Janine M. Ziermann

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.

Cranial Muscle Development in the Model Organism Ambystoma mexicanum: Implications for Tetrapod and Vertebrate Comparative and Evolutionary Morphology and Notes on Ontogeny and Phylogeny

There is still confusion about the homology of several cranial muscles in salamanders with those of other vertebrates. This is true, in part, because of the fact that many muscles present in early ontogeny of amphibians disappear during development and specifically during metamorphosis. Resolving this confusion is important for the understanding of the comparative and evolutionary morphology of vertebrates and tetrapods because amphibians are the phylogenetically most plesiomorphic tetrapods, concerning for example their myology, and include two often used model organisms, Xenopus laevis (anuran) and Ambystoma mexicanum (urodele). Here we provide the first detailed report of the cranial muscle development in axolotl from early ontogenetic stages to the adult stage. We describe different and complementary types of general muscle morphogenetic gradients in the head: from anterior to posterior, from lateral to medial, and from origin to insertion. Furthermore, even during the development of neotenic salamanders such as axolotls, various larval muscles become indistinct, contradicting the commonly accepted view that during ontogeny the tendency is mostly toward the differentiation of muscles. We provide an updated comparison between these muscles and the muscles of other vertebrates, a discussion of the homologies and evolution, and show that the order in which the muscles appear during axolotl ontogeny is in general similar to their appearance in phylogeny (e.g. differentiation of adductor mandibulae muscles from one anlage to four muscles), with only a few remarkable exceptions, as for example the dilatator laryngis that appears evolutionary later but in the development before the intermandibularis. Anat Rec, 296:1031–1048, 2013.

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. J. Morphol. 275:398–413, 2014.

Muscles of Chondrichthyan Paired Appendages: Comparison With Osteichthyans, Deconstruction of the Fore–Hindlimb Serial Homology Dogma, and New Insights on the Evolution of the Vertebrate Neck

Here we present the first study comparing all the paired appendages muscles of representatives of each major extant gnathostome group. We address a crucial and enigmatic question in evolutionary and comparative anatomy: Why are the pelvic and pectoral appendages of gnathostomes, and particularly of tetrapods, in general so similar to each other? We argue that an integrative analysis of the new myological data and the information from the literature contradicts the idea that the forelimbs and hindlimbs are serial homologues. The data show that many of the strikingly similar fore‐ and hindlimb muscles of extant tetrapods evolved independently in each appendage because the ancestors of extant gnathostomes and osteichthyans only had an adductor and an abductor in each fin. Therefore, these data contradict the idea that at least some muscles present in the tetrapod fore‐ and hindlimbs were already present in some form in the first fishes with pectoral and pelvic appendages, as the result of an ancestral duplication of the paired appendages leading to a true serial homology. The origin of the pectoral girdle was instead likely related to head evolution, as illustrated by the cucullaris of gnathostomes such as chondrichthyans inserting onto both the branchial arches and pectoral girdle. Only later in evolution the cucullaris became differentiated into the levatores arcuum branchialium and protractor pectoralis, which gave rise to the amniote neck muscles trapezius and sternocleidomastoideus. These changes therefore contributed to an evolutionary trend toward a greater anatomical and functional independence of the pectoral girdle from head movements. Anat Rec, 298:513–530, 2015.

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.

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 Beers “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.

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.

Anatomical Analysis of Thumb Opponency Movement in the Capuchin Monkey (Sapajus sp)

Capuchin monkeys present a wide variety of manipulatory skills and make routine use of tools both in captivity and in the wild. Efficient handling of objects in this genus has led several investigators to assume near-human thumb movements despite the lack of anatomical studies. Here we perform an anatomical analysis of muscles and bones in the capuchin hand. Trapezo-metacarpal joint surfaces observed in capuchins indicate that medial rotation of metacarpal I is either absent or very limited. Overall, bone structural arrangement and thumb position relative to the other digits and the hand’s palm suggest that capuchins are unable to perform any kind of thumb opponency, but rather a ‘lateral pinch’ movement. Although the capuchin hand apparatus bears other features necessary for complex tool use, the lack thumb opposition movements suggests that a developed cognitive and motor nervous system may be even more important for high manipulatory skills than traditionally held.

Analyzing developmental sequences with Parsimov—A case study of cranial muscle development in anuran larvae

Parsimov is a parsimony-based method for identifying the minimum number of heterochronic event-shifts on all branches of a given phylogenetic framework to explain the developmental sequences seen in the species investigated, and has been used to investigate the evolution of developmental sequences in various animal groups. However, the biological interpretation of the results is difficult not least because Parsimov uses non-independent data resulting from event-pairing as the basis for its analyses. To test the applicability of Parsimov to a large data set, larval cranial muscle development was studied in 15 anurans, three caudates and the Australian lungfish. We analyzed the developmental sequences with Parsimov to investigate: if there are (1) heterochronies on deep branches of a cladogram indicating changes in the ancestral sequences, (2) heterochronies that can be related to larval life-history, and (3) the sensitivity of the analysis to different underlying cladograms. We discovered general patterns of cranial muscle development, such as an anterior-to-posterior gradient, an outside-in pattern and a tendency for cranial muscles to develop from their region of origin toward their insertion. We found most heterochronies on terminal branches and only a few shifts on deep branches in the cladograms indicating changes in the ancestral sequences. No changes could be related to larval life-history. The underlying cladogram clearly influenced the outcome of the analysis. We propose that Parsimov has the potential, combined with other methods, to find evolutionary important changes and to aid the biological interpretation of these changes.

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. Willistons 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.