Overview of Head Muscles with Special Emphasis on Extraocular Muscle Development.

The head is often considered the most complex part of the vertebrate body as many different cell types contribute to a huge variation of structures in a very limited space. Most of these cell types also interact with each other to ensure the proper development of skull, brain, muscles, nerves, connective tissue, and blood vessels. While there are general mechanisms that are true for muscle development all over the body, the head and postcranial muscle development differ from each other. In the head, specific gene regulatory networks underlie the differentiation in subgroups, which include extraocular muscles, muscles of mastication, muscles of facial expression, laryngeal and pharyngeal muscles, as well as cranial nerve innervated neck muscles. Here, I provide an overview of the difference between head and trunk muscle development. This is followed by a short excursion to the cardiopharyngeal field which gives rise to heart and head musculature and a summary of pharyngeal arch muscle development, including interactions between neural crest cells, mesodermal cells, and endodermal signals. Lastly, a more detailed description of the eye development, tissue interactions, and involved genes is provided.

Sequence of chondrocranial development in basal anurans-Let's make a cranium.

BACKGROUND: The craniofacial skeleton is an evolutionary innovation of vertebrates. Due to its complexity and importance to protect the brain and aid in essential functions (e.g., feeding), its development requires a precisely tuned sequence of chondrification and/or ossification events. The comparison of sequential patterns of cartilage formation bears important insights into the evolution of development. Discoglossus scovazzi is a basal anuran species. The comparison of its chondrocranium (cartilaginous neuro- & viscerocranium) development with other basal anurans (Xenopus laevis, Bombina orientalis) will help establishing the ancestral pattern of chondrification sequences in anurans and will serve as basis for further studies to reconstruct ancestral conditions in amphibians, tetrapods, and vertebrates. Furthermore, evolutionary patterns in anurans can be studied in the light of adaptations once the ancestral sequence is established. RESULTS: We present a comprehensive overview on the chondrocranium development of D. scovazzi. With clearing and staining, histology and 3D reconstructions we tracked the chondrification of 44 elements from the first mesenchymal Anlagen to the premetamorphic cartilaginous head skeleton and illustrate the sequential changes of the skull. We identified several anuran and discoglossoid traits of cartilage development. In D. scovazzi the mandibular, hyoid, and first branchial arch Anlagen develop first followed by stepwise addition of the branchial arches II, III, and IV. Nonetheless, there is no strict anterior to posterior chondrification pattern within the viscerocranium of D. scovazzi. Single hyoid arch elements chondrify after elements of the branchial arch and mandibular arch elements chondrify after elements of the branchial arch I. CONCLUSIONS: In Osteichthyes, neurocranial elements develop in anterior to posterior direction. In the anurans investigated so far, as well as in D. scovazzi, the posterior parts of the neurocranium extend anteriorly, while the anterior parts of the neurocranium, extend posteriorly until both parts meet and fuse. Anuran cartilaginous development differs in at least two crucial traits from other gnathostomes which further supports the urgent need for more developmental investigations among this clade to understand the evolution of cartilage development in vertebrates.

Anatomical comparison across heads, fore- and hindlimbs in mammals using network models.

Animal body parts evolve with variable degrees of integration that nonetheless yield functional adult phenotypes: but, how? The analysis of modularity with Anatomical Network Analysis (AnNA) is used to quantitatively determine phenotypic modules based on the physical connection among anatomical elements, an approach that is valuable to understand developmental and evolutionary constraints. We created anatomical network models of the head, forelimb, and hindlimb of two taxa considered to represent a 'generalized' eutherian (placental: mouse) and metatherian (marsupial: opossum) anatomical configuration and compared them with our species, which has a derived eutherian configuration. In these models, nodes represent anatomical units and links represent their physical connection. Here, we aimed to identify: (1) the commonalities and differences in modularity between species, (2) whether modules present a potential phylogenetic character, and (3) whether modules preferentially reflect either developmental or functional aspects of anatomy, or a mix of both. We predicted differences between networks of metatherian and eutherian mammals that would best be explained by functional constraints, versus by constraints of development and/or phylogeny. The topology of contacts between bones, muscles, and bones + muscles showed that, among all three species, skeletal networks were more similar than musculoskeletal networks. There was no clear indication that humans and mice are more alike when compared to the opossum overall, even though their musculoskeletal and skeletal networks of fore- and hindlimbs are slightly more similar. Differences were greatest among musculoskeletal networks of heads and next of forelimbs, which showed more variation than hindlimbs, supporting previous anatomical studies indicating that in general the configuration of the hindlimbs changes less across evolutionary history. Most observations regarding the anatomical networks seem to be best explained by function, but an exception is the adult opossum ear ossicles. These ear bones might form an independent module because the incus and malleus are involved in forming a functional primary jaw that enables the neonate to attach to the teat, where this newborn will complete its development. Additionally, the human data show a specialized digit 1 module (thumb/big toe) in both limb types, likely the result of functional and evolutionary pressures, as our ape ancestors had highly movable big toes and thumbs.

First use of anatomical networks to study modularity and integration of heads, forelimbs and hindlimbs in abnormal anencephalic and cyclopic vs normal human development.

The ill-named "logic of monsters" hypothesis of Pere Alberch - one of the founders of modern evo-devo - emphasized the importance of "internal rules" due to strong developmental constraints, linked teratologies to developmental processes and patterns, and contradicted hypotheses arguing that birth defects are related to a chaotic and random disarray of developmental mechanisms. We test these hypotheses using, for the first time, anatomical network analysis (AnNA) to study and compare the musculoskeletal modularity and integration of both the heads and the fore- and hindlimbs of abnormal cyclopic trisomy 18 and anencephalic human fetuses, and of normal fetal, newborn, and adult humans. Our previous works have shown that superficial gross anatomical analyses of these specimens strongly support the "logic of monsters" hypothesis, in the sense that there is an 'order' or 'logic' within the gross anatomical patterns observed in both the normal and abnormal individuals. Interestingly, the results of the AnNA done in the present work reveal a somewhat different pattern: at least concerning the musculoskeletal modules obtained in our AnNA, we observe a hybrid between the "logic of monsters" and the "lack of homeostasis" hypotheses. For instance, as predicted by the latter hypothesis, we found a high level of left-right asymmetry in the forelimbs and/or hindlimbs of the abnormal cyclopic trisomy 18 and anencephalic human fetuses. That is, a network analysis of the organization of/connection between the musculoskeletal structures of these fetuses reveals a more "chaotic" pattern than that detected by superficial gross anatomical comparisons. We discuss the broader developmental, evolutionary, and medical implications of these results.

Neural crest and the patterning of vertebrate craniofacial muscles.

Patterning of craniofacial muscles overtly begins with the activation of lineage-specific markers at precise, evolutionarily conserved locations within prechordal, lateral, and both unsegmented and somitic paraxial mesoderm populations. Although these initial programming events occur without influence of neural crest cells, the subsequent movements and differentiation stages of most head muscles are neural crest-dependent. Incorporating both descriptive and experimental studies, this review examines each stage of myogenesis up through the formation of attachments to their skeletal partners. We present the similarities among developing muscle groups, including comparisons with trunk myogenesis, but emphasize the morphogenetic processes that are unique to each group and sometimes subsets of muscles within a group. These groups include branchial (pharyngeal) arches, which encompass both those with clear homologues in all vertebrate classes and those unique to one, for example, mammalian facial muscles, and also extraocular, laryngeal, tongue, and neck muscles. The presence of several distinct processes underlying neural crest:myoblast/myocyte interactions and behaviors is not surprising, given the wide range of both quantitative and qualitative variations in craniofacial muscle organization achieved during vertebrate evolution.

Innervation of the Long Head of the Triceps Brachii in Humans-A Fresh Look.

The triceps brachii muscle occupies the posterior compartment of the arm in humans and has three heads. The lateral and medial heads originate from the humerus and the long head arises from the infraglenoid tubercle of the scapula. All heads form a common tendon that inserts onto the olecranon and the deep antebrachial fascia on each side of it. Each head receives its own motor branch, which all are thought to originate from the radial nerve. However, several studies reported that the motor branch of the long head of the triceps (LHT) arises from the axillary nerve or the posterior cord. Here, we dissected 27 triceps in 15 cadavers to analyze the innervation of the LHT and found only radial innervation, which contradicts those studies. We examined studies reporting that the motor branch to the LHT in humans does not arise from the radial nerve as well as studies of the triceps in primates. Occasional variations of the innervation of skeletal muscles are normal, but a change of principal motor innervation from radial to axillary nerve has important implications. This is because the axillary nerve is often involved during shoulder injuries. The precise identification of the prevalence of axillary versus radial innervation is therefore clinically relevant for surgery, nerve drafting, and occupational and physical therapy. We conclude that the primary motor branch to the LHT arises from the radial nerve but axillary/posterior cord innervations occur occasionally. We suggest the development of a standard methodology for further studies. Anat Rec, 301:473-483, 2018. © 2018 Wiley Periodicals, Inc.

Cephalic muscle development in the Australian lungfish, Neoceratodus forsteri.

Lungfishes are the extant sister group of tetrapods. As such, they are important for the study of evolutionary processes involved in the water to land transition of vertebrates. The evolution of a true neck, that is, the complete separation of the pectoral girdle from the cranium, is one of the most intriguing morphological transitions known among vertebrates. Other salient changes involve new adaptations for terrestrial feeding, which involves both the cranium and its associated musculature. Historically, the cranium has been extensively investigated, but the development of the cranial muscles much less so. Here, we present a detailed study of cephalic muscle development in the Australian lungfish, Neoceratodus forsteri, which is considered to be the sister taxon to all other extant lungfishes. Neoceratodus shows several developmental patterns previously described in other taxa; the tendency of muscles to develop from anterior to posterior, from their region of origin toward insertion, and from lateral to ventral/medial (outside-in), at least in the branchial arches. The m.protractor pectoralis appears to develop as an extension of the most posterior m.levatores arcuum branchialium, supporting the hypothesis that the m.cucullaris and its derivatives (protractor pectoralis, levatores arcuum branchialium) are branchial muscles. We present a new hypothesis regarding the homology of the ventral branchial arch muscles (subarcualis recti and obliqui, transversi ventrales) in lungfishes and amphibians. Moreover, the morphology and development of the cephalic muscles confirms that extant lungfishes are neotenic and have been strongly influenced via paedomorphosis during their evolutionary history.

Anatomical variations of the deep head of Cruveilhier of the flexor pollicis brevis and its significance for the evolution of the precision grip.

Cruveilhier described in 1834 the human flexor pollicis brevis (FPB), a muscle of the thenar compartment, as having a superficial and a deep head, respectively, inserted onto the radial and ulnar sesamoids of the thumb. Since then, Cruveilhier's deep head has been controversially discussed. Often this deep head is confused with Henle's "interosseous palmaris volaris" or said to be a slip of the oblique adductor pollicis. In the 1960s, Day and Napier described anatomical variations of the insertions of Cruveilhier's deep head, including its absence, and hypothesized, that the shift of the deep head's insertion from ulnar to radial facilitated "true opposability" in anthropoids. Their general thesis for muscular arrangements underlying the power and precision grip is sound, but they did not delineate their deep head from Henle's muscle or the adductor pollicis, and their description of the attachments of Cruveilhier's deep head were too vague and not supported by a significant portion of the anatomical literature. Here, we reinvestigated Cruveilhier's deep head to resolve the controversy about it and because many newer anatomy textbooks do not describe this muscle, while it is often an obvious functionally (writing, texting, precision grip) and clinically significant thenar muscle. For the first time, we empirically delineated Cruveilhier's deep head from neighboring muscles with which it was previously confused. We observed 100% occurrence of the uncontested deep head in 80 human hands, displaying a similar variability of insertions as Day and Napier, but in significantly different numbers. Furthermore, we found variability in the origin and included as important landmarks the trapezoid and the ligamentum carpi radiatum. We tested the assertion regarding the evolutionary morphology and its role in the improvements in thumb movements during various precision grips. Our overall conclusions differ with respect to the developmental and evolutionary origin of the FPB heads.

Muscle development in the shark Scyliorhinus canicula: implications for the evolution of the gnathostome head and paired appendage musculature.

BACKGROUND: The origin of jawed vertebrates was marked by profound reconfigurations of the skeleton and muscles of the head and by the acquisition of two sets of paired appendages. Extant cartilaginous fish retained numerous plesiomorphic characters of jawed vertebrates, which include several aspects of their musculature. Therefore, myogenic studies on sharks are essential in yielding clues on the developmental processes involved in the origin of the muscular anatomy. RESULTS: Here we provide a detailed description of the development of specific muscular units integrating the cephalic and appendicular musculature of the shark model, Scyliorhinus canicula. In addition, we analyze the muscle development across gnathostomes by comparing the developmental onset of muscle groups in distinct taxa. Our data reveal that appendicular myogenesis occurs earlier in the pectoral than in the pelvic appendages. Additionally, the pectoral musculature includes muscles that have their primordial developmental origin in the head. This culminates in a tight muscular connection between the pectoral girdle and the cranium, which founds no parallel in the pelvic fins. Moreover, we identified a lateral to ventral pattern of formation of the cephalic muscles, that has been equally documented in osteichthyans but, in contrast with these gnathostomes, the hyoid muscles develop earlier than mandibular muscle in S. canicula. CONCLUSION: Our analyses reveal considerable differences in the formation of the pectoral and pelvic musculatures in S. canicula, reinforcing the idea that head tissues have contributed to the formation of the pectoral appendages in the common ancestor of extant gnathostomes. In addition, temporal differences in the formation of some cranial muscles between chondrichthyans and osteichthyans might support the hypothesis that the similarity between the musculature of the mandibular arch and of the other pharyngeal arches represents a derived feature of jawed vertebrates.

A detailed musculoskeletal study of a fetus with anencephaly and spina bifida (craniorachischisis), and comparison with other cases of human congenital malformations.

Few descriptions of the musculoskeletal system of humans with anencephaly or spina bifida exist in the literature. Even less is published about individuals in which both phenomena occur together, i.e. about craniorachischisis. Here we provide a detailed report on the musculoskeletal structures of a fetus with craniorachischisis, as well as comparisons with the few descriptions for anencephaly and with musculoskeletal anomalies found in other congenital malformations. We focused in particular on the comparison with trisomies 13, 18, and 21 because neural tube defects have been associated with such chromosomal defects. Our results showed that many of the defects found in the fetus with craniorachischisis are similar not only to anomalies previously described in the available works on musculoskeletal phenotypes seen in fetuses with anencephaly and spina bifida, but also to a wide range of other different conditions/syndromes including trisomies 13, 18 and 21, and cyclopia. The fact that similar anomalies are seen commonly not only in a wide range of different syndromes, but also as variants of the normal human population and as the 'normal' phenotype of other animals, supports Pere Alberch's unfortunately named idea of a 'logic of monsters'. That is, it supports the idea that development is so constrained that both in 'normal' and abnormal development one sees certain outcomes being produced again and again because ontogenetic constraints only allow a few possible outcomes, thus also leading to cases where the anatomical defects of some organisms are similar to the 'normal' phenotype of other organisms. In fact, this applies not only to specific anomalies but also to general patterns, such as the fact that in pathological conditions affecting different regions of the body, one consistently sees more defects on the upper limbs than on the lower limbs. Such general patterns are, again, seen in the fetus examined for this study, which had 29 muscle anomalies on the right upper limb and 22 muscle anomalies on the left upper limb, vs. seven muscle anomalies on the right lower limb and two on the left lower limb. It is therefore hoped that this work, which is part of our effort to describe and compile information on human musculoskeletal defects found in a wide range of conditions, will contribute not only to a better understanding of craniorachischisis in particular and of human congenital malformations in general, but also to broader discussions on the fields of comparative anatomy, and developmental and evolutionary biology.

An untold story: The important contributions of Muslim scholars for the understanding of human anatomy.

It is usually assumed that Galen is one of the fathers of anatomy and that between the Corpus Galenicum and the Renaissance there was no major advance in anatomical knowledge. However, it is also consensually accepted that Muslim scholars had the intellectual leadership from the 8th/9th to 13th centuries, and that they made remarkable progresses in numerous scientific fields including medicine. So, how is it possible that they did not contribute to advance human anatomy during that period? According to the dominant view, Muslim scholars exclusively had a passive role: their transmission of knowledge from the Greeks to the West. Here, we summarize, for the first time in a single paper, the studies of major Muslim scholars that published on human anatomy before Vesalius. This summary is based on analyses of original Arabic texts and of more recent publications by anatomists and historians, and on comparisons between the descriptions provided by Galen and by these Muslim scholars. We show that Arabic speakers and Persians made important advances in human anatomy well before Vesalius. The most notable exception concerns the muscular system: strikingly, there were apparently neither advances made by Muslims nor by Westerners for more than 1000 years. Unbiased discussions of these and other related issues, and particularly of the mainly untold story about the major contributions of Muslim scholars to anatomy, are crucial to our knowledge of the history of anatomy, biology and sciences, and also of our way of thinking, biases, and prejudices. Anat Rec, 300:986-1008, 2017. © 2017 Wiley Periodicals, Inc.

Evolutionary developmental pathology and anthropology: A new field linking development, comparative anatomy, human evolution, morphological variations and defects, and medicine.

We introduce a new subfield of the recently created field of Evolutionary-Developmental-Anthropology (Evo-Devo-Anth): Evolutionary-Developmental-Pathology-and-Anthropology (Evo-Devo-P'Anth). This subfield combines experimental and developmental studies of nonhuman model organisms, biological anthropology, chordate comparative anatomy and evolution, and the study of normal and pathological human development. Instead of focusing on other organisms to try to better understand human development, evolution, anatomy, and pathology, it places humans as the central case study, i.e., as truly model organism themselves. We summarize the results of our recent Evo-Devo-P'Anth studies and discuss long-standing questions in each of the broader biological fields combined in this subfield, paying special attention to the links between: (1) Human anomalies and variations, nonpentadactyly, homeotic transformations, and "nearest neighbor" vs. "find and seek" muscle-skeleton associations in limb+facial muscles vs. other head muscles; (2) Developmental constraints, the notion of "phylotypic stage," internalism vs. externalism, and the "logic of monsters" vs. "lack of homeostasis" views about human birth defects; (3) Human evolution, reversions, atavisms, paedomorphosis, and peromorphosis; (4) Scala naturae, Haeckelian recapitulation, von Baer's laws, and parallelism between phylogeny and development, here formally defined as "Phylo-Devo parallelism"; and (5) Patau, Edwards, and Down syndrome (trisomies 13, 18, 21), atavisms, apoptosis, heart malformations, and medical implications.

Development, metamorphosis, morphology, and diversity: The evolution of chordate muscles and the origin of vertebrates.

Recent findings that urochordates are the closest sister-group of vertebrates have dramatically changed our understanding of chordate evolution and vertebrate origins. To continue to deepen our understanding of chordate evolution and diversity, in particular the morphological and taxonomical diversity of the vertebrate clade, one must explore the origin, development, and comparative anatomy of not only hard tissues, but also soft tissues such as muscles. Building on a recent overview of the discovery of a cardiopharyngeal field in urochordates and the profound implications for reconstructing the origin and early evolution of vertebrates, in this study we focus on the broader comparative and developmental anatomy of chordate cephalic muscles and their relation to life history, and to developmental, morphological and taxonomical diversity. We combine our recent findings on cephalochordates, urochordates, and vertebrates with a literature review and suggest that developmental changes related to metamorphosis and/or heterochrony (e.g., peramorphosis) played a crucial role in the early evolution of chordates and vertebrates. Recent studies reviewed here supported de Beer's "law of diversity" that peramorphic animals (e.g., ascidians, lampreys) are taxonomically and morphologically less diverse than nonperamorphic animals (e.g., gnathostomes), probably because their "too specialized" development and adult anatomy constrain further developmental and evolutionary innovations. Developmental Dynamics 244:1046-1057, 2015. © 2014 Wiley Periodicals, Inc.

Genetically induced abnormal cranial development in human trisomy 18 with holoprosencephaly: comparisons with the normal tempo of osteogenic-neural development.

Craniofacial malformations are common congenital defects caused by failed midline inductive signals. These midline defects are associated with exposure of the fetus to exogenous teratogens and with inborn genetic errors such as those found in Down, Patau, Edwards' and Smith-Lemli-Opitz syndromes. Yet, there are no studies that analyze contributions of synchronous neurocranial and neural development in these disorders. Here we present the first in-depth analysis of malformations of the basicranium of a holoprosencephalic (HPE) trisomy 18 (T18; Edwards' syndrome) fetus with synophthalmic cyclopia and alobar HPE. With a combination of traditional gross dissection and state-of-the-art computed tomography, we demonstrate the deleterious effects of T18 caused by a translocation at 18p11.31. Bony features included a single developmentally unseparated frontal bone, and complete dual absence of the anterior cranial fossa and ethmoid bone. From a superior view with the calvarium plates removed, there was direct visual access to the orbital foramen and hard palate. Both the eyes and the pituitary gland, normally protected by bony structures, were exposed in the cranial cavity and in direct contact with the brain. The middle cranial fossa was shifted anteriorly, and foramina were either missing or displaced to an abnormal location due to the absence or misplacement of its respective cranial nerve (CN). When CN development was conserved in its induction and placement, the respective foramen developed in its normal location albeit with abnormal gross anatomical features, as seen in the facial nerve (CNVII) and the internal acoustic meatus. More anteriorly localized CNs and their foramina were absent or heavily disrupted compared with posterior ones. The severe malformations exhibited in the cranial fossae, orbital region, pituitary gland and sella turcica highlight the crucial involvement of transcription factors such as TGIF, which is located on chromosome 18 and contributes to neural patterning, in the proper development of neural and cranial structures. Our study of a T18 specimen emphasizes the intricate interplay between bone and brain development in midline craniofacial abnormalities in general.

A new heart for a new head in vertebrate cardiopharyngeal evolution.

It has been more than 30 years since the publication of the new head hypothesis, which proposed that the vertebrate head is an evolutionary novelty resulting from the emergence of neural crest and cranial placodes. Neural crest generates the skull and associated connective tissues, whereas placodes produce sensory organs. However, neither crest nor placodes produce head muscles, which are a crucial component of the complex vertebrate head. We discuss emerging evidence for a surprising link between the evolution of head muscles and chambered hearts - both systems arise from a common pool of mesoderm progenitor cells within the cardiopharyngeal field of vertebrate embryos. We consider the origin of this field in non-vertebrate chordates and its evolution in vertebrates.

Towards the resolution of a long-standing evolutionary question: muscle identity and attachments are mainly related to topological position and not to primordium or homeotic identity of digits.

Signaling for limb bone development usually precedes that for muscle development, such that cartilage is generally present before muscle formation. It remains obscure, however, if: (i) tetrapods share a general, predictable spatial correlation between bones and muscles; and, if that is the case, if (ii) such a correlation would reflect an obligatory association between the signaling involved in skeletal and muscle morphogenesis. We address these issues here by using the results of a multidisciplinary analysis of the appendicular muscles of all major tetrapod groups integrating dissections, muscle antibody stainings, regenerative and ontogenetic analyses of fluorescently-labeled (GFP) animals, and studies of non-pentadactyl human limbs related to birth defects. Our synthesis suggests that there is a consistent, surprising anatomical pattern in both normal and abnormal phenotypes, in which the identity and attachments of distal limb muscles are mainly related to the topological position, and not to the developmental primordium (anlage) or even the homeotic identity, of the digits to which they are attached. This synthesis is therefore a starting point towards the resolution of a centuries-old question raised by authors such as Owen about the specific associations between limb bones and muscles. This question has crucial implications for evolutionary and developmental biology, and for human medicine because non-pentadactyly is the most common birth defect in human limbs. In particular, this synthesis paves the way for future developmental experimental and mechanistic studies, which are needed to clarify the processes that may be involved in the elaboration of the anatomical patterns described here, and to specifically test the hypothesis that distal limb muscle identity/attachment is mainly related to digit topology.

Retraction: 'Development, Metamorphosis, Morphology and Diversity: Evolution of Chordates muscles and the Origin of Vertebrates'.

The above article, published as an Accepted Article online on December 5, 2014, in Wiley Online Library (wileyonlinelibrary.com), has been retracted by agreement between the authors, the journal Editor in Chief, Parker B. Antin, and Wiley Periodicals, Inc. The retraction has been agreed due to an error at the publishers, which resulted in a preliminary draft of the article being posted online. The correct article, 'Development, metamorphosis, morphology and diversity: the evolution of chordate muscles and the origin of vertebrates' by Rui Diogo and Janine M. Ziermann, was published online on December 22, 2014, doi: 10.1002/dvdy.24245. REFERENCES: Diogo R, Ziermann JM. 2014. Development, Metamorphosis, Morphology and Diversity: The Evolution of Chordate muscles and the Origin of Vertebrates. Dev. Dyn., 10.1002/dvdy.24236 Diogo R, Ziermann JM. 2014. Development, Metamorphosis, Morphology and Diversity: The Evolution of Chordate muscles and the Origin of Vertebrates. Dev. Dyn., 10.1002/dvdy.24245.

Is evolutionary biology becoming too politically correct? A reflection on the scala naturae, phylogenetically basal clades, anatomically plesiomorphic taxa, and 'lower' animals.

The notion of scala naturae dates back to thinkers such as Aristotle, who placed plants below animals and ranked the latter along a graded scale of complexity from 'lower' to 'higher' animals, such as humans. In the last decades, evolutionary biologists have tended to move from one extreme (i.e. the idea of scala naturae or the existence of a general evolutionary trend in complexity from 'lower' to "higher" taxa, with Homo sapiens as the end stage) to the other, opposite, extreme (i.e. to avoid using terms such as 'phylogenetically basal' and 'anatomically plesiomorphic' taxa, which are seen as the undesired vestige of old teleological theories). The latter view tries to avoid any possible connotations with the original anthropocentric idea of a scala naturae crowned by man and, in that sense, it can be regarded as a more politically correct view. In the past years and months there has been renewed interest in these topics, which have been discussed in various papers and monographs that tend to subscribe, in general, to the points defended in the more politically correct view. Importantly, most evolutionary and phylogenetic studies of tetrapods and other vertebrates, and therefore most discussions on the scala naturae and related issues have been based on hard tissue and, more recently, on molecular data. Here we provide the first discussion of these topics based on a comparative myological study of all the major vertebrate clades and of myological cladistic and Bayesian phylogenetic analyses of bony fish and tetrapods, including Primates. We specifically (i) contradict the notions of a scala naturae or evolutionary progressive trends leading to more complexity in 'higher' animals and culminating in Homo sapiens, and (ii) stress that the refutation of these old notions does not necessarily mean that one should not keep using the terms 'phylogenetically basal' and particularly 'anatomically plesiomorphic' to refer to groups such as the urodeles within the Tetrapoda, or the strepsirrhines and lemurs within the Primates, for instance. This review will contribute to improving our understanding of these broad evolutionary issues and of the evolution of the vertebrate Bauplans, and hopefully will stimulate future phylogenetic, evolutionary and developmental studies of these clades.

Specialize or risk disappearance - empirical evidence of anisomerism based on comparative and developmental studies of gnathostome head and limb musculature.

William K. Gregory was one of the most influential authors defending the existence of an evolutionary trend in vertebrates from a higher degree of polyisomerism (more polyisomeric or 'serial' anatomical structures arranged along any body axis) to cases of anisomerism (specialization or loss of at least some original polyisomeric structures). Anisomerism was the subject of much interest during the 19th and the beginning of the 20th centuries, particularly due to the influence of the Romantic German School and the notion of 'primitive archetype' and because it was conceptually linked to other crucial biological issues (e.g. complexity, scala naturae, progress, modularity or phenotypic integration). However, discussions on anisomerism and related issues (e.g. Williston's law) have been almost exclusively based on hard tissues. Here we provide the first detailed empirical test, and discussion, of anisomerism based on quantitative data obtained from phylogenetic and comparative analyses of the head and forelimb muscles of gnathostomes. Our results strongly support the existence of such a trend in both forelimb and head musculature. For instance, the last common ancestor (LCA) of extant tetrapods likely had 38 polyisomeric muscles (PMs) out of a total of 70 forelimb muscles (i.e. 54%), whereas in the LCAs of extant amniotes and of mammals these numbers were 38/73 (52%) and 21/67 (31%), and in humans are 11/59 (19%). Interestingly, the number of PMs that became specialized during the forelimb evolutionary transition from the LCA of extant tetrapods to humans (13) is very similar to the number of PMs that became lost (14), indicating that both specialization and loss contributed equally to the trend towards anisomerism. By contrast, during the evolution of the head musculature from the LCA of gnathostomes to humans a total of 27 PMs were lost whereas only one muscle became specialized. Importantly, the evolutionary trend towards anisomerism is not related to a general trend leading to the presence of fewer muscles in derived taxa, because for instance humans have more head muscles in total, but many less head polyisomeric muscles than early gnathostomes and extant fish such as sharks, and than early tetrapods and amphibians such as salamanders. This is because new muscles have also been acquired during gnathostome evolution (e.g. facial muscles of mammals). Interestingly, many new PMs have also been acquired during head evolution (but subsequently lost during the transitions towards humans), whereas only a few new PMs were acquired during forelimb evolution. Our comparisons and review of the literature indicate that there is also a trend towards anisomerism during development, thus providing a further example of a parallel between ontogeny and phylogeny, e.g. some forelimb PMs (e.g. contrahentes, intermetacarpales) become specialized or lost (re-absorbed) during human ontogeny and some head PMs (e.g. constrictores branchiales) become lost during salamander ontogeny. This review will inform future discussions on modularity, complexity, body plans, phenotypic integration and macroevolution, which should ideally include soft tissues and the use of new tools (e.g. anatomical networks) in order to provide a broader and more integrative understanding of these relevant subjects.

Cranial muscle development in frogs with different developmental modes: direct development versus biphasic development.

Normal development in anurans includes a free swimming larva that goes through metamorphosis to develop into the adult frog. We have investigated cranial muscle development and adult cranial muscle morphology in three different anuran species. Xenopus laevis is obligate aquatic throughout lifetime, Rana(Lithobates) pipiens has an aquatic larvae and a terrestrial adult form, and Eleutherodactylus coqui has direct developing juveniles that hatch from eggs deposited on leaves (terrestrial). The adult morphology shows hardly any differences between the investigated species. Cranial muscle development of E. coqui shows many similarities and only few differences to the development of Rana (Lithobates) and Xenopus. The differences are missing muscles of the branchial arches (which disappear during metamorphosis of biphasic anurans) and a few heterochronic changes. The development of the mandibular arch (adductor mandibulae) and hyoid arch (depressor mandibulae) muscles is similar to that observed in Xenopus and Rana (Lithobates), although the first appearance of these muscles displays a midmetamorphic pattern in E. coqui. We show that the mix of characters observed in E. coqui indicates that the larval stage is not completely lost even without a free swimming larval stage. Cryptic metamorphosis is the process in which morphological changes in the larva/embryo take place that are not as obvious as in normal metamorphosing anurans with a clear biphasic lifestyle. During cryptic metamorphosis, a normal adult frog develops, indicating that the majority of developmental mechanisms towards the functional adult cranial muscles are preserved.