Sexual dimorphism and interpopulation differences in lizard hind limb length: locomotor performance or chemical signalling?

Intraspecific variation in morphology has often been related to fitness differences through its effects on performance. In lizards, variation in hind limb length can be shaped by natural selection for increased locomotor performance, sexual selection on the number or size of femoral pores involved in chemical signalling, or both. Here, we analyse the selective forces involved in sexual dimorphism and differences in hind limb length between two populations of Psammodromus algirus living at different elevation. Males were more robust and had longer hind limbs and limb segments than females, and low‐elevation lizards had longer limbs than high‐elevation lizards. However, differences in locomotor performance were small and non‐significant, making natural selection for faster runs an unlikely explanation for the observed pattern. On the other hand, males had more femoral pores than females, and lizards had more pores at lower elevation, although the difference was significant only for males (which invest more in chemical signalling). In males, the number of pores, which remains constant along a lizard's life, was not correlated with hind limb length. However, femur length was positively correlated with mean pore size, allowing low‐elevation males to have larger than expected pores, which could increase the effectiveness with which they spread their signals in a dry and warm habitat where chemicals become volatile rapidly. Also, saturation of the sexual coloration of the head was higher for low‐elevation males, suggesting that sexual selection pressures may be more intense. Overall, our results indicate that sexual selection plays a significant role in shaping intraspecific variation in hind limb length. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 318–329.     

Limb and tail lengths in relation to substrate usage in Tropidurus lizards

A close relationship between morphology and habitat is well documented for anoline lizards. To test the generality of this relationship in lizards, snout-vent, tail, and limb lengths of 18 species of Tropidurus (Tropiduridae) were measured and comparisons made between body proportions and substrate usage. Phylogenetic analysis of covariance by computer simulation suggests that the three species inhabiting sandy soils have relatively longer feet than do other species. Phylogenetic ANCOVA also demonstrates that the three species inhabiting tree canopies and locomoting on small branches have short tails and hind limbs. These three species constitute a single subclade within the overall Tropidurus phylogeny and analyses with independent contrasts indicate that divergence in relative tail and hind limb length has been rapid since they split from their sister clade. Being restricted to a single subclade, the difference in body proportions could logically be interpreted as either an adaptation to the clade's lifestyle or simply a nonadaptive synapomorphy for this lineage. Nevertheless, previous comparative studies of another clade of lizards (Anolis) as well as experimental studies of Sceloporus lizards sprinting on rods of different diameters support the adaptive interpretation.     

Relations between microhabitat use and limb shape in phrynosomatid lizards

With the exception of the well-documented case for anoline lizards, recent studies have found few evolutionary relationships between morphology and habitat use in lizards despite clear-cut biomechanical predictions. One of the factors typically hampering these analyses is the clustering of habitat use within evolutionary lineages. In the present study, body shape was quantified for male and female lizards of 30 species of phrynosomatid lizards. This group was selected as little clustering of ecological variables seemed to be present. The results of traditional analyses indicate that evolutionary correlates of habitat use were prominent in the hindlimbs of both sexes. Species living in open habitats are characterized by longer femurs, and longer hindlimbs relative to the forelimb. Moreover, males from ground-dwelling species utilizing open habitats have longer toes on the hind foot than males from climbing species. Phylogenetic analyses indicated strong evolutionary associations between habitat use and the relative length of front and hindlimbs, with species from open terrestrial habitats having significantly shorter frontlimbs relative to their hindlimb than rock or tree climbing species. Evolutionary associations between morphology and habitat use were generally stronger for male lizards, indicating a potentially important contribution of sexual selection to the evolution of differences in limb proportions.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 149–163.     

Correlations between habitat use and body shape in a phrynosomatid lizard (Urosaurus ornatus): a population-level analysis

Recent ecomorphological studies have shown that the predicted correlations between morphology and ecology on broad taxonomic levels are often obscured when comparing more closely related groups. Among species, comparisons of lizards often indicate very little support for adaptive radiations into novel habitats. As few population level studies have been performed, we compared body, head and limb shape between four populations of Urosaurus ornatus living in structurally distinct habitats (cliffs, rocks, trees and boulders). Surprisingly, clear correlations between habitat use and body shape among populations were found, most of which were in good accordance with a priori biomechanical predictions (e.g. flat body and head for extreme climbers; long distal hindlimb segments for jumpers and runners; narrow body and long tail for tree dwelling lizards). This indicates that populations of Urosaurus ornatus are seemingly 'adapted' to the habitat they live in. However, quantification of performance and behaviour are needed to determine the adaptive nature of these observations.     

The quick and the dead: correlational selection on morphology, performance, and habitat use in island lizards

Natural selection is an important driver of microevolution. Yet, despite significant theoretical debate, we still have a poor understanding of how selection operates on interacting traits (i.e., morphology, performance, habitat use). Locomotor performance is often assumed to impact survival because of its key role in foraging, predator escape, and social interactions, and shows strong links with morphology and habitat use within and among species. In particular, decades of study suggest, but have not yet demonstrated, that natural selection on locomotor performance has shaped the diversification of Anolis lizards in the Greater Antilles. Here, we estimate natural selection on sprinting speed and endurance in small replicate island populations of Anolis sagrei. Consistent with past correlational studies, long-limbed lizards ran faster on broad surfaces but also had increased sprint sensitivity on narrow surfaces. Moreover, performance differences were adaptive in the wild. Selection favored long-limbed lizards that were fast on broad surfaces, and preferred broad substrates in nature, and also short-limbed lizards that were less sprint sensitive on narrow surfaces, and preferred narrow perches in nature. This finding is unique in showing that selection does not act on performance alone, but rather on unique combinations of performance, morphology, and habitat use. Our results support the long-standing hypothesis that correlated selection on locomotor performance, morphology, and habitat use drives the evolution of ecomorphological correlations within Caribbean Anolis lizards, potentially providing a microevolutionary mechanism for their remarkable adaptive radiation.     

Intraspecific ecomorphological variation: linear and geometric morphometrics reveal habitat‐related patterns within Podarcis bocagei wall lizards

Morphological variation in relation to habitat is known to occur in several lizard groups. Comparative studies have linked morphology and habitat use, showing that locomotion is the principal mediator of this evolutionary relationship. Here, we investigate intraspecific ecomorphological variation in Podarcis bocagei by examining three habitat types, representing a variety between saxicolous and ground‐dwelling habits. Our results indicate variation in absolute and relative limb length, but patterns are only partially concordant to biomechanical predictions. Whereas the femur and hind foot are longer in ground‐dwelling lizards, confirming previous observations, the tibia and hind limb are relatively shorter, contradicting expectations. Additionally, head shape varies substantially between habitats, in line with a hypothesis of mechanical restrictions related to microhabitat and refuge use. Finally, we detect male‐specific variation between habitats in total body size and head size, providing evidence for interactions between natural and sexual selection. Although performance and behaviour studies are necessary to definitely confirm the functional and evolutionary significance of the observed patterns, our study indicates that ecomorphological adaptations can arise in a very short evolutionary time in this group of lizards.     

Limb segment contributions to the evolution of hind limb length in phrynosomatid lizards

Longer hind limbs are often associated with faster maximum sprint speeds measured in the laboratory and sometimes with increased Darwinian fitness in studies of individual variation in natural populations. Limb length may be altered by changing the length of one or all segments, with different functional consequences. Segment length evolution can be influenced by both natural and sexual selection, and lineage‐specific effects (multiple solutions) may also occur. We examined the evolution of total hind limb length, as well as thigh, crus, pes, and toe length, among 46 species of phrynosomatids and also investigated the role of habitat use and shared evolutionary history in shaping limb morphology. Because sexes are usually behaviourally and morphologically dimorphic, we examined them separately. In females, habitat was only an important predictor of crus (lower leg) length. In males, habitat was not an important predictor of any variable. Overall, clade‐level differences were more important than habitat as predictors of segment or total hind limb length. Not all limb segments scaled isometrically with the combined length of other segments, and both sex and clade affected the scaling of some segments. These results suggest that clade‐level differences are more important than habitat use for explaining differences in limb length and proportions, and sexual dimorphism may be an important consideration in morphology–performance–behaviour–fitness relationships.     

Functional consequences of morphological differentiation between populations of the Cape Dwarf Chameleon (Bradypodion pumilum)

Variation in phenotype between species or populations of the same species living in different habitats is often explained in an adaptive context with local habitat differences driving selection on morphological traits relevant in a given ecological context. Previous studies have demonstrated significant differences in limb and tail morphology between populations of the Cape Dwarf Chameleon (Bradypodion pumilum) living in closed vs. open habitats. However, the adaptive nature of the observed differences remains unclear. Here, we quantify the structural habitat use in two different populations, test whether the random habitat differs between the two sites and whether or not chameleons select perches randomly. Next, we test whether morphology is correlated with structural habitat use and test for differences in performance between populations. Our results demonstrate that habitats are structurally different, that chameleons in the two populations use perches of different diameters and that, in one of the populations, chameleons select relatively wider perches than available at random. Performance traits (hand and tail grip performance and sprint speed) are correlated with morphology (hand size, tail length and tibia length) and differ between sexes and populations. Moreover, performance is dependent on dowel size. These results suggest that differences in performance between populations are indeed adaptive and indicate the existence of true ecomorphs in chameleons of the genus Bradypodion. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 692–700.     

Nowhere to run: the role of habitat openness and refuge use in defining patterns of morphological and performance evolution in tropical lizards

For species from open habitats with little cover and few refugia, selection should favour morphologies that enhance performance at tasks that enable rapid movement across open areas. Similarly, selection should also favour traits that enable rapid access and movement within suitable refugia. This study examined the relationship between habitat openness, refuge use, morphology and performance of 19 species representing 23 populations of tropical Lygosomine skink. Species from this group occupy a wide array of habitats from open forest and open rocky intertidal zones to high‐altitude heaths and dense, closed forests. Species that occupied open habitats were faster at sprinting, climbing and had better cling ability than species from more cluttered, closed habitats. In addition, species from habitats that used rock crevices as refuges had enhanced sprinting ability. This study shows the importance of both habitat openness and refuge type in the evolution of both the morphology and performance in lizards.     

Landscape configuration determines gene flow and phenotype in a flightless forest-edge ground-dwelling bush-cricket, Pholidoptera griseoaptera

Spatial configuration of habitats influences genetic structure and population fitness whereas it affects mainly species with limited dispersal ability. To reveal how habitat fragmentation determines dispersal and dispersal-related morphology in a ground-dispersing insect species we used a bush-cricket (Pholidoptera griseoaptera) which is associated with forest-edge habitat. We analysed spatial genetic patterns together with variability of the phenotype in two forested landscapes with different levels of fragmentation. While spatial configuration of forest habitats did not negatively affect genetic characteristics related to the fitness of sampled populations, genetic differentiation was found higher among populations from an extensive forest. Compared to an agricultural matrix between forest patches, the matrix of extensive forest had lower permeability and posed barriers for the dispersal of this species. Landscape configuration significantly affected also morphological traits that are supposed to account for species dispersal potential; individuals from fragmented forest patches had longer hind femurs and a higher femur to pronotum ratio. This result suggests that selection pressure act differently on populations from both landscape types since dispersal-related morphology was related to the level of habitat fragmentation. Thus observed patterns may be explained as plastic according to the level of landscape configuration; while anthropogenic fragmentation of habitats for this species can lead to homogenization of spatial genetic structure.     

An analysis of continent-wide patterns of sexual selection in a passerine bird

Patterns of selection are widely believed to differ geographically, causing adaptation to local environmental conditions. However, few studies have investigated patterns of phenotypic selection across large spatial scales. We quantified the intensity of selection on morphology in a monogamous passerine bird, the barn swallow Hirundo rustica, using 6495 adults from 22 populations distributed across Europe and North Africa. According to the classical Darwin-Fisher mechanism of sexual selection in monogamous species, two important components of fitness due to sexual selection are the advantages that the most attractive males acquire by starting to breed early and their high annual fecundity. We estimated directional selection differentials on tail length (a secondary sexual character) and directional selection gradients after controlling for correlated selection on wing length and tarsus length with respect to these two fitness components. Phenotype and fitness components differed significantly among populations for which estimates were available for more than a single year. Likewise, selection differentials and selection gradients differed significantly among populations for tail length, but not for the other two characters. Sexual selection differentials differed significantly from zero across populations for tail length, particularly in males. Controlling statistically for the effects of age reduced the intensity of selection by 60 to 81%, although corrected and uncorrected estimates were strongly positively correlated. Selection differentials and gradients for tail length were positively correlated between the sexes among populations for selection acting on breeding date, but not for fecundity selection. The intensity of selection with respect to breeding date and fecundity were significantly correlated for tail length across populations. Sexual size dimorphism in tail length was significantly correlated with selection differentials with respect to breeding date for tail length in male barn swallows across populations. These findings suggest that patterns of sexual selection are consistent across large geographical scales, but also that they vary among populations. In addition, geographical patterns of phenotypic selection predict current patterns of phenotypic variation among populations, suggesting that consistent patterns of selection have been present for considerable amounts of time.     

Sex differences in survival selection in the serin,Serinus serinus

Natural selection is demonstrated in most natural populations which suggests that populations are dispatched from their adaptive peaks as a result of selection on correlated characters, or conflicting selection between the sexes. We analysed patterns of survival selection in a population of serins (Serinus serinus) outside Barcelona over a period of 13 years. There was directional selection for increased wing length in males and females accompanied by strong disruptive selection on both tail and wing length in males and a selection against a positive correlation between the two characters in males. In females there was directional selection for increased bill width but decreased bill depth, which should be contrasted to the stabilizing selection acting on bill depth in males. There were conflicting selection on the characters within a sex and conflicting selection of the same characters between sexes, which constrain the rate of access to the nearest adaptive peak.     

Searching for the fundamental niche using individual‐based habitat selection modelling across populations

Strictly speaking, fundamental niches are inestimable. Nevertheless, ecologists attempt approximating them to understand species’ distribution and plasticity to environmental changes, with invaluable repercussions on both theoretical and applied ecology. So far, individual‐based habitat selection models only characterized realized niches of populations delimited by physical (e.g. fences), historical (colonization) and biotic (competition) barriers constraining access to a subset of resources available to the species. As populations with different realized niches share the same fundamental niche, we developed a novel framework to scale‐up response curves from population‐scale habitat selection models to approximate the species’ optimal habitat choices, unbiased by barriers constraining accessibility. We used GPS‐locations from 147 wild mountain reindeer Rangifer t. tarandus, belonging to 7 of the remaining populations scattered throughout the subspecies’ range. We linked individual choices to accessible habitat features using conditional‐logistic regression with log‐link function in a use‐available design. Focal variables were modeled using 2nd degree polynomials on log‐scale, which correspond to a Gaussian curve used to approximate the fundamental niche optimum (curve mean) and breadth (variance). Using both real and simulated data we demonstrate that robust approximations of a fundamental niche optimum and breadth can be estimated using a relatively small number of representative populations with relatively few individuals. While each classical realized niche model had strong predictive power for the focal population but poorly predicted across populations, the approximation of the fundamental niche allowed for robust inter‐population comparisons in habitat quality. The proposed approach brings individual‐based habitat selection models forward along the continuum from investigating the realized niche of a population towards investigating a species’ fundamental niche, and allows us to quantify empirically the relationship between realized and fundamental niches. This allows improving the understanding of differences in fitness among populations, the prediction of species’ distributions and plasticity to environmental changes, and suggestions for mitigation priorities.     

Differences in morphology, performance and behaviour between recently diverged populations of Podarcis sicula mirror differences in predation pressure

We investigated the possible role of variation in predation pressure in the phenotypic divergence of two island populations of the Italian wall lizard, Podarcis sicula . In 1971, ten adult specimens from the island of Pod Kopište (Adriatic Sea, Croatia) were transported to the island of Pod Mrčaru, 3.5 km east, where they founded a new population. Although the two islands resemble each other in general physiognomy (size, elevation, microclimate) and in the absence of terrestrial predators, lizards from the newly established population are now on average larger and have shorter hind limbs. They also exhibit lower maximal sprint speed as measured on a racetrack, and fatigue faster when chased in a torus track. In the field, lizards from the original population of Pod Kopište respond to a simulated predatory attack by fleeing at larger approach distances and by running further from the predator than lizards from Pod Mrčaru. These changes in morphology, behaviour and performance may result from the relaxed predation intensity on the latter island. Our analysis of the structural features of the microhabitats suggests that the vegetation on Pod Mrčaru offers more protection to lizards. Also, plasticine models of lizards, laid out on the islands, less often exhibited signs of being attacked by birds on Pod Mrčaru than on Pod Kopište. Our findings provide an example of how changes in (possibly a single) environmental factor may simultaneously produce responses in behaviour, morphology and whole-animal physiology, and this on a surprisingly small spatial and temporal scale.     

Is phylogeny driving tendon length in lizards?

Tulli, M.J., Herrel, A., Vanhooydonck, B. and Abdala, V. 2012. Is phylogeny driving tendon length in lizards?—Acta Zoologica (Stockholm) 93 : 319–329. Tendons transmit tensile forces generated by muscles and are a crucial part of the musculoskeletal system in vertebrates. Because tendons and tendon cells respond to altered mechanical load by increasing collagen synthesis, we hypothesized that a correlation between tendon morphology and the loading regime imposed by locomotor style or habitat use exists. This makes tendons an interesting model for studying the relationship between morphology and environment. In this study, we compare the general morphology of the palmar flexor plate, the length of the digital tendons, and the length of the flexor carpi ulnaris tendon in species of lizards that exploit a variety of structural habitats. The results from statistical analyses show that phylogenetic relatedness has a major impact on our ability to detect differences between habitat groups, and no differences in tendon length could be detected between iguanian species occupying different habitats when taking into account the relatedness between species. Our data for lizards diverge from the general mammalian paradigm where variation in tendon is often associated with habitat use or locomotor style.     

Lifetime reproductive success,selection on lifespan,and multiple sexual ornaments in male European barn swallows

Natural and sexual selection arise when individual fitness varies according to focal traits. Extra‐pair paternities (EPPs) can affect the intensity of selection by influencing variance in fitness among individuals. Studies of selection require that individual fitness is estimated using proxies of lifetime reproductive success (LRS). However, estimating LRS is difficult in large, open populations where EPPs cause reallocation of biological paternity. Here, we used extensive field sampling to estimate LRS in a population of barn swallows (Hirundo rustica) to estimate selection on lifespan and ornamental traits of males. We found selection on lifespan mediated both by within‐ and extra‐pair fertilization success and selection on tail length mediated by within‐ but not extra‐pair fertilization success. In addition, we found selection on tail white spots via extra‐pair fertilization success after controlling for selection on other traits. These results were not confounded by factors that hamper studies of LRS, including nonexhaustive sampling of offspring and biased sampling of males. Hence, natural and sexual selection mediated by LRS operates on lifespan, tail length, and size of the tail white spots in barn swallows.     

Aegean wall lizards switch foraging modes,diet, and morphology in a human‐built environment

Foraging mode is a functional trait with cascading impacts on ecological communities. The foraging syndrome hypothesis posits a suite of concurrent traits that vary with foraging mode; however, comparative studies testing this hypothesis are typically interspecific. While foraging modes are often considered typological for a species when predicting foraging‐related traits or mode‐specific cascading impacts, intraspecific mode switching has been documented in some lizards. Mode‐switching lizards provide an opportunity to test foraging syndromes and explore how intraspecific variability in foraging mode might affect local ecological communities.Because lizard natural history is intimately tied to habitat use and structure, I tested for mode switching between populations of the Aegean wall lizard, Podarcis erhardii, inhabiting undisturbed habitat and human‐built rock walls on the Greek island of Naxos. I observed foraging behavior among 10 populations and tested lizard morphological and performance predictions at each site. Furthermore, I investigated the diet of lizards at each site relative to the available invertebrate community.I found that lizards living on rock walls were significantly more sedentary—sit and wait—than lizards at nonwall sites. I also found that head width increased in females and the ratio of hindlimbs to forelimbs in both sexes increased as predicted. Diet also changed, with nonwall lizards consuming a higher proportion of sedentary prey. Lizard bite force also varied significantly between sites; however, the pattern observed was opposite to that predicted, suggesting that bite force in these lizards may more closely relate to intraspecific competition than to diet.This study demonstrates microgeographic variability in lizard foraging mode as a result of human land use. In addition, these results demonstrate that foraging mode syndromes can shift intraspecifically with potential cascading effects on local ecological communities.     

Testing for microevolution in body size in three blue tit populations

Quantifying the genetic variation and selection acting on phenotypes is a prerequisite for understanding microevolutionary processes. Surprisingly, long-term comparisons across conspecific populations exposed to different environments are still lacking, hampering evolutionary studies of population differentiation in natural conditions. Here, we present analyses of additive genetic variation and selection using two body-size traits in three blue tit (Parus caeruleus) populations from distinct habitats. Chick tarsus length and body mass at fledging showed substantial levels of genetic variation in the three populations. Estimated heritabilities of body mass increased with habitat quality. The poorer habitats showed weak positive selection on tarsus length, and strong positive selection on body mass, but there was no significant selection on either trait in the good habitat. However, there was no evidence of any microevolutionary response to selection in any population during the study periods. Potential explanations for this absence of a response to selection are discussed, including the effects of spatial heterogeneity associated with gene flow between habitats.     

ADAPTATION AND CONSTRAINT IN THE EVOLUTION OF SPECIALIZATION OF BAHAMIAN ANOLIS LIZARDS

Interspecific interactions affect habitat use and subsequent morphological adaptation in Anolis lizards. We examined populations of two species of Anolis lizards that evolved in the species-rich communities of Cuba and are now widespread in the Bahamas. Because the species occupy islands in the Bahamas that vary in the number of lizard species present and other characteristics, we predicted that directional selection should have led to morphological differentiation. In particular, we expected that populations on one-species islands should have evolved toward a generalist morphology because of the lack of competitors. Divergence in both species has been adaptive; populations that use wider perches have longer legs. Nonetheless, these differences are relatively minor, and none of the populations appears to have differentiated from its ancestral “ecomorph” type toward a more generalized morphology. This stasis mirrors a trend observed in the radiation of Caribbean anoles, which exhibits repeated instances of evolutionary specialization, but few or no cases of reversion to a more generalized condition. The explanation for this directionality of evolution is not obvious but probably involves the tendency of specialized species to continue using and further adapting the niches for which they are specialized even as conditions change.     

Sexual differences in caudal morphology and its relation to tail autotomy in lacertid lizards

We hypothesized that the presence of the forked hemipenes, and associated musculature, at the base of the tail in male lizards should constrain the capacity to autotomize the tail. Thus, this hypothesis predicts that the non-autotomous base of the tail should be longer in male than in female lizards. We tested this hypothesis in four species oflacertid lizards. Males have on average one to two non-autotomous vertebrae more than females, and the sexual difference in length of the non-autotomous tail base remains constant over the entire body size range. In addition, the first functional autotomy plane in males is usually located on, or is distal to, the vertebrae from which two hemipenial muscles take origin. These observations support the view that functional demands of the male intromittent organs impose constraints on the abilities of tail autotomy. In a natural population of Lacerta vivipara , the proportion of tail breaks that occurred at very short distances from the base was highest in females, indicating that the small sexual difference in length of the non-autotomous tail part is of functional significance. Total length of the tail was largest in males. This can be interpreted as a compensation for the decline in autotomy capacities at the tail base, such that the length of the autotomous part remains similar in both sexes.