Jennifer A. Clack made groundbreaking fossil discoveries of
the emergence of animals with backbones out of the water onto the land.
Her work lifted the study of the transition from fishes to tetrapods
from palaeontological obscurity to star status, ranking alongside such
favourites as the origin of birds or the evolution of the human lineage.
A happy convergence of brilliance, tenacity, opportunity, generosity
and modesty enabled Clack (née Agnew) to rejuvenate an entire research
field. She died on 26 March, aged 72.
Clack amassed an
unprecedented trove of several hundred tetrapod fossils from the
Devonian (419 million to 359 million years ago) and Carboniferous
periods (359 million to 299 million years ago). She did so through a
combination of fieldwork in southern Scotland and two expeditions to
Greenland, the latter following up a chance discovery in a museum
drawer. These strange animals resembled large salamanders or small
crocodiles but they retained fish-like characteristics such as tail
fins. Her papers describing and interpreting them shed light on the
evolution of the body plan of land vertebrates. She broke open the
entrenched positions of the previous generation of researchers.
Clack
was born in 1947 in Manchester, UK. She studied zoology at the
University of Newcastle upon Tyne, graduating in 1970. One of her
lecturers, Alec Panchen, was re-evaluating Carboniferous tetrapod
fossils discovered during the nineteenth century. Clack was intrigued,
but Panchen was unable to offer her a PhD position. Instead, Clack did a
one-year graduate certificate in museum studies at the University of
Leicester, which led to a job at the City of Birmingham Museum and Art
Gallery. During this time, she met fellow biker and fossil enthusiast
Rob Clack. They married in 1980.
In 1978, Clack was finally able
to begin a PhD in Panchen’s lab, working on a specimen of the large,
salamander-like Carboniferous tetrapod Pholiderpeton. It proved
to have an ear bone (stapes) shaped like a butterfly and probably no
eardrum, defying expectations that these early tetrapods would have had
ears like those of frogs, with an eardrum and a rod-like stapes. Clack
proposed that the ‘middle ear’ of the earliest tetrapods was much more
primitive, still a small gill opening as in fishes, and that the drum
evolved later, a hypothesis that is now widely accepted.
In 1981,
Clack secured a permanent position at the University Museum of Zoology
in Cambridge, UK, where she remained. In 1986, she made a chance
discovery that defined her career: in the Sedgwick Museum in Cambridge
she found fossils of Late Devonian tetrapods from eastern Greenland,
collected in the 1960s.
Only three Devonian tetrapods were then known, two of them (Ichthyostega and Acanthostega) also from eastern Greenland. The Ichthyostega material was quite extensive; Acanthostega was little more than a name attached to half a skull. In the Sedgwick, Clack found several skulls of Acanthostega,
with sections of vertebral column attached, the tight fit of the pieces
showing that the tetrapods had been lying packed together in the rock.
In
June 1987, Clack set off for Greenland with Rob, myself (her first PhD
student) and two colleagues from Copenhagen to find more specimens. The
results exceeded her wildest expectations. She returned with the largest
haul of tetrapod fossils ever recovered in one season from the Devonian
deposits in Greenland. Back in Cambridge, Clack recruited two new team
members — a postdoc, Michael Coates, and a fossil preparator, Sarah
Finney — and set to work.
A series of groundbreaking papers poured forth describing Acanthostega
specimens, many of which showed new and unexpected features that were
to overturn established views of the transition from water to land.
The paper with the greatest impact — popular and scientific — showed that the feet of Ichthyostega and Acanthostega had, respectively, seven and eight toes apiece, rather than the canonical five (M. I. Coates and J. A. Clack Nature 347, 66–69; 1990).
The paper received the ultimate pop-science accolade: the US
palaeontologist Stephen Jay Gould devoted one of his regular essays in Natural History magazine to it. A follow-up expedition to Greenland in 1998 found more material, especially of Ichthyostega.
During
the last decade of her life, Clack increasingly turned her attention
back to the Carboniferous tetrapods. She worked especially on ‘Romer’s
Gap’ — the 30-million-year break in the fossil record between the Late
Devonian forms and the more advanced tetrapods of the mid-Carboniferous.
She suspected that this lacuna might be a sampling artefact. She
assembled a team of researchers to investigate sediments in northern
England and southern Scotland, called the Ballagan Formation, which
represent the earliest Carboniferous (around 359 million to 347 million
years ago).
These sandstones and mudstones promptly started
yielding fossils of previously unknown tetrapods. Six genera have been
described so far and more material awaits description. They look set to
revolutionize our understanding of the early diversification of
tetrapods by filling in the wide morphological gap between very
primitive ones, such as Acanthostega, and the more modern tetrapods of the Carboniferous.
Amid all this triumph, and having seen her book Gaining Ground
(2002, 2012) become the standard text on the origin of tetrapods, Clack
noticed the first symptoms of cancer. She continued working until her
last few days. Clack leaves behind a vibrant research area,
characterized by collegial openness that she did much to foster. Her
death leaves a very big void.
Nature580, 587 (2020)
doi: 10.1038/d41586-020-01217-8
sexta-feira, 25 de outubro de 2019
Early tetrapods had an eye on the land
Fossil finds that can provide clues about how
aquatic vertebrates evolved into land dwellers are elusive. But the
ancient bones of a newly discovered species of tetrapod now provide some
crucial missing evidence.
Following the scientific investigations into how
vertebrates transitioned from water to land is like reading a good crime
novel. We have a range of suspects, patchy evidence and a lot of
unanswered questions. And to complicate matters, this transition from
finned fish to four-limbed creatures (tetrapods) is a ‘cold case’ from
nearly 400 million years ago. In a paper in Nature, Beznosov et al.1 present some compelling detective work that sheds light on this.
The earliest-known tetrapod specimens are
380-million-year-old bone fragments that, although identifiable as
belonging to a tetrapod, do not provide many details about what these
animals looked like or how they lived2.
There are also fossilized tetrapod footprints that pre-date these fossil finds by more than 14 million years3,
indicating the presence of a four-limbed, still fully aquatic track
maker — but they do not reveal what the track maker looked like above
the soles of its feet.
More-detailed insights into the body shape,
life and growth of our early vertebrate ancestors are provided by
more-complete fossil finds, including the iconic tetrapods Acanthostega and Ichthyostega2,4.
However, these lived 365 million years ago, when tetrapods had already
achieved an impressive geographical distribution and a diverse variety
of body shapes and ways of life2.
By
contrast, the earliest phase of tetrapod evolution and diversification
has long been mysterious. However, Beznosov and colleagues now describe
skeletal fossils of a species they call Parmastega aelidae, which is the most ancestral (basal-most) tetrapod reported so far.
Like its known younger relatives, P. aelidae
was a gill-breathing water dweller, and the authors estimate that this
animal reached a size of more than one metre long. It lived about 372
million years ago during the Devonian period, and inhabited a shallow
lagoon in a landmass that is now part of northwestern Russia. These
excellently preserved fossils provide crucial data about how the major
changes in breathing, sensory perception, locomotion and feeding might
have taken place as tetrapods transitioned to life on land. The
discovery also raises many exciting questions.
The most striking features of the P. aelidae
skull are the large, oval-shaped eye openings, which face to the front
and side, and which are positioned high up, towards the top of the skull
(Fig. 1). This eye shape and position is surprising because it
indicates that this water dweller was looking above the surface of the
water.
Figure 1 | The evolution of tetrapod skulls. Beznosov et al.1
report 372-million-year-old fossils of a four-limbed vertebrate
(tetrapod) from just before the time when tetrapods moved onto land.
They call this newly discovered species Parmastega aelidae. Its
nasal passages (nares) are close to its jaw and would have been
positioned under water. Water passing though the nares (blue arrow)
would have been used for breathing when it reached the gills (not
shown). P. aelidae could also breathe air directly through a skull opening called a spiracle (grey). Comparing these ancestral features of P. aelidae
with other tetrapods reveals patterns of evolutionary change. The other
tetrapods shown are: an early tetrapod group called colosteids;
seymouriamorphs and embolomeres, members of a lineage that gave rise to
amniotes (birds, reptiles and mammals); and temnospondyls, which gave
rise to modern amphibians (such as frogs and salamanders). Colosteids
lacked spiracles and breathed solely through their gills using water
taken up through the nares. Compared with P. aelidae,
seymouriamorphs and temnospondyls had larger and higher nares, which
they would have used to breathe air (red arrow). These tetrapods lacked
spiracles, and had ears (yellow) instead in that area of their skull.
Embolomeres retained the breathing system used by P. aelidae.
Mudskippers (species from the family Oxudercidae) are modern
amphibious fish that inhabit marine mud flats, and they are useful
living creatures with which to compare P. aelidae because their
eyes have a similar shape and position. Mudskippers peek above the water
surface to look out for prey and potential danger5. But what was P. aelidae
looking for? The need to detect enemies on land or in the air can be
ruled out, because during the late Devonian period, such animals were
not yet present there.
One possibility is that P. aelidae
was looking for prey on the shore. If so, what kind of terrestrial or
semi-terrestrial prey was it watching? Some have suggested that early
water-dwelling tetrapods and their closest fish-like relatives might
have preyed on terrestrial invertebrates of the phylum Arthropoda, which
includes insects6. However, the large arthropods that could have provided sufficient food to sustain an animal the size of P. aelidae were still rare in the Devonian period7. Moreover, P. aelidae
had large fangs, which suggests that it preyed mainly on vertebrates.
Perhaps it searched for fish carcasses stranded on the shore. Or, to
make an even more speculative suggestion, maybe it scavenged early
amphibious tetrapods that rested near the water. However, evidence for
such creatures has not yet been found among the fossils of the
Sosnogorsk Formation (the rock layers that contained the P. aelidae fossil).
Another notable feature of P. aelidae is the
extremely low position, close to its jaws, of the external openings of
its nose (the nares), which would have been under water (Fig. 1). This
is in striking contrast to the high position of its eyes and is quite
different from the configuration of nares in modern-day aquatic tetrapod
animals, such as crocodiles, hippopotamuses or frogs. The eyes of those
animals sit on top of their head, and their nares are likewise
positioned high on the snout, which enables them to breathe air while
looking above water. Judging from their submerged position, P. aelidae nares acted as openings through which an inflow of water was directed towards the gills during breathing. P. aelidae
also had the option of breathing air through a large opening in its
skull called a spiracle (Fig. 1), and such a breathing process would
probably have been similar to that used by modern air-breathing fish8.
This
low position of the nares is found in most known early tetrapods
(called stem tetrapods) of the Devonian period (approximately 419.2
million to 358.9 million years ago) and Carboniferous period (358.9
million to 298.9 million years ago). In all of these animals, the
passage from the nares to the mouth cavity might still have served to
transport water rather than air. Some fossils of stem tetrapods, such as
those of a grouping called colosteids (Fig. 1), had lost their spiracle
opening — they must therefore have relied on gill breathing. In some
other early tetrapods that arose later than P. aelidae and were
more evolved than their ancestors (a state described as being more
derived), the spiracle is absent, and its place is taken by an ear2.
These tetrapods’ nares are larger and higher on the snout (Fig. 1)
compared with the ancestral form, suggesting that they used their nares
to transport air towards the lungs while peeking out of the water when
on the lookout for prey.
The P. aelidae fossils offer a
treasure trove of information that could help to disentangle some of the
complex evolutionary changes that took place when vertebrates made the
transition from aquatic to terrestrial life. This discovery also reminds
us that much still remains to be learnt in the next gripping chapter of
this detective story.
Nature574, 494-495 (2019)
doi: 10.1038/d41586-019-03107-0
Updates & Corrections
Correction 24 October 2019: The version of Figure 1 originally published was incorrect. This has now been corrected. The pdf version was correct.
quinta-feira, 31 de maio de 2018
Euryhaline ecology of early tetrapods revealed by stable isotopes
Ecologia de Euryhalina dos primeiros tetrápodes revelada por isótopos estáveis
The
fish-to-tetrapod transition—followed later by
terrestrialization—represented a major step in vertebrate evolution that
gave rise to a successful clade that today contains more than 30,000
tetrapod species. The early tetrapod Ichthyostega was discovered
in 1929 in the Devonian Old Red Sandstone sediments of East Greenland
(dated to approximately 365 million years ago). Since then, our
understanding of the fish-to-tetrapod transition has increased
considerably, owing to the discovery of additional Devonian taxa that
represent early tetrapods or groups evolutionarily close to them.
However, the aquatic environment of early tetrapods and the vertebrate
fauna associated with them has remained elusive and highly debated. Here
we use a multi-stable isotope approach (δ13C, δ18O and δ34S)
to show that some Devonian vertebrates, including early tetrapods, were
euryhaline and inhabited transitional aquatic environments subject to
high-magnitude, rapid changes in salinity, such as estuaries or deltas.
Euryhalinity may have predisposed the early tetrapod clade to be able to
survive Late Devonian biotic crises and then successfully colonize
terrestrial environments.
quinta-feira, 28 de junho de 2012
Three-dimensional limb joint mobility in the early tetrapod Ichthyostega
Nature 486, 523–526 (28 June 2012) doi:10.1038/nature11124
Received
Accepted
Published online
The origin of
tetrapods and the transition from swimming to walking was a pivotal step
in the evolution and diversification of terrestrial vertebrates. During
this time, modifications of the limbs—particularly the specialization
of joints and the structures that guide their motions—fundamentally
changed the ways in which early tetrapods could move1, 2, 3, 4.
Nonetheless, little is known about the functional consequences of limb
anatomy in early tetrapods and how that anatomy influenced locomotion
capabilities at this very critical stage in vertebrate evolution. Here
we present a three-dimensional reconstruction of the iconic Devonian
tetrapod Ichthyostega and a quantitative and comparative analysis of limb mobility in this early tetrapod. We show that Ichthyostega
could not have employed typical tetrapod locomotory behaviours, such as
lateral sequence walking. In particular, it lacked the necessary rotary
motions in its limbs to push the body off the ground and move the limbs
in an alternating sequence. Given that long-axis rotation was present
in the fins of tetrapodomorph fishes5, 6, 7, it seems that either early tetrapods evolved through an initial stage of restricted shoulder8, 9 and hip joint mobility or that Ichthyostega was unique in this respect. We conclude that early tetrapods with the skeletal morphology and limb mobility of Ichthyostega were unlikely to have made some of the recently described Middle Devonian trackways10.
Early tetrapods, and the fish that gave rise to them, were
originally interpreted as being terrestrially capable animals with
load-bearing fins or limbs11, 12, 13.
Since the 1990s, however, new fossil discoveries and anatomical
interpretations have demonstrated that the first limbed vertebrates were
primarily aquatic in habit and that limbs evolved before the ability to
‘walk’ on land1, 2.
More recently, work has suggested that hindlimb-powered locomotion
first evolved in sarcopterygian fish, well before the origin of
digit-bearing limbs or terrestriality14; this model implies that a muscularly supported pelvis and sacrum are not compulsory for fin/limb–substrate interactions10. Others have even unconventionally proposed that some early tetrapods may have been more seal-like in their mode of locomotion3, 4,
rather than moving in a primitively salamander-like fashion. This
apparent conflict surrounding the timing of events that gave rise to
modern tetrapod locomotory styles has left our understanding of the
evolution of terrestriality uncertain.
To illuminate the evolution
of early tetrapod locomotion, we conducted a computer-aided assessment
of limb joint mobility in one of the best known Devonian tetrapods, Ichthyostega. To achieve this goal, we used micro-computed tomography (μCT) to scan suitable Ichthyostega specimens, created a digitally rendered three-dimensional skeletal model (Fig. 1),
and quantified maximum range of motion in the shoulder, elbow, hip and
knee in three orthogonal planes of movement. To interpret joint mobility
in a locomotor context, we compared the data of Ichthyostega
with those of five morphologically and phylogenetically distinct modern
tetrapod analogues with varying joint morphologies and locomotion
behaviours. These include a salamander (Ambystoma tigrinum), crocodile (Crocodylus niloticus), platypus (Ornithorhynchus anatinus), seal (Halichoerus grypus) and otter (Lutra vulgaris).
Moreover, we validated our methodology through dissection and joint
manipulation to determine the effect of soft tissues (or lack thereof)
on joint mobility (see Supplementary Information).
Figure 1: Three-dimensional reconstruction of Ichthyostega from μCT scan data.
a, Anterolateral view. b, Dorsal view. c, Lateral view. d,
Ventral view. The forelimbs and hindlimbs are shown in their resting
pose from which ranges of motion were calculated. A list of the
specimens used to create the model and the procedure followed for model
construction can be found in Supplementary Information, as can a comparison with the most recent two-dimensional reconstruction presented in ref. 4. Scale bar, 10cm.
Data from the hindlimb demonstrate that the hip joint in Ichthyostega
has a comparable degree of mobility, in terms of flexion/extension and
adduction/abduction, to that of the modern tetrapods. However, unlike
the modern tetrapods, the hip joint of Ichthyostega has a minimal degree of long-axis rotation (pronation/supination) capacity (Fig. 2a,
but note that the seal, whose hindlimb is modified as a flipper, has a
reduced range of long-axis rotation in comparison with the other modern
taxa). When range of mobility is partitioned into positive (increasing
angle between limb and girdle) and negative (decreasing angle between
limb and girdle) angular movements (Fig. 3a), the hip joint of Ichthyostega shows a relatively equal distribution of mobility, with the pattern approaching that seen in the modern tetrapods (see Supplementary Table 5); however, there is somewhat more abduction capacity. In terms of knee joint movements, Ichthyostega displays the most restricted mobility in flexion/extension (see Supplementary Table 6),
but no discernible differences were recovered for the other two planes
of movement, presumably because soft tissues rather than osteology are
primary limits on knee mobility, as in many other tetrapods.
Figure 2: Maximum ranges of mobility in the limb joints of Ichthyostega and five modern tetrapod analogues.
a, Hip joint. b, Shoulder
joint. Mobility was examined in three orthogonal planes of movement
including flexion/extension, adduction/abduction and
pronation/supination (or long-axis rotation). The most obvious
difference between Ichthyostega and the modern tetrapods analysed
is a distinct lack of long-axis rotation. A validation test of the
method used to calculate range of mobility can been found in Supplementary Information.
Figure 3: Partitioned range of mobility in the hip joint and shoulder joint of Ichthyostega.
a, Hip joint mobility partitioned into positive and negative angular movements. b, Movement of the hip in flexion/extension. c, Movement of the hip in adduction/abduction. d, Shoulder joint mobility partitioned into positive and negative angular movements. e, Movement of the shoulder in flexion/extension. f,
Movement of the shoulder in adduction/abduction. Asterisks indicate the
resting pose. Specific details of the method used to calculate joint
range of mobility are provided in Supplementary Information, as are animations of maximum range of mobility in the shoulder and hip of Ichthyostega. Scale bars, 10cm.
The hip joint in Ichthyostega forms a condyloid-like
articulation with greatly enlarged dorsal and ventral bony buttresses
surrounding an anteroventrally-to-posterodorsally elongated acetebulum13.
In addition to this, the femoral head is boomerang-shaped with a large
ventral intertrochanteric fossa enveloping the ventral bony buttress of
the acetabulum, forming a locking mechanism. This type of hip morphology
permits the femur to rock along the primary and secondary axes of the
acetabulum but prevents any major long-axis rotary movements. Because
the primary axis of the acetabulum (and associated femoral head) in Ichthyostega
is tilted anteriorly, movement of the hindlimb would have occurred at
an angle about 45° from the main horizontal axis of the body.
Consequently, the hindlimb would primarily have moved in an
anteroventral-to-posterodorsal arc during hip extension and an
anterodorsal-to-posteroventral arc during hip adduction (Fig. 3b, c).
The
limited range of hip long-axis rotation, in combination with a joint
offset of about 45° from the horizontal, implies that the plantar
surface of the pes in Ichthyostega was unable to contact the
substrate. In particular, the femur would have been prevented from
attaining a horizontal orientation and the pes would not have been
capable of pointing anteriorly, a limb pose conventionally considered
plesiomorphic for terrestrial tetrapods15, 16 (see Supplementary Figs 5 and 6).
This means that the pelvis could not have been lifted free of the
ground and that the hindlimbs were more critical during swimming, with a
more passive or stabilizing function during land/substrate movement
(analogous to phocid seals17). This proposed model of hindlimb movement in Ichthyostega is in accordance with the development of broad, paddle-shaped, distal limb bones and expanded pedes1.
It is also further supported by a reduced range of flexion/extension in
the knee, which is an essential component of terrestrial locomotion in
living tetrapods18, 19, 20, 21.
With respect to the forelimb, the shoulder joint in Ichthyostega has the most restricted range of angular motions in all three planes of movement (Fig. 2b),
with the most striking characteristic again being a distinct lack of
long-axis rotation (pronation/supination). Partitioning the range of
motion into positive and negative angular movements further reveals that
the shoulder joint in Ichthyostega is primarily restricted to negative angular movements, with the majority of mobility occurring in flexion and adduction (Fig. 3d). In contrast to Ichthyostega, the modern tetrapods examined show appreciable shoulder mobility in all three planes of movement (Fig. 2b) and a more equal distribution between positive and negative angular movements (see Supplementary Table 3). Elbow joint mobility in Ichthyostega
is, as far as can be judged from the ulna articulation, comparable to
that in the modern tetrapods. It is relatively flexible in all degrees
of freedom and shows a pattern intermediate between more sprawling
animals and those that use more upright limb postures (see Supplementary Table 4).
The restricted range of shoulder mobility in Ichthyostega is primarily the product of an anteroposteriorly elongated and dorsoventrally flattened glenoid fossa and humeral head13.
As with the hip, this type of joint morphology produces a
condyloid-like joint articulation, permitting flexion/extension and
adduction/abduction but preventing humeral long-axis rotation. Further
to this, the glenoid fossa in Ichthyostega is somewhat twisted
along its primary axis, with its anterior portion facing ventrally and
its posterior portion facing dorsally. The morphology of the glenoid
fossa in Ichthyostega guides the forelimb to move in a slight
anteroventral-to-posterodorsal plane during shoulder joint flexion,
whereas during adduction it directs the forelimb to move in an inclined
plane from the vertical, causing the humerus to trend posteriorly (Fig. 3e, f). In addition to joint shape, the pectoral girdle of Ichthyostega
also has a large bony buttress surrounding the anterodorsal border of
the glenoid itself, further restricting movements in extension and
abduction.
Given that symmetrical gaits (for example lateral
sequence walking, trotting) require a large degree of limb retraction
and rotation, in addition to girdle rotation by means of bending of the
vertebral column15, 16, 18, 19, 20, 21, 22, 23, it is unlikely that Ichthyostega employed such gaits with its forelimbs. Indeed, the pattern of shoulder joint mobility in Ichthyostega, in combination with a rigid pectoral girdle and thorax (due to large overlapping ribs13)
and terrestrially ineffectual hindlimbs, indicates that the most likely
mode of forelimb movement on land/substrate involved synchronous
mudskipper-like ‘crutching’ motions24. This proposed locomotory behaviour for the forelimbs of Ichthyostega concurs with previous conjectures3, 4
and is further supported by highly developed elbow extensor musculature
(implied by large dorsally extending olecranon processes)9
attached to a relatively mobile elbow joint. In addition to
land/substrate movement, however, the large amount of shoulder adduction
and elbow extension in the forelimb of Ichthyostega would have enabled both station-holding and lifting of the head out of the water to breathe and potentially feed25.
On the basis of our study of limb joint mobility, combined with rib and vertebral morphology4, 13, we conclude that Ichthyostega
could not use ‘normal’ quadrupedal gaits. The ability to rotate the
humerus and femur longitudinally and use symmetrical gaits (for example
lateral sequence walking) must have evolved in other early tetrapod
species. Given that a similar type of shoulder and/or hip joint
morphology presents itself in some other early tetrapod species2, 8, 26, limited limb joint mobility—particularly long-axis rotation—may have been more widespread (see Supplementary Information).
However, the use of symmetrical gaits, or lack thereof, in other early
tetrapods would need to be tested through further three-dimensional
investigations of both the limbs and axial skeleton. Nevertheless,
long-axis rotation capacity was present in the fins of tetrapodomorph
fishes5, 6, 7, indicating that some tetrapods evolved through a phase of restricted shoulder8, 9
and hip joint mobility before acquiring the ability to perform rotary
motions and the associated locomotory behaviours that persist in extant
taxa.
In addition, our data indicate that the tetrapod forelimb
was the first to gain a role in land/substrate locomotion, with the
pelvis and hindlimb becoming robust more as a muscular and propulsive
adjunct to the tail for swimming and only later being exapted for
walking on land (contra ref. 14).
The divergent functional roles of early tetrapod limbs and the late
onset of hindlimb-powered land/substrate locomotion are consistent with
both the diminutive pelvic fins of tetrapodomorph fishes compared with
their pectoral fins, and with the genetic mechanisms controlling the
formation of fin and limb musculature. In particular, studies
demonstrate a distinct evolutionary lag between the developmental modes
of pectoral and pelvic fin musculature in bony fishes27, 28. Therefore, in addition to hip joint constraints, it is conceivable that Ichthyostega
did not yet have the pelvic musculature necessary for hindlimb-driven
land/substrate movement, but rather gradually transformed the existing
musculature from a more aquatic to a more terrestrial propulsive role.
Given our results, could an Ichthyostega-like early tetrapod have produced similar trackways to some of those recently described from the Middle Devonian10? All available evidence from limb joint mobility and axial anatomy4, 13
indicates that such animals could not have made symmetrical gait ‘foot’
prints. In particular, these early tetrapods probably lacked the
necessary rotary motions in their limbs (and perhaps lateral flexion of
the vertebral column) to push the body off the substrate and progress
using alternating limb movements. Maybe as yet unknown tetrapod species
(or known taxa that currently lack postcranial material) with different
joint mobility and axial anatomy made these traces; available data
cannot yet answer this conundrum. Nonetheless, the analysis presented
here supports the possibility that Ichthyostega-like animals
could produce synchronous (parallel) trackways, as our findings indicate
that such a trace should consist of a series of bilateral forelimb
impressions.
A large selection of Ichthyostega specimens (see Supplementary Information), particularly focusing on postcranial material, and five modern analogues including a Tiger salamander (Ambystoma tigrinum; TNHC 17991), Nile crocodile (Crocodylus niloticus; RVC ‘Flunch’ specimen in J.R.H.’s research collection), Platypus (Ornithorhynchus anatinus; USNM 221110), Grey seal (Halichoerus grypus; UMZC K.7943) and European otter (Lutra vulgaris; UMZC K.2768), were scanned with a medical CT or μCT
(depending on size; settings varied widely) to capture
three-dimensional bone geometry. All files were segmented in Mimics
software (Materialise), exported as high-resolution .stl files and then
reconstructed in the three-dimensional modelling, animation and
rendering software Autodesk 3D Studio Max. Because articular cartilage
is no longer present on the bones of Ichthyostega, all joints in
the extant taxa were also reconstructed without any articular cartilage,
ensuring that modelling conditions were kept consistent; however, we
investigate this assumption further below.
Model alignment
All animals and models (Supplementary Fig. 1)
were articulated in a stepwise fashion. First, the skull and vertebral
column of each animal studied were aligned in a straight line; however,
because of the ventrally directed sacral ‘hip fan’ in Ichthyostega,
the tail was left sloping ventrally. The pectoral and pelvic girdles
were then positioned. Unlike the pelvic girdle, which attaches to the
sacrum, the placement of the pectoral girdle is slightly more
subjective. The salamander, platypus and crocodile were all scanned as
cadaveric specimens; positioning of the pectoral girdle was therefore
fairly straightforward. The seal and otter, however, were scanned as
disarticulated skeletons; in this case, the pectoral girdle (or scapula)
was considered to sit over the anterior ribs with the straight edge of
the scapular blade pointing dorsally and not extending above the level
of the neural spines. In Ichthyostega the pectoral girdle was
aligned with an impression of the left cleithrum on the thoracic ribs of
MGUH VP 6115. The limbs were then positioned and their centres of
rotation and joint axes aligned (see below).
Limb joint axes
With
respect to the shoulder and hip, spheres were placed in the glenoid and
acetabulum to estimate each joint’s centre of rotation, assuming a
ball-and-socket (three degrees of freedom) joint. The humerus and femur
were then positioned in an anatomical resting pose, which was determined
by moving the bones until they were gently resting—with no bone
contact—in their respective sockets/spheres. As a result, the resting
pose inherently accounts for a certain thickness of soft tissue (for
example articular cartilage). However, because of the elongated and
narrow glenoid and acetabulum in Ichthyostega, the centre of
rotation in the shoulder and hip was determined by first aligning and
scaling a cylinder along the primary axis of the glenoid and acetabulum
and then aligning a sphere, with the same cross-sectional diameter, to
the cylinder’s centre of rotation; the humerus and femur were then
positioned into a resting pose, and the size of the sphere was adjusted
to ensure that it entirely enveloped the humeral or femoral head. In
addition, because the glenoid in Ichthyostega twists along its
primary axis, a plane was also placed through the glenoid to estimate,
more realistically, the orientation of the humerus.
After
establishing each joint’s centre of rotation, the three orthogonal axes
of each sphere were aligned to the anatomical axes of the humerus and
femur, first by determining the long axis of the bone, and then
orienting the craniocaudal axis and dorsoventral axis (in sprawling
animals) or mediolateral axis (in parasagittal animals). Then the
centres of rotation and joint axes of the humerus and femur were aligned
with their respective spheres (Supplementary Fig. 2).
The same procedure was followed for aligning the antebrachium (ulna and
radius), manus, crus (tibia and fibula) and pes, but this time spheres
were placed on the distal ends of the humerus and femur to estimate
joint axes in the elbow and knee or the ulna/radius and tibia/fibula to
estimate joint axes in the wrist and ankle (which were not examined in
this study, particularly because of the absence of a manus and the lack
of a clear ankle joint in Ichthyostega).
Bone segments
To
reduce processing time, the high-resolution Autodesk 3D Studio Max
models were partitioned into two files, one composed of the pectoral
girdle and left forelimb and another of the pelvic girdle and left
hindlimb. Individual bones were grouped to create four segments: the
girdle segment (pectoral or pelvic), followed by the proximal limb
segment (humerus or femur), the distal limb segment (antebrachium or
crus) and finally the manus or pes segment. However, because the ulna
and radius in Ichthyostega do not articulate in close proximity
to each other, and the radial condyle is partly missing, the distal
segment of the forelimb in Ichthyostega consists solely of the
ulna. To preserve positional relationships, segments (and associated
spheres) were linked hierarchically such that if a segment was moved,
all associated distal segments moved in the same direction.
SIMM model
To
quantify maximum range of movement, each limb model was recreated in
the biomechanical modelling software SIMM (Musculographics, Inc.)29.
To build a SIMM model, each bone’s positional relationship in a
Cartesian coordinate system was determined in Autodesk 3D Studio Max.
First, the centre of rotation or pivot point of the girdle segment was
aligned to x,y,z coordinates of 0,0,0. The x,y,z
coordinates of the proximal segment were recorded and then the pivot
point of the proximal segment (and associated sphere) was realigned to
0,0,0, such that it was overlapping the girdle segment. This procedure
was repeated for the distal segment and then finally the manus/pes
segment. The joint axes were then determined using each segments
associated sphere. To do this, the pivot point of each sphere was moved a
short distance along its local xaxis (craniocaudal direction) and then the new x,y,z
location (compared with 0,0,0) was recorded. The pivot point was then
returned to 0,0,0 and the same procedure was repeated for the local yaxis (dorsoventral or mediolateral) and zaxis
(long axis of bone). The coordinates of the joint axes were then
normalized by dividing each by its standard deviation. Finally, all
0,0,0 aligned segments were exported as .stl files to create a ‘bone
file’ and the positional relationships were combined to construct a
linked ‘joint file’ (.jnt).
Range of movement
In SIMM, each joint was modelled with three degrees of freedom: adduction/abduction (about the xaxis), flexion/extension (about the yaxis) and pronation/supination (that is, long-axis rotation; about the zaxis) (Supplementary Fig. 2).
The terms used to describe movement in this study are specific to joint
angles rather than net limb/segment movement during active locomotion
(for example, protraction/retraction, elevation/depression). In terms of
angular movements, the resting pose of each segment was set to a
starting angle of 0°. Movements in adduction, flexion and pronation were
considered to be negative angular movements (decreasing angle between
segments) and ranged from a minimum of 0° to a maximum of −180°.
Conversely, movements in abduction, extension and supination were
considered to be positive angular movements (increasing angle between
segments) and ranged from a minimum of 0° to a maximum of +180° (Supplementary Fig. 2).
Finally, to obtain the maximum range of motion three assumptions were
followed: first, joints were only permitted to move along one plane at
any time (that is, movements were uncoupled); second, joints were
permitted to translate or slide within their presumed joint capsule30; and third, joints were moved in 5° increments until there was either bone-to-bone contact or the joint became disarticulated.
Institutional abbreviations
MGUH,
Geological Museum, Copenhagen; RVC, Royal Veterinary College, London;
TNHC, Texas Natural History Collections; UMZC, University Museum of
Zoology, Cambridge; USNM, Smithsonian Institution National Museum of
Natural History.
Clack, J. A.Devonian tetrapod trackways and trackmakers: a review of the fossils and footprints. Palaeogeogr. Palaeoclimatol. Palaeoecol.130, 227–250 (1997)
Shubin, N. H., Daeschler, E. B. & Jenkins, F. A., JrThe pectoral fin of Tiktaalik roseae and the origin of the tetrapod limb. Nature440, 764–771 (2006)
Ahlberg, P. E.Humeral homology and the origin of the tetrapod elbow: a reinterpretation of the enigmatic specimens ANSP 21350 and GSM 104536. Spec. Pap. Palaeontol.86, 17–29 (2011)
Niedzwiedzki, G., Szrek, P., Narkiewicz, K., Narkiewicz, M. & Ahlberg, P. E.Tetrapod trackways from the early Middle Devonian period of Poland. Nature463, 43–48 (2010)
King, H. M., Shubin, N. H., Coates, M. I. & Hale, M. E.Behavioural evidence for the evolution of walking and bounding before terrestriality in sarcopterygian fishes. Proc. Natl Acad. Sci. USA108, 21146–21151 (2011)
Reilly, S. M. & Elias, J. A.Locomotion in Alligator mississippiensis: kinematic effects of speed and posture and their relevance to the sprawling-to-erect paradigm. J. Exp. Biol.201, 2559–2574 (1998)
Jayne, B. C. & Irschick, D. J.Effects of incline and speed on the three-dimensional hindlimb kinematics of a generalized iguanian lizard (Dipsosaurus dorsalis). J. Exp. Biol.202, 143–159 (1998)
Ashley-Ross, M. A., Lundin, R. & Johnson, K. L.Kinematics of level terrestrial and underwater walking in the California newt, Taricha torosa. J. Exp. Zool.311A, 240–257 (2009)
Jenkins, F. A., Jr & Goslow, G. E., JrThe functional anatomy of the shoulder of the savannah monitor lizard (Varanus exanthematicus). J. Morphol.175, 195–216 (1983)
Pridmore, P. A.Submerged walking in the epaulette shark Hemiscyllium ocellatum (Hemischyllidae) and its implications for locomotion in rhipidistian fishes and early tetrapods. Zoology98, 278–297 (1994)
Markey, M. J. & Marshall, C. R.Terrestrial-style
feeding in a very early aquatic tetrapod is supported by evidence from
experimental analysis of suture morphology. Proc. Natl Acad. Sci. USA104, 7134–7138 (2007)
Delp, S. L. & Loan, J. P.A graphics-based software system to develop and analyze models of musculoskeletal structures. Comput. Biol. Med.25, 21–34 (1995)
We thank J. Molnar for assistance with segmentation, model
construction, and movie generation; L. Witmer for access to platypus
scan data; Digimorph for access to salamander scan data (National
Science Foundation grant IIS-9874781 and IIS-0208675 to T. Rowe); M.
Lowe for collections support at the University Museum of Zoology,
Cambridge; G. Cuny for access to collections housed in the Geological
Museum at the University of Copenhagen; J. Rankin for musculoskeletal
modelling support; and P. Ahlberg for commenting on an earlier draft of
this manuscript. For access to μCT scanning
equipment in their care, we also acknowledge R. Abel, C. Martin and A.
Heaver. This research was supported by Natural Environment Research
Council grants NE/G005877/1 and NE/G00711X/1.
Department of Veterinary Basic Sciences and Structure and
Motion Laboratory, The Royal Veterinary College, Hawkshead Lane,
Hatfield AL9 7TA, UK
Stephanie E. Pierce &
John R. Hutchinson
University Museum of Zoology, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
Stephanie E. Pierce &
Jennifer A. Clack
Contributions
All authors contributed to project concept and design. S.E.P.
collected and analysed the data and wrote the manuscript, including main
text, figures and Supplementary Information. J.A.C. and J.R.H. provided a critical review of all aspects of manuscript development. All authors approved the final draft.
Competing financial interests
The authors declare no competing financial interests.
This
proof contains Supplementary Text, which includes details of how the 3D
model of Ichthyostega was constructed, Supplementary References,
Supplementary Figures 1-6 and Supplementary Tables 1-6.
![Three-dimensional reconstruction of Ichthyostega from [mgr]CT scan data.](https://lh3.googleusercontent.com/blogger_img_proxy/AEn0k_v5uHjqv3WbK9ecEP_afyOPE8BObEpTUnzfi7y891ghNcwUPypM9sUPH4UtNPWb67n2Xw6Qxk91WqIH9qO7ftnW2DZJUJjIUYWvu_LmN0nEJff5kAF_tFhZh-2UPHq2eTmHwGcRh39HmSsGS9AZM68j=s0-d "Figure 1: Three-dimensional reconstruction of Ichthyostega from [mgr]CT scan data.")
![Three-dimensional reconstruction of Ichthyostega from [mgr]CT scan data.](https://lh3.googleusercontent.com/blogger_img_proxy/AEn0k_u9bvaXUzJD1OPvP96cKZfmEpMk6VD2r2aYEUwkWRnoh-PcE5w9HAWYgtgB2FMzeoRLNeQi7hhwBdxWTbIj12hcpmX73QgaLCsbaw1VoKa9l7OQj2HHMcau6ewHZ8Y5tjzwwvN8BMO5XpE4ggniikQahtdFPps6=s0-d)
