to the chemical cues of predatory snakes. Asian house geckos did not show a generalised antipredator response, that is, they did not respond to the chemical cues of all snakes in the same way. Asian house geckos avoided the chemical cues of carpet pythons more strongly than those of other snake species, providing some support for the threat‐sensitivity hypothesis. There was no difference in the antipredator behaviour of Asian house geckos collected from buildings vs. natural vegetation, suggesting that individuals that have invaded natural habitats have not changed their antipredator behaviour compared to urban individuals. Overall, we found some evidence indicating Asian house geckos are threat‐sensitive to some Australian predacious snakes.     

Cryptic diversity within the Moroccan endemic day geckos Quedenfeldtia (Squamata: Gekkonidae): a multidisciplinary approach using genetic,morphological and ecological data

Quedenfeldtia (Boettger, 1883) is a genus of diurnal geckos, endemic to the Atlas Mountains in Morocco, with two species being recognized: Quedenfeldtia moerens and Quedenfeldtia trachyblepharus. Quedenfeldtia moerens is found across a wide variety of habitats, from sea level to 3000 m a.s.l., whereas Q. trachyblepharus occupies exclusively high mountain regions reaching up to 4000 m a.s.l. This differentiation, offers an interesting model for study biogeographical patterns and evolutionary scenarios in a North African endemic. Analysis of two mitochondrial (12S rRNA and ND4) and four nuclear (ACM4, MC1R, PDC, and Rag1) DNA markers revealed high genetic variation, consistent with other recent phylogeographical studies, and with the two currently described species. However, within each species, a subdivision into two groups with geographical consistence was found. Multivariate morphological analyses confirmed the existence of two main phenotypes, whereas ecological niche modelling identified various environmental variables associated with the distribution of each species, and helped to predict occurrences outside the confirmed ranges. The results obtained in the present study indicate the possible existence of additional ‘cryptic’ species within this genus, a condition found in many North African reptiles, and particularly common in geckos. In general, North African montane fauna appears to reflect the occurrence of diverse palaeoendemics, as seen in Central Africa Mountain systems, rather than the pattern of recent postglacial recolonization observed in Europe. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

A new angle on clinging in geckos: incline,not substrate,triggers the deployment of the adhesive system

Lizards commonly climb in complex three-dimensional habitats, and gekkotans are particularly adept at doing this by using an intricate adhesive system involving setae on the ventral surface of their digits. However, it is not clear whether geckos always deploy their adhesive system, given that doing so may result in decreased (i.e. reduction in speed) locomotor performance. Here, we investigate circumstances under which the adhesive apparatus of clinging geckos becomes operative, and examine the potential trade-offs between speed and clinging. We quantify locomotor kinematics of a gecko with adhesive capabilities (Tarentola mauritanica) and one without (Eublepharis macularius). Whereas, somewhat unusually, E. macularius did not suffer a decrease in locomotor performance with an increase in incline, T. mauritanica exhibited a significant decrease in speed between the level and a 10° incline. We demonstrate that this results from the combined influence of slope and the deployment of the adhesive system. All individuals kept their digits hyperextended on the level, but three of the six individuals deployed their adhesive system on the 10° incline, and they exhibited the greatest decrease in velocity. The deployment of the adhesive system was dependent on incline, not surface texture (600 grit sandpaper and Plexiglas), despite slippage occurring on the level Plexiglas substrate. Our results highlight the type of sensory feedback (gravity) necessary for deployment of the adhesive system, and the trade-offs associated with adhesion.     

Ultrahydrophobicity indicates a non-adhesive default state in gecko setae

Geckos may represent the world’s most demanding adhesives application. The adhesive setae on the toes of climbing geckos must adhere strongly yet avoid fouling or attachment at inappropriate times. We tested the hypothesis that gecko setae are non-adhesive in their unloaded default state by comparing the water droplet contact angle (θ) of isolated setal arrays to the smooth surface of eye spectacle scales of tokay geckos (Gekko gecko). At equilibrium, θ was 98.3 ± 3.4° in spectacle scales of live geckos and 93.3 ± 3.5° in isolated spectacles. Isolated setal arrays were ultrahydrophobic, with θ of 160.6 ± 1.3° (means ± SD). The difference in θ of setal arrays and smooth spectacles indicates a very low contact fraction. Using Cassie’s law of surface wettability, we infer that less than 6.6% of the surface of unloaded setae is solid and at least 93.4% is air space. We calculated that the contact fraction must increase from 6.6% in the unloaded state to 46% in the loaded state to account for previously measured values of adhesion. Thus gecko setae may be non-sticky by default because only a very small contact fraction is possible without mechanically deforming the setal array.     

The structure of anoline (Reptilia: Dactyloidae: Anolis) toe pads in relation to substratum conformity

Adhesive toe pads of geckos house modified components of vascular and/or connective tissues that promote conformity of the setal fields with the locomotor substratum. Similar modifications have been claimed for the digits of Anolis, but evidence for them is not compelling. Angiographic and histological investigations of Anolis failed to identify any evidence of either an intralamellar vascular reticular network or a central sinus. Instead, their vascularity more closely resembles that of lizards in general than that of pad‐bearing geckos. The loose connective tissue of the toe pads likely contributes to their general pliability and flexibility, promoting localized compliance with the substratum. Through the shedding cycle, the lamellae change shape as the replacing setae elongate. The outer epidermal generation lacunar cells on the inner lamellar faces simultaneously hypertrophy, providing for compatibility between overlapping lamellae, enabling reciprocity between them. This contributes to continuing compliance of the setal fields with the substratum. Overall, digital structure and attachment and release kinematics of the toe pads of Anolis are very similar to those of geckos exhibiting an incipient adhesive mechanism. Both lack major anatomical specializations for promoting conformity of the setae with the locomotor substratum beyond those of the seta‐bearing portions of the epidermis.     

Character displacement in the midst of background evolution in island populations of Anolis lizards: A spatiotemporal perspective

Negative interactions between species can generate divergent selection that causes character displacement. However, other processes cause similar divergence. We use spatial and temporal replication across island populations of Anolis lizards to assess the importance of negative interactions in driving trait shifts. Previous work showed that the establishment of Anolis sagrei on islands drove resident Anolis carolinensis to perch higher and evolve larger toepads. To further test the interaction's causality and predictability, we resurveyed a subset of islands nine years later. Anolis sagrei had established on one island between surveys. We found that A. carolinensis on this island now perch higher and have larger toepads. However, toepad morphology change on this island was not distinct from shifts on six other islands whose Anolis community composition had not changed. Thus, the presence of A. sagrei only partly explains A. carolinensis trait variation across space and time. We also found that A. carolinensis on islands with previously established A. sagrei now perch higher than a decade ago, and that current A. carolinensis perch height is correlated with A. sagrei density. Our results suggest that character displacement likely interacts with other evolutionary processes in this system, and that temporal data are key to detecting such interactions.