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New Twists on the Ancient Body of Craniatesଝ Zoology 117 (2014) 1–6 Contents lists available at ScienceDirect Zoology journa l homepage: www.elsevier.com/locate/zool Axial systems and their actuation: new twists on the ancient body of craniatesଝ a b,∗ Nadja Schilling , John H. Long Jr. a Institute of Systematic Zoology and Evolutionary Biology, Friedrich-Schiller-University Jena, Erbertstr. 1, 07743 Jena, Germany b Department of Biology, Vassar College, Box 513, Poughkeepsie, NY 12603, USA a r t a b i s c l e i n f o t r a c t Article history: Craniate animals – vertebrates and their jawless sister taxa – have evolved a body axis with powerful Received 23 November 2013 muscles, a distributed nervous system to control those muscles, and an endoskeleton that starts at the Accepted 26 November 2013 head and ends at the caudal fin. The body axis undulates, bends, twists, or holds firm, depending on Available online 12 December 2013 the behavior. In this introduction to the special issue on axial systems and their actuation, we provide an overview of the latest research on how the body axis functions, develops, and evolves. Based on Keywords: this research, we hypothesize that the body axis of craniates has three primary, post-cranial modules: Evolution precaudal, caudal, and tail. The term “module” means a portion of the body axis that functions, develops, Development and evolves in relative independence from other modules; “relative independence” means that structures Axial system and processes within a module are more tightly correlated in function, development, and behavior than Motor control Modularity the same processes are among modules. © 2013 Elsevier GmbH. All rights reserved. 1. Introduction tissue growth are sensitive to feedback over an individual’s life span. When we study the development of a part or region of the Animals locomote by changing shape. They flutter fins, bend body axis, we tease apart genetic and environmental components, legs, and flap wings. Those appendicular motions transfer momen- find homologous building processes among disparate species, and tum from the body to the water, ground, or air. While propulsive understand the constraints that limit morphological possibilities. work is done by appendages, those fins and limbs are attached to While it’s obvious that behavior and development evolve over a body axis, which, in most craniates, augments or supersedes the generational time (Fig. 1C), it’s worth stating that evolutionary work of the appendicular system by undulating, bending, twisting, processes, like behavior and development, also involve feedback or providing a firm base. When one considers that the body axis with the world. Thus behavior, development, and evolution are all evolved before the appendages (Janvier, 1996), then it becomes different scales in a dynamical system. Moreover, this dynamical clear that to understand appendages and craniates we need a more perspective highlights the fact that to understand the function of integrated understanding of the body axis, its function, develop- the body axis, it must be studied in the context of the whole system ment, and evolution. To contribute to that understanding is the (Fig. 2). This requirement presents a methodological challenge to goal of this special issue. biologists, who often dissect, isolate, and reduce in order to observe Locomotion figures centrally in our work because of the primacy phenomena, measure properties, and test hypotheses. In this intro- of movement in behavior. To understand the behavior of craniates duction to this special issue, we’ll explore how these challenges can we must understand how animals operate as part of the dynamical be addressed. system that couples the animal and its world in an on-going phys- ical interaction (Fig. 1A). Physics rules these interactions. Animals and their environments exchange momentum and energy, and both 2. Approaches move in response (Fig. 1B). Another type of interaction between the animal and its world A traditional way to study the body axis of vertebrates is to occurs during development, when patterns of gene expression and examine the skeleton in isolation. For example, when we exam- ine just the bones of the blue marlin, Makaira nigricans, we can see how the skeletal framework of this large, predatory fish is domi- ଝ nated, in terms of number of elements and their coverage, by the This article is part of a special issue entitled “Axial systems and their actuation: bones of the body axis, the vertebral column, the ribs, and the skele- new twists on the ancient body of craniates”. ∗ tal elements of the median fins (Fig. 3). But what does this view tell Corresponding author. Tel.: +1 8454377305. E-mail address: [email protected] (J.H. Long Jr.). us about the marlin as a dynamical system? Very little, since the 0944-2006/$ – see front matter © 2013 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.zool.2013.11.002 2 N. Schilling, J.H. Long Jr. / Zoology 117 (2014) 1–6 Fig. 1. Animals operate as dynamical systems. (A) A dynamical systems analysis explicitly contains the animal, the physical world, and the unfolding temporal history of their interactions. (B) Animals locomote by transferring the momentum of their body reconfigurations to the world via Newton’s third law. Momentum flux is evident in the wake that a swimming marine iguana, Amblyrhynchus cristatus, creates. This image was taken on Isla Fernandina, Galapagos. (C) Functional analysis occurs on the three time scales of biological dynamical systems: (i) behavior, (ii) development, and (iii) evolution. skeleton in this snapshot is removed from the physical context in marlin (Hebrank et al., 1990), they measured morphological vari- which it operates. ation in the size and orientation of those structures within and In contrast, when we examine the axial skeleton as part of a among species. Combining high-speed video and measurements whole, behaving animal, we are able to understand how its func- of the ground reaction force of the jump to measure momentum tion depends on its physical context. For example, while fish swim flux, they placed the skeleton back into its dynamical system. Their in water, some species, without any obvious external morpho- preliminary experiments show that the morphology of the axial logical adaptations, jump on land (Gibb et al., 2011). Ashley-Ross skeleton alone predicts neither the flexural stiffness of the intact and colleagues (2014) wonder if the adaptations are on the inside. body nor the jumping performance of the individual. Taking advantage of differences in jumping performance among While some changes in body shape during swimming can be species of teleost fishes, they posited that good terrestrial jumpers predicted from the morphology of the body and the vertebral ought to have superior elastic energy storage compared to poor ter- column (Porter et al., 2009), the vertebral column’s mechanical restrial jumpers. Considering the mechanical contribution of the function is best understood by first directly measuring the move- expanded neural and hemal spines of the vertebrae of the blue ment of the skeleton during a particular behavior. To do this in N. Schilling, J.H. Long Jr. / Zoology 117 (2014) 1–6 3 Fig. 4. The axial musculature of a bowfin, Amia calva. Skin and muscles in the precau- dal and caudal (post-anal) regions have been removed to show the curved surfaces of the deep myomeric muscles. Darker, superficial muscle can be seen between the white myoseptal connective tissue that attaches to the skin. The shape of the muscle and its position within the context of the body is insufficient to understand how the body axis would operate in life. function of axial skeletons in any craniate species. We endorse it wholeheartedly. In addition to the axial skeleton, the muscles that power the reconfigurations of the body can be the focus of study. Investi- gations of gross anatomy can reveal the complexities of muscle geometry and their tendinous connections to skin and skeleton (Fig. 4). Such work, at its best, uses morphology to create plausible Fig. 2. Axial, cranial, and appendicular systems co-operate, as seen here during the mechanical hypotheses (e.g., Westneat et al., 1993; Gemballa et al., courtship display of the blue-footed booby, Sula nebouxii. 2006). What morphology alone misses, however, is the behavioral This image was taken on Isla Espanola,˜ Galapagos. complexity that can result from a single system able to alter its propulsive reconfigurations. One such system is the axially driven escape response, which is swimming sharks, Porter and colleagues (2014) implanted sonomi- a fundamental and widely conserved behavior in vertebrates (Hale crometry crystals, which use ultrasound to measure inter-crystal et al., 2002). The pattern of muscle activity that allows fishes to distance, in vertebrae. To their surprise, they found that not only create high-amplitude, “C”-shaped axial body movements, a so- did the intervertebral joints bend, but so did the vertebral centra. called “C-start,” is initiated by the reticulospinal neural circuit that They confirmed the result by testing isolated sections of vertebral includes the Mauthner system, which was originally thought to columns, instrumented with crystals, in a bending machine. Thus, produce inflexible and stereotyped responses (Eaton et al., 2001). at least in cartilaginous fishes, the whole vertebral column – the But as Liu and Hale (2014) show, the shape of the bending body connective tissues of the intervertebral joints and the calcified car- is variable within and among species. By reference to the litera- tilage of the vertebrae – appears to be operating as a spring during ture and through their new experiments on zebra fish (Danio rerio) swimming. they draw the critical conclusion that the escape neural circuit is However, the spring-like functioning of the axial skeleton of involved in more than a single behavior. Even if one considers only fishes is far from universal.
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