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Evolution and Development of the Cartilaginous Skull: from a Lancelet

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Evolution and Development of the Cartilaginous Skull: from a Lancelet Seminars in Cell & Developmental Biology 91 (2019) 2–12 Contents lists available at ScienceDirect Seminars in Cell & Developmental Biology j ournal homepage: www.elsevier.com/locate/semcdb Review Evolution and development of the cartilaginous skull: From a lancelet towards a human face a,b a,b,∗ Marketa Kaucka , Igor Adameyko a Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden b Department of Molecular Neurosciences, Medical University Vienna, Vienna, Austria a r a t b i c s t l e i n f o r a c t Article history: Chrondrocranium, the cartilaginous skull, is one of the major innovations that underlie evolution of the Received 22 April 2017 vertebrate head. Control of the induction and shaping of the cartilage is a key for the formation of the Received in revised form facial bones and largely defines facial shape. The appearance of cartilage in the head enabled many new 27 November 2017 functions such as protection of central nervous system and sensory structures, support of the feeding Accepted 9 December 2017 apparatus and formation of muscle attachment points ensuring faster and coordinated jaw movements. Available online 14 December 2017 Here we review the evolution of cartilage in the cranial region and discuss shaping of the chondrocranium in different groups of vertebrates. Keywords: Chondrocranium © 2017 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license Evolution (http://creativecommons.org/licenses/by/4.0/). Embryonic development Cartilage function in the head Invertebrate cartilage Cartilage in chordates Facial shape Protection of central nervous system Support of feeding apparatus Face Cartilage Cranial evolution Contents 1. General role of cartilage during the evolution of the head . 2 2. Cartilages in invertebrates: support for the feeding apparatus and protection of the nervous system . 3 3. Evolution of the chondrocranium in chordates: amphioxus – cartilage of the feeding apparatus . 4 4. Chondrocranium in extant and extinct agnathans . 5 5. Evolution of chondrocranium in gnathostomes . 6 6. Chondrocrania in amphibians and beyond . 8 7. Conclusion . 10 Acknowledgements. .10 References . 10 1. General role of cartilage during the evolution of the head the head is a highly composite compartment, and includes many The head represents the most complex part of the vertebrate tissue types assembled together during morphogenesis, the pre- body. Despite enduring efforts to cast light on the evolutionary cise sequence of evolutionary transitions, innovations, and tissue origins of the head, unambiguous answers remain elusive. Since coordination events are at the core of cranial evolution and its understanding. In animals that possess a cartilaginous skeleton only, cartilage plays a major supporting role for the pharynx, ∗ muscles, and other organs in the body. During evolution, cranial Corresponding author. E-mail address: [email protected] (I. Adameyko). cartilage began to protect the central nervous system (CNS) and https://doi.org/10.1016/j.semcdb.2017.12.007 1084-9521/© 2017 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). M. Kaucka, I. Adameyko / Seminars in Cell & Developmental Biology 91 (2019) 2–12 3 Fig. 1. Major advancements during the incremental evolution of the chondrocranium. (A) Gain of multiple functions during the evolution of the cranial/head cartilage. (B) Evolutionary and developmental trends shaping the gnathostome neurocranium. sensory organs from displacement or damage. During the devel- serves as a load-bearing physical integrator of multiple tissues, and opment of vertebrates, cartilage played a leading role in facial as a protective building block of the evolving head. Despite the large outgrowth and shaping [1,2]. Other developmental functions of car- diversity of “stiff” matrix tissue types in different animal groups [9], tilage account for the programmable placement, expansion, and its evolutionary purpose looks similar - the protection of sensitive shaping of bones in the process of endochondral ossification [3–5]. nervous tissues, stabilization of the feeding apparatus, and a scaf- Chordates first acquired and developed the head compartment fold for muscle attachment, enabling faster and more coordinated during the Cambrian explosion, a major evolutionary event related locomotion. to the origin and diversification of body plans in animal phyla Gans and Northcutt proposed a hypothesis for the develop- [6]. Starting from a simple filter-feeding lifestyle, chordates ben- mental origin of the vertebrate head as a new body unit [10]. eficiated to becoming rather active predators and changed their This hypothesis established the cranial neural crest, placodes, and body size [7]. In line with the shift from passive to active preda- other integrating tissues as the evolutionary substrates and power- tory lifestyle, a stiffened feeding apparatus became an indisputable ful propellants for further cranial evolution, resulting in increased advantage for food acquisition and survival. Thus, one of the driving complexity. Cartilage, being derived from both the neural crest forces behind the evolution of the chondrocranium is likely to be and mesoderm [11], played a key role in these processes, and is optimization and strengthening of the oral apparatus, which sub- inevitably linked to the origin of the vertebrate head and the for- sequently led to the acquisition of articulated jaws before/around mation of articulated jaws. the early Devonian [8]. It is worth mentioning that diverse cellu- lar and acellular cranial cartilage elements are well represented in 2. Cartilages in invertebrates: support for the feeding cyclostomes lacking articulated jaws. It seems that one of the most apparatus and protection of the nervous system important evolutionary directions is represented by the variations in mechanisms driving the shaping and scaling of cartilage. The Cartilaginous tissue is not an exclusive prerogative of chor- acquisition of jaws, as well as other morpho-functional innovations, dates. Many distant groups of invertebrates developed a specialized could stimulate the development of further complex geometrical connective tissue that is morphologically, histologically, and features, rather than generating additional types of cartilage with molecularly similar to the classical vertebrate cartilage (see Fig. 1A) different histological properties. [12]. However, it is unknown whether these cartilage-like connec- Species with an active feeding mode also underwent an exten- tive tissues evolved independently, or have been inherited from the sive centralisation and further enlargement of the nervous tissue. common ancestor. Furthermore, they established an optimal niche for the evolution For instance, annelid worms (Sabellid polychaetes) develop long and engagement of sensory organs and motor relays. Such devel- feeding tentacles that are reinforced by internal cartilaginous tis- opment of sensory organs, oral apparatuses, and CNS integration sue [12,13]. Similarly, brachiopod feeding tentacles possess a tissue led to an increase in the complexity of the chondrocranium, which similar to cartilage in terms of its extracellular matrix, which 4 M. Kaucka, I. Adameyko / Seminars in Cell & Developmental Biology 91 (2019) 2–12 includes collagen, acidic mucopolysaccharides, elastin, chondroitin cords [17]. Despite recent progress in the field, it remains unknown sulphate, and keratan sulphate [12]. The proboscis and gills whether cartilage evolved once or several times independently, of enteropneust hemichordates are supported by a tissue that and which cell or tissue types developed this innovative program strongly resembles acellular cartilage, and contains collagen [14]. or co-opted the gene regulatory network responsible for matrix Molluscs also demonstrate the presence of cartilage in multi- secretion. ple locations. For instance, gastropod snails possess a cartilaginous In summary, there are interesting general trends that direct the odontophore supporting the radula, their main feeding organ placement and function of cartilage, even in very distant inverte- [12,15]. Cephalopod molluscs have an internal skeleton that is par- brate groups: protection of the CNS (cephalopods and horseshoe tially represented by the remnants of the shell, but also composed crab), and support of the feeding apparatus (marine polychaetae of numerous separated cellular cartilaginous elements, including worms, brachiopods, hemichordates, and molluscs). Both of these cranial cartilage protecting the brain, pallial and funnel cartilage, initial functions support the idea that the first cartilaginous tissue nuchal and dorsal cartilage, diaphragm and branchial cartilage, as evolved in the head or anterior compartment of a common bilat- well as cartilage supporting the fin [16]. eralian ancestor. However, later, these purposes converged during When it comes to molecular deep homology, the recent evi- the evolution of the chondrocranium in chordates. dence gathered from distant invertebrate species, the horseshoe crab (Limulus polyphemus, Arthropoda) and cuttlefish (Sepia ban- densis, Mollusca), suggests that the evolution of the chondrogenic 3. Evolution of the chondrocranium in chordates: gene regulatory network might have already started in the common amphioxus – cartilage of the feeding apparatus ancestor of Bilateria [17]. The horseshoe crab, known as a living fossil,
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