The terroir of the finch: How spatial and temporal variation shapes phenotypic traits in DARWIN'S finches.

The term terroir is used in viticulture to emphasize how the biotic and abiotic characteristics of a local site influence grape physiology and thus the properties of wine. In ecology and evolution, such terroir (i.e., the effect of space or "site") is expected to play an important role in shaping phenotypic traits. Just how important is the pure spatial effect of terroir (e.g., differences between sites that persist across years) in comparison to temporal variation (e.g., differences between years that persist across sites), and the interaction between space and time (e.g., differences between sites change across years)? We answer this question by analyzing beak and body traits of 4388 medium ground finches (Geospiza fortis) collected across 10 years at three locations in Galápagos. Analyses of variance indicated that phenotypic variation was mostly explained by site for beak size (η 2 = 0.42) and body size (η 2 = 0.43), with a smaller contribution for beak shape (η 2 = 0.05) and body shape (η 2 = 0.12), but still higher compared to year and site-by-year effects. As such, the effect of terroir seems to be very strong in Darwin's finches, notwithstanding the oft-emphasized interannual variation. However, these results changed dramatically when we excluded data from Daphne Major, indicating that the strong effect of terroir was mostly driven by that particular population. These phenotypic results were largely paralleled in analyses of environmental variables (rainfall and vegetation indices) expected to shape terroir in this system. These findings affirm the evolutionary importance of terroir, while also revealing its dependence on other factors, such as geographical isolation.

Do the relationships between hindlimb anatomy and sprint speed variation differ between sexes in Anolis lizards?

The ability of an animal to run fast has important consequences on its survival capacity and overall fitness. Previous studies have documented how variation in the morphology of the limbs is related to variation in locomotor performance. Although these studies have suggested direct relations between sprint speed and hindlimb morphology, few quantitative data exist. Consequently, it remains unclear whether selection acts in limb segment lengths, overall muscle mass or muscle architecture (e.g. muscle fiber length and cross-sectional area). Here, we investigate whether muscle architecture (mass, fiber length and physiological cross-sectional area), hindlimb segment dimensions, or both, explain variation in sprint speed across 14 species of Anolis lizards. Moreover, we test whether similar relationships exist between morphology and performance for both sexes, which may not be the case given the known differences in locomotor behavior and habitat use. Our results show that the main driver of sprint speed is the variation in femur length for both males and females. Our results further show sexual dimorphism in the traits studied and, moreover, show differences in the traits that predict maximal sprint speed in males and females. For example, snout vent length and overall muscle mass are also good predictors of sprint speed in males, whereas no relationships between muscle mass and sprint speed was observed in females. Only a few significant relationships were found between muscle architecture (fiber length, cross-sectional area) and sprint speed in male anoles, suggesting that overall muscles size, rather than muscle architecture, appears to be under selection.

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.

Do Adult Phenotypes Reflect Selection on Juvenile Performance? A Comparative Study on Performance and Morphology in Lizards.

When competing for food or other resources, or when confronted with predators, young animals may be at a disadvantage relative to adults because of their smaller size. Additionally, the ongoing differentiation and growth of tissues may constrain performance during early ontogenetic stages. However, juveniles must feed before they can become reproductively active adults and as such the adult phenotype may be the result of an ontogenetic filter imposing selection on juvenile phenotype and performance. Here we present ontogenetic data on head morphology and bite force for different lizard species. We test whether adults reflect selection on juveniles by comparing slopes of growth trajectories before and after sexual maturity in males and females and by examining the variance in head morphology and bite force in juveniles versus adults. Finally, we also present the first results of a selection study where animals were measured, marked and released, and recaptured the subsequent year to test whether head morphology and bite force impact survival.

Larger lacertid lizard species produce higher than expected iliotibialis muscle power output: the evolution of muscle contractile mechanics with body size.

Increases in body size can lead to alterations in morphology, physiology, locomotor performance and behaviour of animals. Most studies considering the effects of scaling on muscle performance have studied within-species effects, with few studies considering differences between species. A previous review of published data indicates that maximum muscle-shortening velocity decreases, but that maximum isometric stress does not change, with increased body mass across species of terrestrial animals. However, such previous analyses do not account for the phylogenetic relatedness of the species studied. Our aim was to use phylogenetically informed analysis to determine the effects of body size on isolated iliotibialis muscle performance across 17 species of lacertid lizards. Between one and five individuals were used to obtain mean performance values for each species. We analysed the relationship between each variable and body size, as estimated by snout-vent length (SVL), whilst taking into account the phylogenetic relationships between species. We found that isometric tetanus relaxation time, maximal tetanus stress (force per muscle cross-sectional area) and maximal work loop power output (normalised to muscle mass) all significantly increased with greater SVL. In contrast, fatigue resistance during repeated work loops significantly decreased with SVL and there was no effect of size on tetanus activation time. When we compare our findings with those that would be predicted by dynamic similarity, then as these lacertid species become bigger, there is a greater than expected increase in the normalised muscle power output, probably to counter the larger than expected increase in body mass.

Impact of temperature on performance in two species of South African dwarf chameleon, Bradypodion pumilum and B. occidentale.

Temperature is an extrinsic factor that influences reptile behavior because of its impact on reptile physiology. Understanding the impact of temperature on performance traits is important as it may affect the ecology and fitness of ectothermic animals such as reptiles. Here, we examined the temperature dependence of performance in two species of South African dwarf chameleon (Bradypodion): one adapted to a semi-arid environment and one to a mesic environment. Ecologically relevant performance traits were tested at different temperatures to evaluate their thermal dependence, and temperature-performance breadths for 80% and 90% of each performance trait were calculated. Our results show distinct differences in the thermal dependence of speed- versus force-related performance traits. Moreover, our results show that the semi-arid species is better adapted to higher temperatures and as such has a better chance of coping with the predicted increases in environmental temperature. The mesic area-adapted species seems to be more sensitive to an increase in temperature and could therefore potentially be threatened by the predicted future climate change. However, further studies investigating the potential for acclimation in chameleons are needed to better understand how animals may respond to future climate change.

The evolution of locomotor rhythmicity in tetrapods.

Differences in rhythmicity (relative variance in cycle period) among mammal, fish, and lizard feeding systems have been hypothesized to be associated with differences in their sensorimotor control systems. We tested this hypothesis by examining whether the locomotion of tachymetabolic tetrapods (birds and mammals) is more rhythmic than that of bradymetabolic tetrapods (lizards, alligators, turtles, salamanders). Species averages of intraindividual coefficients of variation in cycle period were compared while controlling for gait and substrate. Variance in locomotor cycle periods is significantly lower in tachymetabolic than in bradymetabolic animals for datasets that include treadmill locomotion, non-treadmill locomotion, or both. When phylogenetic relationships are taken into account the pooled analyses remain significant, whereas the non-treadmill and the treadmill analyses become nonsignificant. The co-occurrence of relatively high rhythmicity in both feeding and locomotor systems of tachymetabolic tetrapods suggests that the anatomical substrate of rhythmicity is in the motor control system, not in the musculoskeletal components.

Slow but tenacious: an analysis of running and gripping performance in chameleons.

Chameleons are highly specialized and mostly arboreal lizards characterized by a suite of derived characters. The grasping feet and tail are thought to be related to the arboreal lifestyle of chameleons, yet specializations for grasping are thought to exhibit a trade-off with running ability. Indeed, previous studies have demonstrated a trade-off between running and clinging performance, with faster species being poorer clingers. Here we investigate the presence of trade-offs by measuring running and grasping performance in four species of chameleon belonging to two different clades (Chamaeleo and Bradypodion). Within each clade we selected a largely terrestrial species and a more arboreal species to test whether morphology and performance are related to habitat use. Our results show that habitat drives the evolution of morphology and performance but that some of these effects are specific to each clade. Terrestrial species in both clades show poorer grasping performance than more arboreal species and have smaller hands. Moreover, hand size best predicts gripping performance, suggesting that habitat use drives the evolution of hand morphology through its effects on performance. Arboreal species also had longer tails and better tail gripping performance. No differences in sprint speed were observed between the two Chamaeleo species. Within Bradypodion, differences in sprint speed were significant after correcting for body size, yet the arboreal species were both better sprinters and had greater clinging strength. These results suggest that previously documented trade-offs may have been caused by differences between clades (i.e. a phylogenetic effect) rather than by design conflicts between running and gripping per se.

Chasing the Patagonian sun: comparative thermal biology of Liolaemus lizards.

The importance of the thermal environment for ectotherms and its relationship with thermal physiology and ecology is widely recognized. Several models have been proposed to explain the evolution of the thermal biology of ectotherms, but experimental studies have provided mixed support. Lizards from the Liolaemus goetschi group can be found along a wide latitudinal range across Argentina. The group is monophyletic and widely distributed, and therefore provides excellent opportunities to study the evolution of thermal biology. We studied thermal variables of 13 species of the L. goetschi group, in order to answer three questions. First, are aspects of the thermal biology of the L. goetschi group modelled by the environment or are they evolutionarily conservative? Second, have thermal characteristics of these animals co-evolved? And third, how do the patterns of co-evolution observed within the L. goetschi group compare to those in a taxonomically wider selection of species of Liolaemus? We collected data on 13 focal species and used species information of Liolaemus lizards available in the literature and additional data obtained by the authors. We tackled these questions using both conventional and phylogenetically based analyses. Our results show that lizards from the L. goetschi group and the genus Liolaemus in general vary in critical thermal minimum in relation to mean air temperature, and particularly the L. goetschi group shows that air temperature is associated with critical thermal range, as well as with body temperature. Although the effect of phylogeny cannot be ignored, our results indicate that these thermal biology aspects are modelled by cold environments of Patagonia, while other aspects (preferred body temperature and critical thermal maximum) are more conservative. We found evidence of co-evolutionary patterns between critical thermal minimum and preferred body temperature at both phylogenetic scales (the L. goetschi group and the extended sample of 68 Liolaemus species).

Taxonomic adjustments in the systematics of the southern African lacertid lizards (Sauria: Lacertidae).

Molecular phylogenetic analyses of southern African lacertid lizards (Eremiadini) using mitochondrial and nuclear markers revealed two examples of generic assignments incompatible with monophyletic clades. Australolacerta Arnold 1989, a genus endemic to South Africa and to which two isolated species have been referred, is paraphyletic at the generic level. In addition, the species Ichnotropis squamulosa Peters 1854 was found to be embedded within the genus Meroles. To resolve the paraphyly in Australolacerta we erect a new genus, Vhembelacerta Edwards, Branch, Herrel, Vanhooydonck, Measey, & Tolley, gen. nov., to accommodate Lacerta rupicola FitzSimons 1933. To maintain a monophyletic Ichnotropis Peters 1854, Ichnotropis squamulosa Peters 1854 is transferred to Meroles Gray 1838, now named Meroles squamulosus comb. nov. Where necessary the genera affected by these actions are re-characterized.

Convergent evolution associated with habitat decouples phenotype from phylogeny in a clade of lizards.

Convergent evolution can explain similarity in morphology between species, due to selection on a fitness-enhancing phenotype in response to local environmental conditions. As selective pressures on body morphology may be strong, these have confounded our understanding of the evolutionary relationships between species. Within the speciose African radiation of lacertid lizards (Eremiadini), some species occupy a narrow habitat range (e.g. open habitat, cluttered habitat, strictly rupicolous, or strictly psammophilic), which may exert strong selective pressures on lizard body morphology. Here we show that the overall body plan is unrelated to shared ancestry in the African radiation of Eremiadini, but is instead coupled to habitat use. Comprehensive Bayesian and likelihood phylogenies using multiple representatives from all genera (2 nuclear, 2 mitochondrial markers) show that morphologically convergent species thought to represent sister taxa within the same genus are distantly related evolutionary lineages (Ichnotropis squamulosa and Ichnotropis spp.; Australolacerta rupicola and A. australis). Hierarchical clustering and multivariate analysis of morphological characters suggest that body, and head, width and height (stockiness), all of which are ecologically relevant with respect to movement through habitat, are similar between the genetically distant species. Our data show that convergence in morphology, due to adaptation to similar environments, has confounded the assignment of species leading to misidentification of the taxonomic position of I. squamulosa and the Australolacerta species.

Female lizards ignore the sweet scent of success: Male characteristics implicated in female mate preference.

Sexual selection molds the morphology, physiology and behavior of males in many animals. At first glance, it seems reasonable to assume that females would use the same male traits and signals in mate choice as males do during male-male competition. However, intra- and intersexual competition may affect traits in the same or the opposite direction, with differing strength. We investigated which color, morphometric and performance traits are selected for through male-male competition and whether female mate preference is based on these same traits and/or dominance status in the three male color morphs of the lizard Podarcis melisellensis. Males with relatively bigger heads and relatively higher bite forces were more likely to win fights and orange males were always dominant over the other morphs. Females, however, preferred scents of bigger males that were in better body condition, and surprisingly had lower bite force capacities. They did not show a preference for scents of any particular color morph or for scents of the more dominant males. These results indicate that intra- and intersexual competition may result in selection for different secondary sexual traits in P. melisellensis.

Shake rattle and roll: the bony labyrinth and aerial descent in squamates.

Controlled aerial descent has evolved many times independently in vertebrates. Squamates (lizards and snakes) are unusual in that respect due to the large number of independent origins of the evolution of this behavior. Although some squamates such as flying geckos of the genus Ptychozoon and the flying dragons of the genus Draco show obvious adaptations including skin flaps or enlarged ribs allowing them to increase their surface area and slow down their descent, many others appear unspecialized. Yet, specializations can be expected at the level of the sensory and neural systems allowing animals to maintain stability during controlled aerial descent. The vestibular system is a likely candidate given that it is an acceleration detector and is well-suited to detect changes in pitch, roll and yaw. Here we use conventional and synchrotron µCT scans to quantify the morphology of the vestibular system in squamates able to perform controlled aerial descent compared to species characterized by a terrestrial or climbing life style. Our results show the presence of a strong phylogenetic signal in the data with the vestibular system in species from the same family being morphologically similar. However, both our shape analysis and an analysis of the dimensions of the vestibular system showed clear differences among animals with different life-styles. Species able to perform a controlled aerial descent differed in the position and shape of the inner ear, especially of the posterior ampulla. Given the limited stability of squamates against roll and the fact that the posterior ampulla is tuned to changes in roll this suggests an adaptive evolution of the vestibular system in squamates using controlled aerial descent. Future studies testing for similar differences in other groups of vertebrates known to use controlled aerial descent are needed to test the generality of this observation.

Burrowing and subsurface locomotion in anguilliform fish: behavioral specializations and mechanical constraints.

Fish swimming is probably one of the most studied and best understood locomotor behaviors in vertebrates. However, many fish also actively exploit sediments. Because of their elongate body shape, anguilliform fishes are not only efficient swimmers but also very maneuverable. Consequently, many species live in complexly structured environments near the bottom and many are known to burrow into the sediment. To better understand burrowing and subsurface locomotion in anguilliform fish we provide descriptive kinematic data on subsurface locomotion in a burrowing eel (Pisodonophis boro) using videofluoroscopy. We also measured the maximal forces that can be exerted by this species during head-first and tail-first burrowing, and explored the implications of head-first burrowing on mechanical stress distribution in the skull. Our data show that P. boro uses lateral undulation to penetrate and move in sandy sediments under water. The kinematics of subsurface locomotion are different from those observed during swimming and are characterized by a very high slip factor. These observations differ considerably from recently published data in terrestrial sand-swimming lizards, and suggest that the sediment behaves like a solid rather than a frictional fluid. Finally, our finite element models show that the cranial shape and structure in the head-first burrowing P. boro is mechanically more suited for head-first burrowing than that of an obligate tail-first burrowing species, Heteroconger hassi.

Seasonal changes in parasite load and a cellular immune response in a colour polymorphic lizard.

Permanent colour polymorphisms may be maintained by complex interactions between physiological traits (e.g. immunity) and environmental pressures. In this study we investigate morph specific variation in parasite load and cellular immune response (induced by a Phytohaemagglutinin, PHA injection) in a colour polymorphic population of the Dalmatian wall lizard (Podarcis melisellensis), where adult males have bright white, yellow or orange throats and ventral sides. Orange males have larger heads and can bite harder than the others. To examine seasonal effects, analyses were performed at an early and late stage in the reproductive season (May and September). Infection with mites and ticks did not differ among morphs, but was more severe at the end of the reproductive season. Fewer orange individuals were infected with haemogregarines at the end of the season, but white males were always more infected (higher number of haemogregarines in their blood) than other morphs. White and yellow males showed an increased PHA response towards the end of the season, but PHA response decreased in the orange morph. Finally, across all morphs, a relationship was found between ectoparasite load and PHA response. Our study provides indications of alternative life-history strategies among colour morphs and evidence for an up-regulation of the immune function at the end of the reproductive season.

Effects of testosterone on morphology, performance and muscle mass in a lizard.

Because sexual selection pressures are high in sexually dimorphic organisms, morphological, physiological and performance traits are often studied in a sexual selection context. The proximate mechanisms underlying evolutionary change in these traits, however, remain largely unstudied. Here, we examined the role of steroids in shaping morphology and physiological performance in males of a sexually dimorphic lizard (Gallotia galloti). We compared morphology and physiological performance of males with experimentally elevated testosterone levels to sham-operated males. Before surgery, inter-individual variation in plasma testosterone levels correlated positively with bite force capacity. Administration of exogenous testosterone resulted in an increase of the mass of both jaw closing and locomotory muscles compared with sham-operated individuals, but the responsiveness varied considerably among muscle groups. In contrast to our expectations, the dramatic testosterone-induced changes in muscle masses did not result in concordant changes in bite force performance or sprint speed.

Ecomorphological analysis of aerial performance in a non-specialized lacertid lizard, Holaspis guentheri.

Controlled aerial descent has evolved at least 30 times independently in different vertebrate and invertebrate lineages. A whole suite of morphological modifications, such as patagia, lateral skin folds and webbed feet, have been suggested to enhance descending ability. In this study, we compare aerial performance (i.e. vertical and horizontal velocity, horizontal distance covered, duration of descent) and morphology (body mass, body width, inter limb distance, surface area and wing loading) among three species of lizards, representing a range of aerial descenders present within the clade. Our performance measurements show that the lacertid Holaspis guentheri performs intermediately to the specialized gekkonid Ptychozoon kuhli and the rock-dwelling lizard Podarcis muralis. The small relative body mass of H. guentheri results in a low wing loading similar to that of P. kuhli thus enhancing its aerial performance. Whereas the latter generates great lift forces and is able to cover great horizontal distances, H. guentheri's low wing loading seems to be responsible for a slow descent and low impact forces upon landing. Our results show that very small morphological changes may result in noticeable and ecologically relevant changes in performance.

Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource.

Although rapid adaptive changes in morphology on ecological time scales are now well documented in natural populations, the effects of such changes on whole-organism performance capacity and the consequences on ecological dynamics at the population level are often unclear. Here we show how lizards have rapidly evolved differences in head morphology, bite strength, and digestive tract structure after experimental introduction into a novel environment. Despite the short time scale ( approximately 36 years) since this introduction, these changes in morphology and performance parallel those typically documented among species and even families of lizards in both the type and extent of their specialization. Moreover, these changes have occurred side-by-side with dramatic changes in population density and social structure, providing a compelling example of how the invasion of a novel habitat can evolutionarily drive multiple aspects of the phenotype.

Microhabitat use, diet, and performance data on the Hispaniolan twig anole, Anolis sheplani: pushing the boundaries of morphospace.

Caribbean Anolis lizards are often cited as a textbook example of adaptive radiation. Similar morphologies (ecomorphs) have originated in similar ecological settings on different large islands in the West Indies. However, relatively little is known about one of the morphologically most specialized and divergent ecomorphs: the twig anoles. Here, we investigate aspects of morphology, dewlap size, locomotor and bite performance, structural habitat and diet of the poorly known twig anole, Anolis sheplani from Hispaniola. Few observations have previously been made of this species in its natural habitat, and few quantitative data on its natural history are available. A. sheplani is an extreme twig anole with respect to its morphology, performance capacities, and ecological niche. Males and females of this species do not differ from each other in body dimensions, performance or habitat use, but males do have a bigger dewlap than females. We present data for 25 individuals and compare them with data for other Greater Antillean anoles. It becomes apparent that twig anoles constitute a large component of the morphological, functional, and ecological diversity of Anolis lizards. Small twig anoles such as A. sheplani appear to be pushing the boundaries of morphospace and are thus crucial in our understanding of the evolution of phenotypic diversity.

Determinants of sexual differences in escape behavior in lizards of the genus Anolis: a comparative approach.

Males and females are known to differ in a whole suite of characteristics, such as morphology, physiology, ecology, and behavior. Intersexual differences are generally believed to arise because of differences in selective pressures on either sex. In this study, we investigated whether intersexual differences in escape behavior exist in lizards of the genus Anolis, and whether these could be explained by intersexual differences in body size and/or microhabitat use. To do so, we compared the behavioral response to an approaching human predator in the field in males and females of 12 Anolis species. We found that ecomorphs and sexes differ greatly with respect to escape behavior. Twig anoles have the shortest approach distance (i.e., distance between the observer and the lizard when it starts fleeing) and final distance (i.e., distance between the observer and the lizard when it stops moving), compared with the other ecomorphs. The distance fled, on the contrary, is greatest in twig anoles. Also, females flee less soon and run over shorter distances than do males. Since twig anoles are considered the most cryptic anoles, and females may be less conspicuous than males, these results corroborate the idea that well camouflaged animals allow predators to come closer. The interspecific variation in sexual dimorphism in escape behavior, however, cannot be explained by the interspecific variation in sexual size dimorphism or sexual dimorphism in microhabitat use. Thus, escape behavior appears determined by different factors in males and females.