Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170
Review
The evolution of tendon — morphology and material properties夞
Adam P. Summersa,*, Thomas J. Koobb
a
Ecology and Evolutionary Biology, 321 Steinhaus Hall, University of California, Irvine, CA 92697-2525, USA
b
Shriners Hospital for Children, 12502 North Pine Drive, Tampa, FL 33612, USA
Received 25 February 2002; received in revised form 19 August 2002; accepted 19 August 2002
Abstract
Phylogenetically, tendinous tissue first appears in the invertebrate chordate Branchiostoma as myosepta. This twodimensional array of collagen fibers is highly organized, with fibers running along two primary axes. In hagfish the first
linear tendons appear and the myosepta have developed specialized regions with unidirectional fiber orientation—a linear
tendon within the flat sheet of myoseptum. Tendons react to compressive load by first forming a fibrocartilaginous pad,
and under severe stress, sesamoid bones. Evidence for this ability to react to load first arises in the cartilaginous fish,
here documented in a tendon from the jaw of a hard-prey crushing stingray. Sesamoid bones are common in bony fish
and also in tetrapods. Tendons will also calcify under tensile loads in some groups of birds, and this reaction to load is
seen in no other vertebrates. We conclude that the evolutionary history of tendon gives us insight into the use of model
systems for investigating tendon biology. Using mammal and fish models may be more appropriate than avian models
because of the apparent evolution of a novel reaction to tensile loads in birds.
䊚 2002 Elsevier Science Inc. All rights reserved.
Keywords: Stress; Strain; Tensile; Collagen; Hagfish; Agnathans; Strength; Stiffness; Morphology; Material properties; Model systems;
Connective tissue; Evolutionary transitions; Vertebrata
‘‘Tendons, forming the attachment of many muscles,
consist of bundles of connective tissue fibers’’
Alfred S. Romer.
1. Introduction
Tendon is most often thought of as the bright
white, parallel fibered connective tissue that joins
夞 This paper was presented at ‘Tendon – Bridging the Gap’,
a symposium at the 2002 Society of Integrative and Comparative Biology. Participation was funded by SICB, The Shriners
Hospitals for Children, and the National Science Foundation
(IBN-0127260).
*Corresponding. Tel.: q1-949-824-9359; fax: q1-510-3153106.
E-mail addresses: [email protected] (A.P. Summers),
[email protected] (T.J. Koob).
muscle to bone, but this definition does not begin
to account for the varied forms of tendinous
tissue—even within a single organism—its adaptation to load, or the form that it takes in lower
vertebrates. In order to understand the evolution
of the musculoskeletal system in vertebrates it is
important to understand the evolutionary history
of tendon as a tissue. Our understanding of tendon
has lagged behind that of bone and cartilage, both
of which have been placed in an evolutionary
context (Moss and Moss-Salentijn, 1983; Person,
1983; Smith and Hall, 1990). In fact, comparative
research on tendon is so rare that this project may
be premature. Nevertheless, we attempt in the next
few pages to synthesize tendon research in an
evolutionary context, if for no other purpose than
1095-6433/02/$ - see front matter 䊚 2002 Elsevier Science Inc. All rights reserved.
PII: S 1 0 9 5 - 6 4 3 3 Ž 0 2 . 0 0 2 4 1 - 6
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to point out those areas that sorely need further
investigation.
We consider tendon to be a tissue, and will refer
to it as such, though at times we will use ‘tendinous tissue’ to make clear the distinction between
the tissue and a particular tendinous organ (i.e.
digital flexor tendon). Our working definition of
tendon is an amalgam of functional and compositional definitions: a dense, highly organized tissue
that transmits force, and is composed predominantly of type I collagen with fibril associated
proteoglycans.
2. Morphology
Tendon is most familiar as the densely packed,
linearly-arrayed, collagenous tissue seen in flexor
and extensor tendons in tetrapod limbs. However,
it should be recognized that there are other collagenous connective tissues that perform the same
functional task, that of transferring force generated
by muscle from the muscle end to a target. These
include the dense, well-organized arrays of connective tissue in the myosepta of lower vertebrates,
as well as aponeuroses.
The body musculature of vertebrates is arranged
in serially homologous myomeres, each separated
from the next by a collagenous myoseptum. In
humans one of the few vestiges of this segmentation is the ‘six-pack’ of the abdominal muscles,
but as anyone who has eaten a fish fillet can attest,
blocky myomeres are far more obvious in lower
vertebrates. Myosepta are not mats of disorganized
collagen but rather highly organized structures with
collagen organized in uni- or bi-directional sheets
(Liem et al., 2000; Vogel and Gemballa, 2000).
Furthermore, it should be recognized that simple
myosepta and linearly-arrayed tendon are extremes
in a continuum. There are numerous examples
from fish and tetrapods of aponeuroses that grade
into tendon (Liem et al., 2000), and, within the
myosepta of fish there are collagen fibers with
preferred orientation that form linear tendon structures (Westneat et al., 1993; Vogel and Gemballa,
2000; Gemballa and Vogel, 2002).
In this section we will examine morphological
innovations in these dense, collagenous tissues that
serve to transmit the force of muscles across an
array of chordate taxa. In the interest of brevity
we will establish a plesiomorphic condition for
tendinous tissue and then specifically treat only
those taxa that exhibit novel morphology relative
to this ‘ancestral’ state.
2.1. Urochordates
The most well known group of urochordates,
the ascidians or sea-squirts, are sessile as adults,
but as larvae they may be free-swimming ‘tadpoles’ propelling themselves along a helical path
with undulations of their tail (Gans et al., 1996;
McHenry, 2001). The muscles that drive this locomotion are not divided by collagenous myosepta,
and the muscle itself more closely resembles cardiac than striated muscle (Cloney and Burighel,
1991). The only hint of tendinous tissue is in a
series of collagenous, connective tissue leaflets
that issue from the notochordal sheath but do not
appear to be attached to muscle (Cloney, 1964).
At present there is no evidence for tendinous
structures in urochordates.
2.2. Cephalochordates
The undulatory locomotion of the lancelets is
powered by myotomal muscle divided by collagenous myosepta (Fig. 1) (Weitbrecht, 2000), a
feature that is clearly seen in several fossil forms
including Pikaia from the Burgess Shale.
There is scant evidence of any linear tendons in
lancelets, the only possible exception being structures that Ruppert (1991) refers to as ‘microligaments’. These are connective tissue projections
that join the myomeric muscle to the body wall,
however, they are quite thin (1–5 mm) and there
is no evidence that they are collagenous. We infer
that well-organized and functional fibrous myosepta appear for the first time in the chordate lineage
in Cephalochordates.
2.3. Agnathans
The jawless fish, lampreys and hagfish use
myomeric muscle to power undulatory locomotion,
and according to the well preserved fossils of
Haikouichthys and Myllokunmingia, this has been
the case since the Lower Cambrian (490–540
MYA) (Chen et al., 1999; Shu et al., 1999). The
myosepta are collagenous sheets with evidence for
the local specializations that form linearly arrayed
tendons in bony fish (Vogel and Gemballa, 2001).
Hagfish also have an interesting hydrostatic tongue
A.P. Summers, T.J. Koob / Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170
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2.4. Cartilaginous and bony fish
Fig. 1. A light micrograph of a single myseptum from Branchiostoma lanceolatum shows the organization of the collagen
fibers into a two-dimensional array. The inscribed lines are to
indicate the two primary directions of the collagen fibers (modified with permission from Weitbrecht, 2000).
protrusion and retraction mechanism that involves
two pennate muscles and two linear tendons (Fig.
2) (Coles, 1905, 1907, 1914). We have prepared
histological sections (10 mm paraffin) of one of
the tongue retractor tendons (M. retractor mandibuli tendon). The tendon is superficially quite
similar in appearance to that of mammals, having
the characteristic bright white color, clearly oriented fibrous material, and discrete edges. However,
it appears to lack the organization into primary
and secondary bundles, as well as the epitenon
and paratenon seen in mammals (Kastelic et al.,
1978). The only indication of this hierarchical
organization is that there is an inner ‘core’ tendon
wrapped with an outer ‘sheath’ tendon (Fig. 3).
Cartilaginous and bony fish have tendinous
myosepta between the blocks of body musculature
as well as linear tendons associated with jaw and
pharyngeal muscles. The former appear quite similar to the myosepta in agnathans with some
specialized regions that are linear in orientation
(Hagen et al., 2001). The linear tendons found in
the feeding apparatus resemble those of mammals
and some individual tendons are likely homologs
of mammalian tendons (i.e. an adductor mandibularis tendonstemporalis tendon) (Liem et al.,
2000). Furthermore, the cartilaginous fish show
tendon specializations that have previously only
been reported in tetrapods. Tendons are normally
subjected to tensile loads, however when one
makes a sharp turn around a corner it is also
subjected to compressive and shear loading in the
region of the bend. This compressive loading leads
to the formation of a fibrocartilaginous pad along
the inner surface of the bend (Vogel and Koob,
1989; Benjamin and Ralphs, 1998).
Some stingrays eat hard prey almost exclusively,
and have several specializations of their jaws that
reinforce their mandibular cartilage and increase
the effective force of their jaw adductors (Summers et al., 1998; Summers, 2000). The ventral
intermandibular tendon of one of these specialists,
the cownose ray (Rhinoptera bonasus), makes a
sharp turn as it passes dorsally around the corner
of the jaws. We found a fibrocartilaginous pad
associated with the tendon along the inner edge of
this sharp bend (Fig. 4a). Histologically it appears
similar to fibrocartilage from mammals (Fig. 4b)
and we believe this is the phylogenetically earliest
example of tendon’s ability to adapt to compressive load. The ability of tendon to respond to
compressive load by forming a fibrocartilaginous
pad has been confirmed in amphibians (Carvalho
and Vidal, 1994, 1995), archosaurs (Felisbino and
Carvalho, 1999), and mammals (for review see
Benjamin and Ralphs, 1998).
A further adaptation to compressive load is the
formation of sesamoid bones in regions of tendon
that bend over a bony prominence (for review see
Sarin et al., 1999). These bones arise within the
tendon and may be encapsulated in a synovial
sheath. In mammals there is evidence that sesamoid formation can be induced by load, however
some sesamoids form regardless of force regime
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Fig. 2. Panels 1–4 show the retraction of the toothy tongue of Myxine glutinosa accomplished by manually pulling on the retractor
tendon. Scale bars5 mm. The lower panel shows the anatomy of the teeth, the supporting cartilage and the two tendons that protract
and retract the tooth plate (modified from Coles, 1907).
(i.e. the patella). There are no sesamoids in cartilaginous fish, but they are prominent in bony fish.
The urohyal, the bone that supports the tongue,
may be the most well known example, though
other bones of the branchial arches are also formed
in tendon and are clear in fossil and recent taxa
(Patterson, 1977; Arratia and Schultze, 1990; Liem
et al., 2000). Sesamoids are widespread in other
vertebrates including amphibians (Olson, 2000;
Trueb et al., 2000), squamate reptiles (Maisano,
2001), archosaurs (Sych, 2001; Hutchinson,
2002), and mammals.
2.5. Archosaurs
In addition to the aforementioned response to a
compressive load there are indications that tendon
will respond to tensile loads by mineralizing (for
review see Landis, 2002). These mineralizations
are quite different from sesamoid bone, in that
they never become encapsulated in a synovial
envelope, they do not have the histology of bone,
and they are not associated with tendons passing
over bony prominences. Rather these mineralizations usually arise when a tendon bifurcates, lead-
A.P. Summers, T.J. Koob / Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170
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3. Material properties
Fig. 3. (a) An alcian blue stained longitudinal section through
the tongue retractor tendon approximately midway along its
length. The gaps in the dense connective tissue separate the
inner ‘core’ tendon from the outer ‘sheath’ tendon and are the
only indication of tendon organization. Scale bars200 mm. (b)
An hemotoxylin and eosin stained section showing the relatively high cellularity of the gap region compared to the tendinous region. There are few tenocytes evident, as is often the
case in mammalian tendon. Scale bars125 mm.
ing to a higher load in the two smaller tendons
than there is in the conjoined tendons. They appear
to have arisen in the non-avian dinosaurs (Hutchinson, 2002), but as far as we can tell are found
in no other group of chordates.
2.6. Mammals
Aside from the hierarchical organization of
mammalian tendon (Kastelic et al., 1978), there
are no morphological characters of tendon that we
do not see in other vertebrate groups. A possible
exception may be in the morphology of the tendon
entheses, the insertion of the tendon onto the bone,
but there are no comparative data from other taxa
(Benjamin et al., 2002).
There are two principal difficulties in synthesizing an evolutionary perspective on the material
properties of tendon: firstly, there is no accepted
standard protocol for testing, so results of different
studies are difficult to compare; second, there are
few literature values for the mechanical properties
of tendon from lower vertebrates, and none at all
from cartilaginous fish or agnathans. To address
the first issue we present a range of representative
published values for several biomechanically
important measures of the response of tendon to
applied force. To provide a broader evolutionary
picture we also present original data from our own
tests on a relatively obscure, linearly arrayed tendon from the hagfish described above.
Biological structures are notoriously difficult to
characterize with the standard material properties,
such as strength and stiffness, used for manufactured solids. The reasons for this fall into two
categories—technical problems that have their
basis in the inconvenient sizes and shapes of living
tissue; and difficulties that arise from the heterogeneous make-up and visco-elasticity of natural
materials (Vogel, 1988; Niklas, 1992; Martin et
al., 1998). Tendons present special technical challenges from the point of view of clamping and
preconditioning, and are certainly heterogeneous,
viscoelastic materials, nevertheless there is an
extensive literature on the tensile properties of
mammalian tendon (i.e. Bennett et al., 1986;
Pollock and Shadwick, 1994b; de Zee et al., 2000).
3.1. Hagfish tendon
We dissected 14, fresh, frozen hagfish (Myxine
glutinosa) heads, removing the complete retractor
mandibuli tendon from its origin on a thin cartilaginous rod at the posterior end of the tongue
retractor muscle to the insertion on the cartilaginous tooth plate (for relevant anatomy see Coles,
1907). Tendons were kept moist with hagfish
Ringers (0.53 M NaCl, 7 mM KCl, 4.5 mM CaCl,
12 mM MgCl2, 0.9 mM Na2SO4, 25 mM Tris at
pH 7.95) (Riegel, 1978) for the brief time between
dissection and testing. Material properties were
determined with a tensile test to failure using an
MTS Mini Bionix with a 500-g load cell at a
strain rate of 2 mmys. Approximately 1 cm of
each end of the tendon was held between the
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Fig. 4. (a) A ventral view of the upper and lower jaws of a cownose ray (Rhinoptera bonasus) showing the arrangement of the adductor
mandibularis medialis (AMM) muscle and the associated tendon. (b) Masson’s trichrome stained paraffin section (10 mm thick) of
the fibrocartilaginous pad from the AMM tendon showing regions of proteoglycan matrix (blue) and organized fibrous areas (red).
Scale bars100 mm. (c) Section of the fibrocartilaginous region of a calf meniscus showing similar morphology to the stingray tendon.
Scale bars100 mm
serrate jaws of standard tensile grips. Grips were
then cooled by manual application of dry ice
(–78 8C) until the tissue inside the grips was
visibly affected. Tissue between the grips (8–15
mm) was checked with forceps to ensure that it
had not frozen. In spite of freeze clamping, the
tendon shifted in the grips in 6 of 14 tests resulting
in slippage artifacts that prevented us from using
these samples in calculating the maximum strain
of the specimen (Fig. 5). The diameter of the
unstretched, cylindrical tendon was measured with
calipers to the nearest tenth of a millimeter. Stress
vs. strain curves were generated from the MTS
data and used to calculate ultimate strength, stiffness, and failure strain.
The strength of the hagfish tongue retractor
tendon was 47.8"3.5 MPa, and from the samples
that did not slip in the clamps (ns8) we calculated
the strain at failure to be 22"2%. This value is
well beyond any reliable estimate of maximum
strain in mammalian tendon (-10%). The stiffness of the tendon was 290"29 MPa. These values
A.P. Summers, T.J. Koob / Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170
1165
Fig. 5. Stress vs. strain curves for the hagfish (Myxine glutinosa) tongue retractor tendon. The ranges of values for strength and breaking
strain in mammalian tendon are indicated by the bars.
are similar to values reported for some mammalian
tendons (Fig. 5).
3.2. Bony and cartilaginous fish
Cartilaginous fish have few linearly arrayed
tendons (Liem and Summers, 1999), and there has
been no assessment of their material properties,
nor the properties of the aponeurotic tendons. The
literature for bony fish contains just two data
points. In this volume Shadwick et al. (2002)
report that the tail tendons of albacore and yellowfin tuna, fast swimming scombrid fish, are quite
stiff (1.19–1.43 GPa), and they estimate a breaking strength near 30 MPa.
3.3. Amphibians
Of the three extant groups of lissamphibians
(frogs, salamanders, and caecilians) only frog tendons have been tested in depth. There are no
records for the limbless and enigmatic caecilians,
and a single record for salamanders—Azizi et al.
(2002) found a maximum stiffness of 7.1 MPa for
the sheet-like tendinous myosepta of the siren
(Siren lacertina). Although frogs are important
model systems for the study of muscle only a few
studies address tendon mechanics, and those only
report values for stiffness (Lieber et al., 1991;
Trestik and Lieber, 1993). Gastrocnemius tendon
(Es1.5 GPa) is similar to mammals, but the
semitendinosus (0.2 GPa) is only as stiff as hagfish
tendon.
3.4. Archosaurs
Of the two extant groups of archosaurs, the birds
and the crocodilians, there are data only from the
former, though the latter have prominent, functionally important tendons. Some groups of birds (and
some extinct non-avian dinosaurs; Hutchinson,
2002) mineralize their tendons, which has a pro-
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1994b; Pike et al., 2000). From a functional point
of view mammalian tendons fall into two categories, those that act as springs, such as the Achilles
and digital flexor tendons of quadrupedal mammals, and those that simply transmit muscle force
without storing significant energy, as in the digital
extensors and biceps tendon (Alexander, 1984;
Biewener and Blickhan, 1988; Biewener, 1998).
Oddly, though these two functions might best be
addressed by varied material properties, it seems
that natural selection has not led to significant
differences between them (Pollock and Shadwick,
1994b). In other words, while it would seem
logical that the amount of strain energy stored in
a tendon could be ‘tuned’ by varying the stiffness
and resilience, in fact these properties are relatively
invariant across a wide variety of tendons.
Rather than rehash these studies, or a subset of
them, we would like to point out the high and low
values that have been reported for several properties and present scattergrams that summarize a
synoptic review of the literature (Fig. 6).
Fig. 6. Scattergram showing values for (a) stiffness and (b)
strength of tendon from several chordate taxa. The values for
hagfish (Myxine glutinosa) are from this paper. Data for fish
(Shadwick et al., 2002), amphibians (Lieber et al., 1991, 2000;
Trestik and Lieber, 1993), birds (Bennett and Stafford, 1988;
Leonard et al., 1976), and mammals (Bennett et al., 1986; Itoi
et al., 1995; Kondo et al., 1998; Pollock and Shadwick, 1994b;
Wren et al., 2001) were gathered from literature sources.
4. Discussion
Though there is too little evidence from nonmammalian taxa to be completely confident in an
evolutionary scenario, we would propose the following hypotheses (Figs. 7 and 8). The first
appearance of tendinous tissue is as myosepta, thin
found effect on their properties (Bennett and Stafford, 1988). Indeed in some cases the stiffness of
calcified tendon can approach that of bone (Leonard et al., 1976; Bennett and Stafford, 1988). Here
we are interested in the unmineralized tendon’s
behavior under load, which has been measured in
the usual tensometer devices as well as in vivo,
and in vitro using disparate techniques such as
sonomicrometry, force buckles, and ultrasound
(Biewener et al., 1992; Mohamed et al., 1995;
Buchanan and Marsh, 2001). The stiffness of avian
tendons (mineralized and unmineralized) ranged
from 0.9 to 13 GPa, and the strength from 54 to
117 MPa.
3.5. Mammals
There is a vast body of literature on the techniques of testing mammalian tendon (i.e. Riemersma and Schamhardt, 1982; Martin et al., 1998;
Ker et al., 2000), and on the properties of tendon
(i.e. Bennett et al., 1986; Pollock and Shadwick,
Fig. 7. Cladogram of the chordates (modified from Liem et al.,
2000) showing the evolutionary transitions of tendon: (1)
‘leaflets’ of connective tissue emanating from the notochord
sheath; (2) an organized array of collagen forms myosepta; (3)
linear tendon; specializations in the myosepta; (4) tendon
responds to compressive loading with a fibrocartilaginous pad;
and (5) sesamoid bones in areas of high compressive loading.
A.P. Summers, T.J. Koob / Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170
Fig. 8. Cladogram of the vertebrates (modified from Liem et
al., 2000) showing the evolutionary transition of tendon: (1)
tendon responds to compressive loading with a fibrocartilaginous pad; (2) sesamoid bones in areas of high compressive
loading; and (3) tendons in tension calcify in response to load.
sheets of connective tissue with collagen fibers
organized to resist tension from several directions.
As body plans became more adapted for highspeed undulatory locomotion the myosepta became
specialized, with some regions being composed
almost entirely of unidirectional collagen fibers—
a linear tendon within the flat sheet of the myoseptal tendon. This is supported by the work of
Gemballa’s group on Branchiostoma, agnathans,
and fish (Vogel and Gemballa, 2001; Weitbrecht
and Gemballa, 2001; Gemballa and Vogel, 2002).
Linear tendons appear in the agnathans (Acrania)
before the advent of vertebrates, and before the
evolution of endochondral bone (Smith and Hall,
1990). This renders the textbook definition of
tendon as a tissue that connects muscle to bone
somewhat problematic.
Sometime in or before the Silurian (440 to 410
mya) tendon acquired the ability to adapt to
compressive loads by forming fibrocartilage, and
by the Devonian, bony fish have formed sesamoid
bones (Patterson, 1977; Arratia and Schultze,
1990). This is supported by our own work on the
fibrocartilage of a cartilaginous fish (see preceding
section) and by the fossil record of fish (Long,
1995). The ability to calcify tendon in response to
tensile loads is not certainly present until the
evolution of birds in the Jurassic period (208 to
146 mya) (Padian, 1997). The uniformity in material properties and the lack of novel responses to
loading in eutherian and metatherian mammals is
1167
an indication that tendon has not undergone any
major evolutionary transitions in the mammals.
This implies that some non-mammals, and even
non-tetrapods, may be used as model systems for
studying tendon development, physiology, morphology, and repair. It is important to note that
birds may not be a good model system for mammalian tendon biology, as avian tendon appears to
have evolved a novel response to tensile stress
(Fig. 8).
On the evolution of material properties there is
little we can be sure of, but we would speculate
that the high strength of linear tendon is primitive
on the basis of our hagfish data. Stiffness may
have increased over evolutionary time in the lineages that gave rise to fish and tetrapods, but
strength arose early and has been little changed
through evolutionary time. We require a more
extensive survey of material properties in fish and
lower tetrapods to generate further hypotheses.
Clearly, we have woefully little knowledge of
non-mammalian tendon. Among the significant
groups for which there are little or no data are the
squamate reptiles, turtles, and cartilaginous fish.
This is particularly troubling given the interesting
transition that apparently takes place between the
agnathans and the tetrapods—tendon becomes
stiffer, it gains an epitenon, and becomes integrated
into the locomotor system as a spring. We cannot
understand the current character states in mammals
without learning the evolutionary trajectory that
they traversed in getting there.
In the area of material properties there are
several topics that would be quite interesting to
know more about. The reported values for resilience, that is the efficiency of energy storage, for
mammalian and fish tendon are quite high—on
the order of 90% (Alexander, 1984; Pollock and
Shadwick, 1994a; Shadwick et al., 2002). The fish
tendons and mammalian tendons that have been
tested are of similar stiffness (Fig. 6). From the
scant comparative data it is clear that there are
tendons of far lesser stiffness in both frogs and
hagfish. It would be interesting to know if the
high resilience is linked to high stiffness or whether these traits are independent.
The lack of an epitenon in the hagfish tongue
tendon may represent a primitive, less hierarchical
structure. Comparative morphological data from
bony and cartilaginous fish, amphibians and reptiles would settle the question of where the mammalian architecture of tendon arose (Kastelic et
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al., 1978; Rowe, 1985), and concomitantly might
show whether the increased stiffness of mammalian tendon relative to hagfish tendon is related to
this organization.
Perhaps the most exciting area in tendon
mechanics is that of the viscoelastic properties and
fatigue quality (Ker et al., 2000; Ker, 2002). With
only a few data from sheep and kangaroos, there
remains a gap in our understanding of the evolution of time-dependent responses to steady and
cyclic loading. This lack of knowledge is particularly troubling given the wide range of locomotor
´
behaviors and novel stress regimes
that appear in
the tetrapod lineage. The evolutionary history of
fatigue quality and creep responses may be linked
to the evolution of terrestriality, a cursorial lifestyle, or even metabolic rate.
Acknowledgments
Magdalena Koob-Emunds performed histological chores on short notice with good spirit. Eric
Hilton provided fossil advice, and the paper benefited from discussions with Beth Brainerd, and
many other participants in the SICB symposium
‘Tendon-Bridging the Gap’. We particularly thank
Sven Gemballa for the lancelet myosepta photograph. Steve Kajiura kindly commented on an
earlier draft of this manuscript. The McDowell
Foundation, The Shriners Hospitals for Children,
and the National Science Foundation (IBN0127260) provided support for this work.
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