What’s in a Head? Comparative Morphology of Head Muscles in the Three Drusinae Clades (Insecta: Trichoptera)

The subfamily Drusinae (Limnephilidae, Trichoptera) comprises a range of species exhibiting differently shaped head capsules in their larval stages. These correspond to evolutionary lineages pursuing different larval feeding ecologies, each of which uses a different hydraulic niche: scraping grazers and omnivorous shredders sharing rounded head capsules and filtering carnivores with indented and corrugated head capsules. In this study, we assess whether changes in head capsule morphology are reflected by changes in internal anatomy of Drusinae heads. To this end, internal and external head morphology was visualized using µCT methods and histological sections in three Drusinae species – Drusus bosnicus, D. franzi and D. discolor – representing the three evolutionary lineages. Our results indicate that Drusinae head musculature is highly conserved across the evolutionary lineages with only minute changes between taxa. Conversely, the tentorium is reduced in D. discolor, the species with the most aberrant head capsule investigated here. Integrating previous research on Drusinae head anatomy, we propose a fundamental Drusinae blueprint comprising 29 cephalic muscles and discuss significance of larval head capsule corrugation in Trichoptera.

Evolution of the vertebrate head is revealed by the rosette mesoderm

The vertebrate head comprises characteristic combinations of the cranium, brain, cranial nerves and head muscles. However, there have long been arguments about the developmental and evolutionary origins and the possible segmental nature of the head muscles, particularly those anterior to the otic vesicle. In gnathostomes, the presence of pre-otic segments (trunk somite homologs) has been denied by anti-segmentalists, but championed by segmentalists, who have focused on marginally detectable somitomeres or on more obvious head cavities. This metameric ideology has generated various definitions of segments, causing great controversy1,2, and the evaluation of such arguments has been impeded by the relative paucity of relevant work on the head mesoderm of cyclostomes (hagfishes and lampreys). Here, we demonstrate the presence of rosettes (which are reminiscent of somites) in the head mesoderm of lamprey (Lethenteron camtschaticum) embryos using confocal laser scanning and transmission electron microscopy. These transient rosettes, which were not segmented by acellular fissures and were genetically distinct from trunk somites, emerged several times during character individualization of the head muscles. This specialty of the rosette dynamics suggests that the lamprey head mesoderm evolved de novo, rather than from somites, and molecular comparison among deuterostomes supported this perspective.

Developmental fates of shark head cavities reveal mesodermal contributions to tendon progenitor cells in extraocular muscles

Vertebrate extraocular muscles (EOMs) function in eye movements. The EOMs of modern jawed vertebrates consist primarily of four recti and two oblique muscles innervated by three cranial nerves. The developmental mechanisms underlying the establishment of this complex and the evolutionarily conserved pattern of EOMs are unknown. Chondrichthyan early embryos develop three pairs of overt epithelial coeloms called head cavities (HCs) in the head mesoderm, and each HC is believed to differentiate into a discrete subset of EOMs. However, no direct evidence of these cell fates has been provided due to the technical difficulty of lineage tracing experiments in chondrichthyans. Here, we set up an in ovo manipulation system for embryos of the cloudy catshark Scyliorhinus torazame and labeled the epithelial cells of each HC with lipophilic fluorescent dyes. This experimental system allowed us to trace the cell lineage of EOMs with the highest degree of detail and reproducibility to date. We confirmed that the HCs are indeed primordia of EOMs but showed that the morphological pattern of shark EOMs is not solely dependent on the early pattern of the head mesoderm, which transiently appears as tripartite HCs along the simple anteroposterior axis. Moreover, we found that one of the HCs gives rise to tendon progenitor cells of the EOMs, which is an exceptional condition in our previous understanding of head muscles; the tendons associated with head muscles have generally been supposed to be derived from cranial neural crest (CNC) cells, another source of vertebrate head mesenchyme. Based on interspecies comparisons, the developmental environment is suggested to be significantly different between the two ends of the rectus muscles, and this difference is suggested to be evolutionarily conserved in jawed vertebrates. We propose that the mesenchymal interface (head mesoderm vs CNC) in the environment of developing EOM is required to determine the processes of the proximodistal axis of rectus components of EOMs.

The CXCR4/SDF-1 Axis in the Development of Facial Expression and Non-somitic Neck Muscles

Trunk and head muscles originate from distinct embryonic regions: while the trunk muscles derive from the paraxial mesoderm that becomes segmented into somites, the majority of head muscles develops from the unsegmented cranial paraxial mesoderm. Differences in the molecular control of trunk versus head and neck muscles have been discovered about 25 years ago; interestingly, differences in satellite cell subpopulations were also described more recently. Specifically, the satellite cells of the facial expression muscles share properties with heart muscle. In adult vertebrates, neck muscles span the transition zone between head and trunk. Mastication and facial expression muscles derive from the mesodermal progenitor cells that are located in the first and second branchial arches, respectively. The cucullaris muscle (non-somitic neck muscle) originates from the posterior-most branchial arches. Like other subclasses within the chemokines and chemokine receptors, CXCR4 and SDF-1 play essential roles in the migration of cells within a number of various tissues during development. CXCR4 as receptor together with its ligand SDF-1 have mainly been described to regulate the migration of the trunk muscle progenitor cells. This review first underlines our recent understanding of the development of the facial expression (second arch-derived) muscles, focusing on new insights into the migration event and how this embryonic process is different from the development of mastication (first arch-derived) muscles. Other muscles associated with the head, such as non-somitic neck muscles derived from muscle progenitor cells located in the posterior branchial arches, are also in the focus of this review. Implications on human muscle dystrophies affecting the muscles of face and neck are also discussed.

Inside the head of a cybertype – three-dimensional reconstruction of the head muscles of Ommatoiulus avatar (Diplopoda: Juliformia: Julidae) reveals insights into the feeding movements of Juliformia

The origin and diversification of the arthropod head is one of the major topics in the field of evolutionary morphology of Arthropoda. Among the major arthropod groups, Myriapoda and, more precisely Diplopoda, are generally poorly studied regarding their head anatomy. However, this group is of pivotal importance to understand the evolutionary functional morphology of the arthropod head. In this study, we investigate the complete musculoskeletal system of the diplopod head with a detailed description of the cephalic anatomy of the recently described species Ommatoiulus avatar. The comparison of our data with the literature on the few other species available show that the morphology of the musculoskeletal system within Juliformia, a subgroup of the Diplopoda, is relatively conservative. Using video recordings of the feeding movements in addition to the anatomical data, we revise the mechanism of the mandibular movements in Juliformia. There was a controversy whether mandibular abduction is an active process, facilitated by contraction of an abductor muscle, or if it is a passive process, mediated by tentorial and gnathochilarial movements not involving a direct abduction by muscular contraction. We show that mandibular abduction in Ommatoiulus is an active movement involving the contraction of an abductor muscle. This is similar to the mandibular abduction in other arthropod groups.

Transformation of internal head structures during the metamorphosis of Chrysopa pallens (Neuroptera: Chrysopidae)

Background The metamorphosis is a complicated but very interesting process because of the highly dynamic transformation in sheath. Very few studies had coverage on the head muscles of larvae, pupae, and adults. Most of these studies were focusing on the model organisms about the rough changes of the external and internal tissues or the time of metamorphosis based on the traditional methods. In our study,the skeleto-muscular system of head, as well as the brain of Chrysopa pallens (Rambur, 1838) from larvae to adults are described in detail for the first time by the technology of micro computed tomography (µ-CT). The transformations of these systems during pupal stage are studied for the first time.Results The morphological differences and functional adaptations between the stages are assessed. Muscles are distinctly slender in larvae than in adults with a significantly larger quantity. A larger brain with improved sensory perception is suggested to be essential for dispersal, mating and flying for adults. For the pupae, the results show that the histolysis of the muscles happens in first third of the pupal period and their reconstruction happens in the following days. The brain exists all along.Conclusion We suggest the transformations of the skeleton occur earlier than the musculature. Most of the transformations are related to tasks they play in the developmental stages.