Virginia Abdala

From fish to modern humans – comparative anatomy, homologies and evolution of the head and neck musculature

In a recent paper Diogo (2008) reported the results of the first part of an investigation of the comparative anatomy, homologies and evolution of the head and neck muscles of osteichthyans (bony fish + tetrapods). That report mainly focused on actinopterygian fish, but also compared these fish with certain non‐mammalian sarcopterygians. The present paper focuses mainly on sarcopterygians, and particularly on how the head and neck muscles have evolved during the transitions from sarcopterygian fish and non‐mammalian tetrapods to monotreme and therian mammals, including modern humans. The data obtained from our dissections of the head and neck muscles of representative members of sarcopterygian fish, amphibians, reptiles, monotremes and therian mammals, such as rodents, tree‐shrews, colugos and primates, including modern humans, are compared with the information available in the literature. Our observations and comparisons indicate that the number of mandibular and true branchial muscles (sensu this work) present in modern humans is smaller than that found in mammals such as tree‐shrews, rats and monotremes, as well as in reptiles such as lizards. Regarding the pharyngeal musculature, there is an increase in the number of muscles at the time of the evolutionary transition leading to therian mammals, but there was no significant increase during the transition leading to the emergence of higher primates and modern humans. The number of hypobranchial muscles is relatively constant within the therian mammals we examined, although in this case modern humans have more muscles than other mammals. The number of laryngeal and facial muscles in modern humans is greater than that found in most other therian taxa. Interestingly, modern humans possess peculiar laryngeal and facial muscles that are not present in the majority of the other mammalian taxa; this seems to corroborate the crucial role played by vocal communication and by facial expressions in primate and especially in human evolution. It is hoped that by compiling, in one paper, data about the head and neck muscles of a wide range of sarcopterygians, the present work could be useful to comparative anatomists, evolutionary biologists and functional morphologists and to researchers working in other fields such as developmental biology, genetics and/or evolutionary developmental biology.

From fish to modern humans – comparative anatomy, homologies and evolution of the pectoral and forelimb musculature

In a recent study Diogo & Abdala [(2007 ) J Morphol 268, 504–517] reported the results of the first part of a research project on the comparative anatomy, homologies and evolution of the pectoral muscles of osteichthyans (bony fish and tetrapods). That report mainly focused on actinopterygian fish but also compared these fish with certain non‐mammalian sarcopterygians. This study, which reports the second part of the research project, focuses mainly on sarcopterygians and particularly on how the pectoral and forelimb muscles have evolved during the transitions from sarcopterygian fish and non‐mammalian tetrapods to monotreme and therian mammals and humans. The data obtained by our own dissections of all the pectoral and forelimb muscles of representative members of groups as diverse as sarcopterygian fish, amphibians, reptiles, monotremes and therian mammals such as rodents, tree‐shrews, colugos and primates, including humans, are compared with the information available in the literature. Our observations and comparisons clearly stress that, with regard to the number of pectoral and forelimb muscles, the most striking transition within sarcopterygian evolutionary history was that leading to the origin of tetrapods. Whereas extant sarcopterygian fish have an abductor and adductor of the fin and a largely undifferentiated hypaxial and epaxial musculature, extant salamanders such as Ambystoma have more than 40 pectoral and forelimb muscles. There is no clear increase in the number of pectoral and forelimb muscles within the evolutionary transition that led to the origin of mammals and surely not to that leading to the origin of primates and humans.

Getting a grip on tetrapod grasping: form, function, and evolution

Human beings have been credited with unparalleled capabilities for digital prehension grasping. However, grasping behaviour is widespread among tetrapods. The propensity to grasp, and the anatomical characteristics that underlie it, appear in all of the major groups of tetrapods with the possible exception of terrestrial turtles. Although some features are synapomorphic to the tetrapod clade, such as well‐defined digits and digital musculature, other features, such as opposable digits and tendon configurations, appear to have evolved independently in many lineages. Here we examine the incidence, functional morphology, and evolution of grasping across four major tetrapod clades. Our review suggests that the ability to grasp with the manus and pes is considerably more widespread, and ecologically and evolutionarily important, than previously thought. The morphological bases and ecological factors that govern grasping abilities may differ among tetrapods, yet the selective forces shaping them are likely similar. We suggest that further investigation into grasping form and function within and among these clades may expose a greater role for grasping ability in the evolutionary success of many tetrapod lineages.

The interplay between claw morphology and microhabitat use in neotropical iguanian lizards.

Traditionally, it has been suggested that variation in locomotor mode should be correlated with variation in the anatomy of the structures responsible for locomotion. Indeed, organisms can expand their ecological niche by using specialized traits of the locomotor system including hooks, claws, adhesive pads, etc. Despite the fact that claws are the most common biological mechanism of clinging in vertebrates, little is known about their function or evolutionary relationship to habitat use. The present study focuses on claw morphology in 57 species of iguanian lizards occupying different microhabitats. Qualitative differences in claw shape were explored by means of digital photographs, and quantitative measurements of the length, height and curvature of the claws of both fingers and toes were taken and correlated to information on microhabitat use obtained from the literature. Our analyses showed a strong phylogenetic component that obscured relationships between morphology and ecology. Our results also show differences in claw morphology between species that appear to be related to microhabitat use (climbing versus terrestrial species), with the best ecological descriptors being claw length and height. Performance measures and biomechanical analyses of claw function may consequently be better suited to explain the evolution of claw shape in relation to habitat use in this group.

Skull anatomy of the miniaturized gecko Sphaerodactylus roosevelti (Squamata: Gekkota)

A detailed description of the skull and jaw of the gecko Sphaerodactylus roosevelti is presented. The bones are described articulated and isolated with special consideration given to the type of suture among joining elements. S. roosevelti was compared with 109 gekkotan species to evaluate the osteological variation and to find characters for cladistic analysis. Changes in the skull associated with the miniaturization process are discussed within the sphaerodactylid geckos. A noticeable increase of overlapping sutures was observed in the snout of the smallest sphaerodactylids compared to other gekkotans. This pattern is convergent with that in miniaturized pygopodids and may be attributed to adaptations for decreasing mechanical resistance of the cranium during feeding or burrowing. New cranial characters support Sphaerodactylinae as a monophyletic group and should be useful for resolving questions such as their relationship with other gekkotans. J. Morphol. 269:1340–1364, 2008.

Developmental Basis of Limb Homology in Lizards

Shubin and Alberch (Evol Biol 1986 ;20:319–387) proposed a scheme of tetrapod limb development based on cartilage morphogenesis that provides the arguments to interpret the homologies of skeletal elements and sets the basis to explain limb specialization through later developmental modification. Morphogenetic evidence emerged from the study of some reptiles, but the availability of data for lizards is limited. Here, the study of adult skeletal variation in 41 lizard taxa and ontogeny in species of Liolaemus and Tupinambis attempts to fill in this gap and provides supporting evidence for the Shubin‐Alberch scheme. Six questions are explored. Is there an intermedium in the carpus? Are there two centralia in the carpus? Is there homology among proximal tarsalia of reptiles? Does digit V belong to the digital arch? Is the pisiform an element of the autopodium plan? And should the ossification processes be similar to cartilage morphogenesis? We found the following answers. Some taxa exhibit an ossified element that could represent an intermedium. There is one centrale in the carpus. Development of proximal tarsalia seems to be equivalent with that observed among reptiles. Digit V could arise from the digital arch. Pisiform does not arise as part of the limb plan. And different patterns of ossification occur following a single and conservative cartilaginous configuration. Lizard limb development shows an early pattern common to other reptiles with clear primary axis and digital arch. The pattern then becomes lizard‐specific with specialization involving some reduction in prechondrogenic elements. Anat Rec 2007.

Comparative anatomy, homologies and evolution of the pectoral and forelimb musculature of tetrapods with special attention to extant limbed amphibians and reptiles.

The main aim of the present work is to synthesize the information obtained from our dissections of the pectoral and forelimb muscles of representative members of the major extant taxa of limbed amphibians and reptiles and from our review of the literature, in order to provide an account of the comparative anatomy, homologies and evolution of these muscles in the Tetrapoda. The pectoral and forelimb musculature of all these major taxa conform to a general pattern that seems to have been acquired very early in the evolutionary history of tetrapods. Although some muscles are missing in certain taxa, and a clear departure from this general pattern is obviously present in derived groups such as birds, the same overall configuration is easily distinguishable in these taxa. Among the most notable anatomical differences between the groups, one that seems to have relevant evolutionary and functional implications, concerns the distal insertion points of the forearm musculature. In tetrapods, the muscles of the radial and ulnar complexes of the forearm are pleisomorphically mainly inserted onto the radius/ulna or onto the more proximal carpal bones, but in mammals some of these muscles insert more distally onto bones such as the metacarpals. Interestingly, a similar trend towards a more distal insertion of these muscles is also found in some non‐mammalian tetrapod taxa, such as some anurans (e.g. Phyllomedusa). This may be correlated with the acquisition of more subtle digital movement abilities in these latter taxa.

Effects of different substrates on the sprint performance of lizards.

SUMMARY The variation in substrate structure is one of the most important determinants of the locomotor abilities of lizards. Lizards are found across a range of habitats, from large rocks to loose sand, each of them with conflicting mechanical demands on locomotion. We examined the relationships among sprint speed, morphology and different types of substrate surfaces in species of lizards that exploit different structural habitats (arboreal, saxicolous, terrestrial and arenicolous) in a phylogenetic context. Our main goals were to assess which processes drive variability in morphology (i.e. phylogeny or adaptation to habitat) in order to understand how substrate structure affects sprint speed in species occupying different habitats and to determine the relationship between morphology and performance. Liolaemini lizards show that most morphological traits are constrained by phylogeny, particularly toe 3, the femur and foot. All ecological groups showed significant differences on rocky surfaces. Surprisingly, no ecological group performed better on the surface resembling its own habitat. Moreover, all groups exhibited significant differences in sprint speed among the three different types of experimental substrates and showed the best performance on sand, with the exception of the arboreal group. Despite the fact that species use different types of habitats, the highly conservative morphology of Liolaemini species and the similar levels of performance on different types of substrates suggest that they confer to the ‘jack of all trades and master of none’ principle.

Morphology and function of the forelimb in arboreal frogs: specializations for grasping ability?

Frogs are characterized by a unique morphology associated with their saltatory lifestyle. Although variation in the form and function of the pelvic girdle and associated appendicular system related to specialized locomotor modes such as swimming or burrowing has been documented, the forelimbs have typically been viewed as relatively unspecialized. Yet, previous authors have noted versatility in forelimb function among arboreal frogs associated with feeding. Here we study the morphology and function of the forelimb and hand during locomotion in two species of arboreal frogs (Litoria caerulea and Phyllomedusa bicolor). Our data show a complex arrangement of the distal forelimb and hand musculature with some notable differences between species. Analyses of high‐speed video and video fluoroscopy recordings show that forelimbs are used in alternating fashion in a diagonal sequence footfall pattern and that the position of the hand is adjusted when walking on substrates of different diameters. Electromyographic recordings show that the flexors of the hand are active during substrate contact, suggesting the use of gripping to generate a stabilizing torque. Measurements of grasping forces in vivo and during stimulation experiments show that both species, are capable of executing a so‐called power grip but also indicates marked differences between species, in the magnitude of forces generated. Stimulation experiments showed an increased control of digit flexion in the more specialized of the two species, allowing it to execute a precision grip paralleled only by that seen in primates.

Relationships among morphology, clinging performance and habitat use in Liolaemini lizards

The central tenet of ecomorphological theory holds that different ecological requirements lead to different organismal designs (morphology). Here, we studied the relationships between performance (interlocking grasping) and forelimb morphological traits in species of lizards that exploit different structural habitats in a phylogenetic context. The performance (measured by the maximum force of clinging to substrate) was measured on different substrate types. After phylogenetically informed analyses, we found that arboreal and saxicolous species showed stronger resistance to mechanical traction in all substrates when compared to generalists and sand dweller lizards. These species showed a positive relationship between forelimb dimensions (humerus length and length of claw of toe 5) and maximum force exerted, on the contrary, hand width, claw height (CH) of digits III and IV and claw length of toe 4 showed a negative relationship. In addition, we observed a partial positive correlation between CH and maximal cling force on rough surfaces, but not on smooth surfaces.