Macroevolution of arboreality in salamanders

Evolutionary theory predicts that selection in distinct microhabitats generates correlations between morphological and ecological traits, and may increase both phenotypic and taxonomic diversity. However, some microhabitats exert unique selective pressures that act as a restraining force on macroevolutionary patterns of diversification. In this study, we use phylogenetic comparative methods to investigate the evolutionary outcomes of inhabiting the arboreal microhabitat in salamanders. We find that arboreality has independently evolved at least five times in Caudata and has arisen primarily from terrestrial ancestors. However, the rate of transition from arboreality back to terrestriality is 24 times higher than the converse. This suggests that macroevolutionary trends in microhabitat use tend toward terrestriality over arboreality, which influences the extent to which use of the arboreal microhabitat proliferates. Morphologically, we find no evidence for an arboreal phenotype in overall body proportions or in foot shape, as variation in both traits overlaps broadly with species that utilize different microhabitats. However, both body shape and foot shape display reduced rates of phenotypic evolution in arboreal taxa, and evidence of morphological convergence among arboreal lineages is observed. Taken together, these patterns suggest that arboreality has played a unique role in the evolution of this family, providing neither an evolutionary opportunity, nor an evolutionary dead end.     

Evolution of morphology and locomotor performance in anurans: relationships with microhabitat diversification

The relationships between morphology, performance, behavior and ecology provide evidence for multiple and complex phenotypic adaptations. The anuran body plan, for example, is evolutionarily conserved and shows clear specializations to jumping performance back at least to the early Jurassic. However, there are instances of more recent adaptation to habit diversity in the post‐cranial skeleton, including relative limb length. The present study tested adaptive models of morphological evolution in anurans associated with the diversity of microhabitat use (semi‐aquatic arboreal, fossorial, torrent, and terrestrial) in species of anuran amphibians from Brazil and Australia. We use phylogenetic comparative methods to determine which evolutionary models, including Brownian motion (BM) and Ornstein‐Uhlenbeck (OU) are consistent with morphological variation observed across anuran species. Furthermore, this study investigated the relationship of maximum distance jumped as a function of components of morphological variables and microhabitat use. We found there are multiple optima of limb lengths associated to different microhabitats with a trend of increasing hindlimbs in torrent, arboreal, semi‐aquatic whereas fossorial and terrestrial species evolve toward optima with shorter hindlimbs. Moreover, arboreal, semi‐aquatic and torrent anurans have higher jumping performance and longer hindlimbs, when compared to terrestrial and fossorial species. We corroborate the hypothesis that evolutionary modifications of overall limb morphology have been important in the diversification of locomotor performance along the anuran phylogeny. Such evolutionary changes converged in different phylogenetic groups adapted to similar microhabitat use in two different zoogeographical regions.     

Ecological radiation with limited morphological diversification in salamanders

A major goal of evolutionary biology is to explain morphological diversity among species. Many studies suggest that much morphological variation is explained by adaptation to different microhabitats. Here, we test whether morphology and microhabitat use are related in plethodontid salamanders, which contain the majority of salamander species, and have radiated into a striking diversity of microhabitats. We obtained microhabitat data for 189 species that also had both morphometric and phylogenetic data. We then tested for associations between morphology and microhabitat categories using phylogenetic comparative methods. Associations between morphology and ecology in plethodontids are largely confined to a single clade within one subfamily (Bolitoglossinae), whereas variation in morphology across other plethodontids is unrelated to microhabitat categories. These results demonstrate that ecological radiation and morphological evolution can be largely decoupled in a major clade. The results also offer a striking contrast to lizards, which typically show close relationships between morphology and microhabitat.     

Functional and ecological relevance of intraspecific variation in body size and shape in the lizard Podarcis melisellensis (Lacertidae)

Within populations, individual animals may vary considerably in morphology and ecology. The degree to which variation in morphology is related to ecological variation within a population remains largely unexplored. We investigated whether variation in body size and shape among sexes and age classes of the lizard Podarcis melisellensis translates in differential whole-animal performance (sprint speed, bite force), escape and prey attack behaviour in the field, microhabitat use and diet. Male and female adult lizards differed significantly in body size and head and limb proportions. These morphological differences were reflected in differences in bite strength, but not in sprint speed. Accordingly, field measurements of escape behaviour and prey attack speed did not differ between the sexes, but males ate larger, harder and faster prey than females. In addition to differences in body size, juveniles diverged from adults in relative limb and head dimensions. These shape differences may explain the relatively high sprint and bite capacities of juvenile lizards. Ontogenetic variation in morphology and performance is strongly reflected in the behaviour and ecology in the field, with juveniles differing from adults in aspects of their microhabitat use, escape behaviour and diet.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 251–264.     

The ecomorphology of Bornean tree frogs (family Rhacophoridae)

Ecomorphological studies generally assume a causal relationship between morphology and ecology mediated by performance. That assumption was tested in a community of Bornean tree frogs of the family Rhacophoridae. Biomechanical models allow a priori predictions about expected intra- and interspecific correlations among toepad area, hind-limb length, body mass, sticking ability, jumping distance, microhabitat, vertical height and substrate. Both intra- and interspecifically, size and shape variables showed patterns of association with ecology predicted on the basis of maintaining relative as well as absolute levels of performance. Unexpectedly, the form-function relationship between toepad area and sticking ability differed intra- and interspecifically. These findings indicate the need for more empirical work examining morphology-performance relationships and their use in ecology.     

Evolutionary aspects of primate locomotion

Both neontological and phylogenetic studies are necessary to interpret primate locomotion. Reference to palaeoprimatology and palaeocology, for instance, will lead to a fuller understanding of the roots of such gaits as the vertical clinging and leaping of Tarsius, Indri and Propithecus. Evolutionary trends in posture and locomotion are discussed. The postural trend has been towards maintenance of trunk verticality and the locomotor trend towards an increasing dependence on the forelimbs among arboreal primates. Three stages are recognized in the phylogenetic course of arboreal locomotor adaptation: Stage A. Vertical clinging and leaping; Stage B. Quadrupedalism; Stage C. Brachiation. The role of prehensility of the hand in the evolution of locomotor types is discussed in relation to forest morphology and, in particular, to stratification. Finally a scheme of evolution, set in the framework of ecology, for Old World Monkey groups is presented.     

Relationships between head morphology, bite performance and ecology in two species of Podarcis wall lizards

Understanding the relationship between form and function is central to our comprehension of how phenotypic diversity evolves. Traits involved in multiple activities, such as social interactions and ecological resource use, are under the influence of different evolutionary forces potentially acting in opposite directions. Such systems provide the opportunity of understanding how potential constraints on morphological variation may influence whole-organism performance. In this study we examined morphology and bite performance in two closely related species of Podarcis wall lizards with divergent microhabitat preferences, to investigate how natural and sexual selection interact to shape the evolution of head traits. Our results show that although head morphology is markedly different between species and sexes, only sexes differ in bite force, indicating that the ecological differentiation between species is reflected in their morphology but does not constrain performance. Rather, the modification of the relative size of head components between species and a shift in the form-function relationship provide a potential explanation of how equal performance is attained by different morphological configurations. Geometric morphometrics provide a clear, biomechanically meaningful image of how this is achieved and show a bisexual pattern of head shape-bite force association in both species. This, together with a strong allometry of head size on body size and head shape on head size, provides indirect morphological evidence for the importance of sexual selection in shaping morphological and functional patterns. Finally, our findings suggest that the differences observed between species and sexes in head traits and bite performance are not reflected in their dietary ecology, implying that if trophic niche segregation between groups occurs, the reasons behind it are not primarily related to head morphology and functional variation.     

The comparative evolution of lizard claw and toe morphology and clinging performance

In this study, I utilize the expected functional relationships between claw and toe morphology and clinging performance as a basis for examining evolutionary trends across 85 lizard taxa from 13 families. After controlling for body size and phylogeny, multivariate comparisons indicate that several aspects of claw and toe morphology are correlated with clinging performance. Specifically, evolutionary increases in claw curvature, toe width and adhesive lamella number are correlated with increases in clinging performance on smooth substrates. Furthermore, evolutionary increases in claw height and decreases in toe length are correlated with increases in clinging performance on rough substrates. Sensitivity analyses revealed that changes in both branch lengths and procedural order of correction for body size and phylogeny do not generally have an effect on phylogenetic comparisons. These results demonstrate that the evolution of claw and toe morphology is correlated with the evolution of clinging performance across a wide range lizard taxa.     

Functional morphology of the hindlimb of tupaiids (Mammalia,Scandentia) and its phylogenetic implications

In this study, the hindlimb of 12 species of tupaiids was analyzed functionally and compared to that of primates, dermopterans, and chiropterans. Many aspects of the tupaiid hindlimb vary in relation to differential substrate use. These differences include width of the ilium, shape of the acetabulum, size of the anterior inferior iliac spine, size of the greater and third trochanters, depth of the femoral condyles, shape of the patellar groove, and size of the tibial tuberosity. The hindlimb of the arboreal Ptilocercus lowii, the only ptilocercine, is better adapted for arboreal locomotion, whereas that of tupaiines is better adapted for rapid terrestrial (or scansorial) locomotion. The hindlimb of Ptilocercus seems to be habitually flexed and has more joint mobility, a condition necessary for movement on uneven, discontinuous arboreal supports. The tarsus of Ptilocercus facilitates inversion of the foot and its grasping hallux is capable of a great range of abduction. Tupaiines, on the other hand, are characterized by more extended hindlimbs and less mobility in their joints. These restricted joints limit movements more to the parasagittal plane, which increases the efficiency of locomotion on a more even and continuous surface like the ground. The hindlimb of tupaiines is adapted for powerful flexion and extension. Even the most arboreal tupaiines remain similar to terrestrial tupaiines in their hindlimb morphology, which probably reflects the terrestrial ancestry of Tupaiinae (but not Tupaiidae). Many attributes of the tupaiid hindlimb, especially those of the foot, reflect the arboreal ancestry of Tupaiidae and it is proposed that the ancestral tupaiid was arboreal like Ptilocercus. Also, compared to the hindlimb character states of tupaiines, those of Ptilocercus are more similar to those of other archontans, and it is proposed that the hindlimb features of Ptilocercus are primitive for the Tupaiidae. Hence, Ptilocercus should be considered in any phylogenetic analysis that includes Scandentia.     

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.     

EVOLUTION OF SCAPULA SIZE AND SHAPE IN DIDELPHID MARSUPIALS (DIDELPHIMORPHIA: DIDELPHIDAE)

The New World family Didelphidae, the basal lineage within marsupials, is commonly viewed as morphologically conservative, yet includes aquatic, terrestrial, scansorial, and arboreal species. Here, I quantitatively estimated the existing variability in size and shape of the Didelphidae scapula (1076 specimens from 56 species) using geometric morphometrics, and compared size and shape differences to evolutionary and ecologic distances. I found considerable variation in the scapula morphology, most of it related to size differences between species. This results in morphologic divergence between different locomotor habits in larger species (resulting from increased mechanical loads), but most smaller species present similarly shaped scapulae. The only exceptions are the water opossum and the short-tailed opossums, and the functional explanations for these differences remain unclear. Scapula size and shape were mapped onto a molecular phylogeny for 32 selected taxa and ancestral size and shapes were reconstructed using squared-changed parsimony. Results indicate that the Didelphidae evolved from a medium- to small-sized ancestor with a generalized scapula, slightly more similar to arboreal ones, but strikingly different from big-bodied present arboreal species, suggesting that the ancestral Didelphidae was a small scansorial animal with no particular adaptations for arboreal or terrestrial habits, and these specializations evolved only in larger-bodied clades.     

Partial humeri of two Miocene Colombian primates

Distal portions of humeri from two Miocene Colombian primates were recovered during field work in 1986. The larger IGM 183420 is very similar in size and morphology to the humerus included in the type specimen of Cebupithecia sarmientoi, recovered from La Venta in 1945 (Stirton and Savage: Serv. Geol. Nac. Bogata 7:345-356, 1951) and is assigned to this taxon. IGM 183420 presents a number of features of the humerus associated with clinging postural behaviors in living platyrrhines, including a medial epicondyle with very little dorsal angulation, a cylindrical trochlea, and a contact facet for the coronoid process of the ulna. In these and other features Cebupithecia most closely resembles the extant genus Pithecia. IGM 183512 is approximately the size of Saimiri sciureus and is very similar in morphology to the humerus of this small arboreal quadruped. The medial epicondyle is more dorsally angled, the medial lip of the trochlea is more pronounced and the capitulum is less spherical as compared to Cebupithecia. This fossil is assigned to the taxon Neosaimiri fieldsi.     

Ecological divergence and talar morphology in gorillas

Gorillas occupy a variety of habitats from the west coast to eastern central Africa. These habitats differ considerably in altitude, which has a pronounced effect on forest ecology. Although all gorillas are obligate terrestrial knuckle‐walking quadrupeds, those that live in lowland habitats eat fruits and climb more often than do those living in highland habitats. Here we test the hypothesis that gorilla talus morphology falls along a morphocline that tracks locomotor function related to a more inverted or everted foot set. This proposed morphocline predicts that gorillas living in lowland habitats may have a talocrural joint configured to facilitate a more medially oriented foot during climbing, suggesting that they may be more adaptively committed to arboreality than gorillas living in highland habitats. To quantify the relative set of the foot in gorillas, we chose two three‐dimensional measurements of the talocrural joint: mediolateral curvature of the trochlea and relative surface area of the lateral malleolus. Our results show that, in comparison to their eastern counterparts, western gorillas have talar features that reflect a more medially directed sole of the foot. This morphology likely facilitates foot placement in a wider range of positions and minimization of shearing stresses across the joint when the foot is loaded on more curved or vertically oriented substrates as occurs during climbing and other arboreal behaviors. In contrast, eastern gorilla talar morphology is consistent with habitual placement of the foot with the sole directed more inferiorly, suggesting more effective loading during plantigrade push‐off on terrestrial substrates. Am J Phys Anthropol 153:526–541, 2014. © 2013 Wiley Periodicals, Inc.     

Divergent morphologies, performance, and escape behaviour in two tropical rock-using lizards (Reptilia: Scincidae)

The present study quantified microhabitat use, morphology, performance (sprinting, climbing, clinging, and jumping), and escape behaviour of two closely related tropical rock-using lizards. Specifically, the study tested whether: (1) a flatter body and longer limbs enhance performance in rocky habitats; (2) escape behaviour supports predictions based on habitat openness; and (3) there is a trade-off between sprinting and climbing performance. Despite the occupation of generally similar rocky habitats, the habitat of Carlia scirtetis was more open and composed of larger boulders with more regular surfaces, whereas the habitat of Carlia mundivensis was composed of more undergrowth and leaf litter, consisting of smaller boulders with irregular surfaces. The longer legs, flatter body, and greater sprinting and climbing ability of C. scirtetis, supports ecomorphological predictions. By contrast to predictions based on habitat openness, C. scirtetis allowed a potential threat to approach closer and ran further to a refuge than C. mundivensis , suggesting that escape behaviour as determined by performance may be species-specific or decoupled in these two species. The increased sprint speed of C. scirtetis highlighted a performance trade-off, with climbing speed lagging behind that of sprint speed. These results suggest that subtle differences in the structural microhabitat and the degree of habitat openness may ultimately result in substantial differences in morphology, performance, and threat behaviour in closely-related lizard species.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 85–98.     

Length–mass allometry in snakes

Body size and body shape are tightly related to an animal's physiology, ecology and life history, and, as such, play a major role in understanding ecological and evolutionary phenomena. Because organisms have different shapes, only a uniform proxy of size, such as mass, may be suitable for comparisons between taxa. Unfortunately, snake masses are rarely reported in the literature. On the basis of 423 species of snakes in 10 families, we developed clade‐specific equations for the estimation of snake masses from snout–vent lengths and total lengths. We found that snout–vent lengths predict masses better than total lengths. By examining the effects of phylogeny, as well as ecological and life history traits on the relationship between mass and length, we found that viviparous species are heavier than oviparous species, and diurnal species are heavier than nocturnal species. Furthermore, microhabitat preferences profoundly influence body shape: arboreal snakes are lighter than terrestrial snakes, whereas aquatic snakes are heavier than terrestrial snakes of a similar length. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ●● , ●●–●●.     

Digest: Microhabitat use and developmental timing shape anuran limb evolution*

Do frog limb shapes reflect microhabitat use against the backdrop of shared ancestry, body size variation, and developmental constraints? Stepanova and Womack found that when phylogeny and body size are controlled, microhabitat use is a key factor in explaining anuran limb evolution. The shape of distal limb elements in anuran limbs also evolves at a higher rate than proximal elements, suggesting that a relaxation of developmental constraints in distal elements may be shared across tetrapod limb development.     

Phylogenetic analysis of ecomorphological divergence, community structure, and diversification rates in dusky salamanders (Plethodontidae: Desmognathus)

An important dimension of adaptive radiation is the degree to which diversification rates fluctuate or remain constant through time. Focusing on plethodontid salamanders of the genus Desmognathus, we present a novel synthetic analysis of phylogeographic history, rates of ecomorphological evolution and species accumulation, and community assembly in an adaptive radiation. Dusky salamanders are highly variable in life history, body size, and ecology, with many endemic lineages in the southern Appalachian Highlands of eastern North America. Our results show that life-history evolution had important consequences for the buildup of plethodontid-salamander species richness and phenotypic disparity in eastern North America, a global hot spot of salamander biodiversity. The origin of Desmognathus species with aquatic larvae was followed by a high rate of lineage accumulation, which then gradually decreased toward the present time. The peak period of lineage accumulation in the group coincides with evolutionary partitioning of lineages with aquatic larvae into seepage, stream-edge, and stream microhabitats. Phylogenetic simulations demonstrate a strong correlation between morphology and microhabitat ecology independent of phylogenetic effects and suggest that ecomorphological changes are concentrated early in the radiation of Desmognathus. Deep phylogeographic fragmentation within many codistributed ecomorph clades suggests long-term persistence of ecomorphological features and stability of endemic lineages and communities through multiple climatic cycles. Phylogenetic analyses of community structure show that ecomorphological divergence promotes the coexistence of lineages and that repeated, independent evolution of microhabitat-associated ecomorphs has a limited role in the evolutionary assembly of Desmognathus communities. Comparing and contrasting our results to other adaptive radiations having different biogeographic histories, our results suggest that rates of diversification during adaptive radiation are intimately linked to the degree to which community structure persists over evolutionary time.     

Intraspecific correlations among morphology, performance and habitat use within a green anole lizard (Anolis carolinensis) population

We examined habitat use, morphology, jumping and clinging ability for 403 juvenile, female and male green anole lizards, Anolis carolinensis, in a population in south‐eastern Louisiana. We sought to answer three questions: (1) Do age/sex classes differ in habitat use, morphology and performance ability? (2) Do habitat use, morphology and performance correlate among all individuals across three age/sex classes (juveniles, females and males)? (3) Do juveniles compensate for their poor absolute performance capacities by being better performers on a relative scale? The three age/sex classes were found to differ significantly in size‐adjusted morphology, habitat use and size‐adjusted performance capacity. Juveniles tended to occupy perches which were closer together than those of adult males and females. The distal elements of the hindlimb (femur, tibia) were significantly longer in males than in females and juveniles, while females were more stocky than males and juveniles. The only significant overall ecomorphological relationship detected was between the lengths of the distal hindlimb elements and maximum jump acceleration. Our hypothesis that juveniles should be better performers (relative to size) compared to adults was disproved, as adult females were always the best performers relative to size. Our analysis of a mainland anole population presents a different view of population structure compared to similar studies involving Caribbean Anolis lizards, which show more ecological differentiation among age/sex classes, and also show that juveniles are relatively good performers. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85 , 211–221.