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.

Institute of Systematic Zoology and Evolutionary Biology, Friedrich-Schiller-University Jena, Erbertstr. 1, 07743 Jena, Germany

Department of Biology, Vassar College, Box 513, Poughkeepsie, NY 12603, USA

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.

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

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. Nowroozi and Brainerd (2013) devel-

escapes, Liu and Hale point out a variety of escape behaviors: C-

oped an X-ray technique that allowed them to carefully measure

start, S-start, and withdrawal. Moreover, the Mauthner system may

the motion of intervertebral joints in the bony striped bass, Morone

be involved in post-feeding turns and predatory strikes. Their con-

saxatilis. Even during the large-amplitude body reconﬁgurations

ceptual framework for understanding how neural patterns interact

of a startle response, striped bass never bend their vertebral col-

with body morphology to produce a system with behavioral ﬂexi-

umn beyond the low-stiffness neutral zone. Thus the vertebral

bility and evolutionary potential yields new insights into how axial

column, at least in this species, never functions as an elastic spring

systems are actuated.

(Nowroozi and Brainerd, 2014). With functional multiplicity in

From the dynamical systems perspective, the actuation of the

mind, they propose an important conceptual framework for addi-

body axis must involve the neural system acting in concert and

tional experiments, across a broad diversity of species, by pairing

coordination with the mechanical behavior of the body as it

mechanical tests and axial kinematics. Their framework is general

exchanges momentum with the environment. This is not the usual

enough to provide important guidance for the investigation of the

way to think of neural or motor control, and the ﬁeld of neurome-

chanics has developed to recognize the complexities of integrated

actuation systems (Nishikawa et al., 2007). One tantalizing hypoth-

esis for the actuation of the body axis is mechanical resonance,

which might, under the right circumstances, allow a ﬁsh to mini-

mize the energy cost of swimming (Tytell et al., 2014). But Tytell and

colleagues point out that the water in which ﬁsh swim will likely

dampen resonance. To determine under what conditions resonance

might be present, Tytell and colleagues created a force-coupled

digital simulation of a swimming lamprey. Depending on the test

conditions, they found that the body axis bends in a complex

way, with multiple modes of bending; resonance, when present,

Fig. 3. Skeletal anatomy of the blue marlin, Makaira nigricans. Marlin, like most bony

occurred at cycle frequencies that do not necessarily correspond

ﬁsh, have a skeletal system that is dominated, in terms of coverage and number of

to the most efﬁcient swimming conditions. Further doubt is cast

elements, by the axial skeleton: vertebral column, ribs, caudal ﬁn, dorsal and anal

ﬁns. upon the importance of mechanical resonance by the inability of a

Illustration by Rosemary Calvert (courtesy of Stephen Wainwright). closed loop neuromuscular preparation of a real lamprey to entrain

4 N. Schilling, J.H. Long Jr. / Zoology 117 (2014) 1–6

to system resonance under most circumstances. All told, the actu- hagﬁshes. Long seen as either the sister taxon to Vertebrata or

ation of the body axis in water is unlikely to be a simple matter of to the other living jawless clade, Petromyzontiformes, myxiniform

mechanical resonance and neural entrainment. species lack bone but have endoskeletal cranial and pharyngeal ele-

The ﬂexible actuation of the body axis is on display as salaman- ments made of cartilage. In terms of an axial skeleton, the Atlantic

ders transition from moving in water to moving on land. While hagﬁsh, Myxine glutinosa, was reported by multiple sources to have

salamanders use their limbs for propulsion, limb motion is aug- no cartilaginous elements, only the ancestral notochord. But the

mented by the reconfigurations of the body axis and by flexible same cannot be said of the inshore hagfish, Eptatretus burgeri. By

neural circuitry (Ashley-Ross and Lauder, 1997). As Cabelguen and imaging the scleratomal cells of embryos, Ota and colleagues (2013)

colleagues (2014) discuss, salamanders react to the change in phys- reported that ventral vertebral elements could be found in the

ical feedback from different environments to alter the pattern and caudal region of E. burgeri. Further gene expression analysis (Ota

magnitude of muscle activation. Central pattern generators (CPGs), et al., 2014) bolsters that ﬁnding. The fact that these hemal arch

auto-rhythmic clusters of cells distributed axially throughout the cartilages are found only in the caudal region clearly supports the

spinal cord, drive alternate contractions of the axial musculature. precaudal–caudal modularity hypothesis.

The combined behavior of the axial CPGs, and hence the axial mus- From a purely functional standpoint, the caudal module is front

cles, adjusts to changes in the slipperiness of a surface or the need to and center in aquatic locomotion of the type described by Webb

make a turn. These adjustments reveal what appear to be two axial (1984) as body-caudal-ﬁn (BCF) swimming. In contrast to the

modules, one for the trunk and one for the tail. All told, the authors median-paired-ﬁn (MPF) mode, BCF swimming involves undula-

hypothesize that salamanders are able to operate as dynamical sys- tions of the body axis, traveling waves of bending that increase

tems by virtue of combining their two functionally independent in lateral amplitude and midline curvature as they propagate to

axial modules with a third set of CPG-driven modules that control the tail (Long et al., 2010). Focusing on the locomotor function of

the motion of the limbs. the caudal region of the body axis, Root and Liew (2014) sought

Functional modularity is also a central feature in understanding to test the hypothesis that the ﬂexural stiffness of the body axis

how the axial system develops. The number of vertebrae in each would increase in a population of ﬁsh-like robots under selection

axial region of a mammal shows remarkably little variation across for enhanced predation. With the dynamical systems approach in

the clade. The numbers of cervical, thoracolumbar, and sacral verte- mind (see Fig. 1), they created a physics-based digital simulation

brae are ﬁxed, or nearly so, at 7, 19, and 3, respectively (Müller of the autonomous robots that coupled the forces generated by the

et al., 2010). This mammalian invariance is unique in vertebrates, undulating body and the forces generated by the surrounding ﬂuid.

and Buchholtz (2014) offers an explanation that integrates informa- Individuals with the best predatory performance had a stiffer body

tion from fossils, locomotor function, and development. Mammals axis and faster tailbeat frequency. Increases in the body’s ﬂexural

are unique in possessing a muscular diaphragm, an organ that stiffness occurred in a punctuated manner, with the change in a sin-

enhances ventilation of the lungs and partitions the thoracic and gle generation accounting for most of the change. Over hundreds of

lumbar regions. The cells for the diaphragm’s muscle migrate, early different trials, a range of ﬂexural stiffnesses was associated with

in development, from the cervical region C3–C5. Buchholtz con- the highest ﬁtnesses. It appears that different behavioral strategies

tends that the C3–C5 area is a developmental module, a region of – stiff-bodied fast swimming on the one hand or ﬂexible-bodied

distinct and independent operation, separate from the surrounding maneuvering on the other – are equally successful in different sit-

cervical segments. She applies similar logic to identify a devel- uations. In either case, it is clear that when predatory behavior is

opmental module in the lumbar region linked to the lack of ribs. under selection, the stiffness of the caudal module is a locomotor

Without ribs, the body axis in the lumbar region has a greater range adaptation.

of motion in the sagittal plane, and that motion can be coupled with Locomotor adaptation may also explain the developmental and

limb movements to increase stride length or maneuverability. The functional modularity within the tail of ﬁshes. The tail of both

trade-off for these respiratory and locomotor adaptations, argues sharks and ray-ﬁnned ﬁshes is modular in the sense that, com-

Buchholtz, is that while the developmental modules permit these pared to the rest of the body axis, it has its own developmental

unique regionalized functions they also constrain variation – and mechanisms, is anatomically distinct, is under separate neuro-

the selection that variation enables – on the number of vertebrae muscular control, and is a distinct target of selection (Flammang,

in mammals. 2014). Moreover, Flammang argues that the incredible diversity of

In contrast to the constraints seen in mammals, the number of tail form and function – and the behavioral complexity that the

vertebrae varies dramatically among the other jawed craniates. A tail underwrites – is linked to the species richness and ecologi-

chordate synapomorphy is a muscular post-anal tail used in loco- cal range of ray-ﬁnned ﬁshes in particular. The ability to precisely

motion (Stach, 2008). Thus the position of the anus demarcates control and adjust the stiffness and shape of the tail allows species

the two fundamental anatomical modules of the craniate body such as bluegill sunﬁsh, Lepomis macrochirus, to move, brake, and

axis: precaudal and caudal. From the literature and specimens, maneuver with precision (Flammang and Lauder, 2009). Precise

Ward and Mehta (2014) collected information on the numbers movements may have evolved in ray-ﬁnned ﬁshes in concert with

of precaudal and caudal vertebrae from over 1400 species. They the evolution of stony corals and the complex three-dimensional

regressed the number of caudal vertebrae onto the number of pre- habitats that they create.

caudal vertebrae. In chondrichthyan and actinopterygian ﬁshes,

when the overall number of vertebrae increases, the number of

caudal vertebrae increases faster than the number of precaudal 3. The modular body axis of craniates

vertebrae. They found the opposite trend in Sarcopterygii, the taxon

that includes tetrapods. That difference is correlated with the pri- Based on the research presented in this special issue, we hypoth-

marily terrestrial selection pressures in the tetrapods. Combined esize that the body axis of craniates has three primary, post-cranial

with the ﬁndings about precaudal developmental modules in mam- modules (Fig. 5). To be clear, the term “module” has the gen-

mals (Buchholtz, 2014), it is tempting to think of the precaudal and eral meaning of relative independence from other modules of

caudal modules of the body axis as the foci of selection for enhanced the system. By “relative independence,” we mean that structures

terrestrial and aquatic locomotion, respectively. and processes within a module are more tightly correlated than

The hypothesis for the modularity of the caudal and precau- structures and processes among modules. For example, the devel-

dal regions is supported by developmental work on the jawless opmental processes that appear to govern precaudal vertebral

N. Schilling, J.H. Long Jr. / Zoology 117 (2014) 1–6 5

Fig. 5. The body axis of craniates has three primary, post-cranial modules. As shown by the research in this special issue, these modules differ in neuromuscular control,

locomotor function, developmental patterning, and evolutionary pliability. These regions are modules in the sense that relative to functional, developmental, and evolutionary

activities within a module, the same activities among modules are more loosely correlated. While this three-module model is likely to be a gross over-simpliﬁcation, it serves

as a first approximation of how the body axis has different degrees of integration. Note that median fins, other than the caudal fin, and paired fins and limbs have been omitted.

In the transverse view (bottom row), the level of gray indicates endo-skeletal elements (light gray), muscle (darker gray), visceral cavity (darkest gray), and connective tissues

of the skin, primary horizontal septum, and vertical septum (black).

development are, in some respects, different from the processes Ashley-Ross, M.A., Perlman, B.M., Gibb, A.C., Long Jr., J.H., 2014. Jumping sans legs:

does elastic energy storage by the vertebral column power terrestrial jumps in

that govern caudal vertebral development (Ward and Mehta, 2014).

bony ﬁshes? Zoology 117, 7–18.

The null hypothesis is that modules do not exist. Without modu-

Buchholtz, E.A., 2014. Crossing the frontier: a hypothesis for the origins of meristic

larity, we would expect anatomy and developmental processes constraint in mammalian axial patterning. Zoology 117, 64–69.

Cabelguen, J.-M., Charrier, V., Mathou, A., 2014. Modular functional organisation of

along the body axis to change gradually. But they do not. In the

the axial locomotor system in salamanders. Zoology 117, 57–63.

extreme case of mammals, we see distinct regions of vertebrae,

Eaton, R.C., Lee, R.K.K., Foreman, M.B., 2001. The Mauthner cell and other identiﬁed

even within the precaudal region, correlated with developmental neurons of the brainstem escape network of ﬁsh. Prog. Neurobiol. 63, 467–485.

Flammang, B.E., 2014. The ﬁsh tail as a derivation from axial musculoskeletal

frontiers (Buchholtz, 2014). While at ﬁrst blush the neuromuscular

anatomy: an integrative analysis of functional morphology. Zoology 117, 86–92.

control of body bending in fast-starting ﬁshes may appear to lack

Flammang, B.E., Lauder, G.V., 2009. Caudal ﬁn shape modulation and control dur-

functional modularity, species with elongated body axes may pass ing acceleration, braking, and backing maneuvers in bluegill sunﬁsh, Lepomis

some threshold where modularity permits S-starts to occur (Liu and macrochirus. J. Exp. Biol. 212, 277–286.

Gemballa, S., Konstantinidis, P., Donley, J.M., Sepulveda, C., Shadwick, R.E., 2006.

Hale, 2014). In salamanders, neuromuscular control of the bending

Evolution of high-performance swimming in sharks: transformations of the

axis can be seen to switch from non-modular to modular, precaudal

musculotendinous system from subcarangiform to thunniform swimmers. J.

and caudal (Cabelguen et al., 2014). Functional and developmental Morphol. 267, 477–493.

Gibb, A.C., Ashley-Ross, M., Pace, C., Long Jr., J.H., 2011. Fish out of water: terrestrial

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gets, as suggested by the broad comparative patterns reported in

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the vertebral morphospace (Ward and Mehta, 2014). and neural control of the fast-start escape response. Evolution 56, 993–1007.

Hebrank, J.H., Hebrank, M.R., Long Jr., J.H., Block, B.A., Wainwright, S.A., 1990. Back-

bone mechanics of the blue marlin Makaira nigricans (Pisces, Istiophoridae). J.

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Long Jr., J.H., Porter, M.E., Liew, C.W., Root, R.G., 2010. Go reconﬁgure: how ﬁsh

change shape as they swim and evolve. Integr. Comp. Biol. 50, 1120–1139.

We wish to thank the International Society of Vertebrate Mor-

Liu, Y.-C., Hale, M.E., 2014. Alternative forms of axial startle behaviors in ﬁshes.

phology (ISVM). Under the leadership of President Larry Witmer Zoology 117, 36–47.

Müller, J., Scheyer, T.M., Head, J.J., Barrett, P.M., Werneberg, I., Ericson, P.G.B., Pol, D.,

and Past-President Marvalee Wake, the ISVM hosted the Inter-

Sanchez-Villagra, M.R., 2010. Homeotic effects, somitogenesis and the evolution

national Congress of Vertebrate Morphology in Barcelona in July

of vertebral numbers in recent and fossil amniotes. Proc. Natl. Acad. Sci. U. S. A.

2013. At that congress, we held the symposium at which most of 107, 2118–2123.

Nishikawa, K., Biewener, A.A., Aerts, P., Ahn, A.N., Chiel, H.J., Daley, M.A., Daniel,

the contributors to this special issue presented their work. Their

T.L., Full, R.J., Hale, M.E., Hedrick, T.L., Lappin, A.K., Nichols, T.R., Quinn, R.D.,

participation was made possible, in part, by the National Science

Satterlie, R.A., Szymki, B., 2007. Neuromechanics: an integrative approach for

Foundation (grant no. IOS-1306718), and we are grateful for their understanding motor control. Integr. Comp. Biol. 47, 16–54.

Nowroozi, B.N., Brainerd, E.L., 2013. X-ray motion analysis of the vertebral column

contributions. JHL was also supported by the National Science

during the startle response in striped bass, Morone saxatilis. J. Exp. Biol. 216,

Foundation (grant no. IOS-0922605). Finally, we thank Adam Sum-

2833–2842.

mers and Renate Schilling of Zoology for their careful shepherding Nowroozi, B.N., Brainerd, E.L., 2014. Importance of mechanics and kinematics in

of this issue through peer-review and publication; we also thank all determining the stiffness contribution of the vertebral column during body-

caudal-ﬁn swimming in ﬁshes. Zoology 117, 28–35.

of the reviewers of the papers for their constructive criticism and

Ota, K.G., Fujimoto, S., Oisi, Y., Kuratani, S., 2013. Late development of hagﬁsh ver-

suggestions.

tebral elements. J. Exp. Zool. B 320, 129–139.

Ota, K.G., Oisi, Y., Fujimoto, S., Kuratani, S., 2014. The origin of developmental mech-

anisms underlying vertebral elements: implications from hagﬁsh evo-devo.

Zoology 117, 77–80.

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