MARGINALIA
A Palaeontological Puzzle Solved?
Keith Thomson
The Devonian fossil Palaeospondylus gunni is one of
paleontology's enduring enigmas. At 20 to 60 millimeters in length,
it is just large enough to show that it is a fish, but not much
more. Within 10 years of its discovery by two amateur collectors,
the cousins Marcus and John Gunn, hundreds of specimens had been
collected from the Achannaras slate quarry in Caithness, Scotland.
Equally quickly, rival scholars eagerly and acrimoniously assigned
it to every possible class and order. By 1903, the debate became so
heated that Bashford Dean (curator both of Ichthyology and
Herpetology at the American Museum of Natural History and of Arms
and Armor at the Metropolitan Museum of Art) concluded in
frustration: "Professor [Thomas Henry] Huxley, the astute
morphologist, is perhaps to be felicitated in having had no traffic
with it." He urged that it be put aside "where it will do
the least harm."
Of course, Dean was ignored. Retreat is unusual among
paleontologists, who always love a puzzle and rarely back away from
a good fight. And now it seems that the problem with Palaeospondylus
was not just in the fossils but in the pal(a)eontologists. Most
early authors were determined to make Palaeospondylus into something
very important from the evolutionary sense: an ancient kind of
jawless fish, a new line of jawed fish, or a tantalizing
"missing link" between ancient placoderms and sharks. For
the purpose of their arguments, therefore, the greater the
mystery—the more different it was from other fishes—the better.
Something New Out of Achanarras
Palaeospondylus gunni, so named by Ramsay Heatland Traquair
of Edinburgh in 1890 (after its discoverers and prominent backbone),
is abundant at Achanarras Quarry but is found nowhere else except
for two nearby localities where a very few additional specimens have
turned up. Not only is it minuscule in size, but its structure,
insofar as one can make it out, seems unlike that of any known
creature, living or fossil. It has a strange basket-like apparatus
on its snout but no teeth, a well-developed vertebral column but no
fins. In a 1992 Marginalia essay in which I reviewed the
sadly inconclusive story of this little fossil, my own meager
contribution was an allometric study of body proportions showing
that it was a larval form. But its anatomy and taxonomic position
were unresolved.
Oddly enough, the possibility that Palaeospondylus is a
larva had been mooted early in the case. Huxley, in famously having
nothing to do with it, dismissed it as a "baby
Coccosteus" (a placoderm arthrodire, one of those
weird extinct forms with a large head articulated onto massive neck
armor). Dean himself noted the change of head-to-body proportions
with size so typical of immature forms of vertebrates. J. W. Dawson
(principal of McGill University) thought it might be a
"primitive tadpole." Professor Graham Kerr of Glasgow
suggested that it was a larval lungfish. However, interpretation as
a larva was not taken seriously again until 1980, when Peter Forey
and Brian Gardiner at the Natural History Museum in London repeated
the suggestion. Now a new study shows that Palaeospondylus
is definitely a larval lungfish, and we can even be pretty sure that
the corresponding adult was the famous Dipterus
valenciennesi, equally abundant at Achanarras. It is
instructive to examine why it has taken so long to get this far.
The Technical Approach
One of the early major contributors to making
Palaeospondylus a bigger puzzle than it needed to be was
Oxford professor William Sollas. He perfected a serial grinding
technique and apparatus for using thin sections of fossils to create
enlarged wax-plate reconstructions. Fossil after fossil was
dissected in this way by Sollas and his daughter Igerna at
Cambridge, including a graptolite, a Triassic dicynodont reptile and
a Cretaceous sea urchin. And, in 1903, Palaeospondylus.
They revealed a wealth of anatomical detail not visible with the
microscope alone. But Sollas also led everyone down a wrong track.
Unable to homologize the head structures he found with those of
other fishes, he gave each its own new name—in Greek. Ampyx,
tauidion, hemidome and gammation are some of the most memorable. The
result was that everyone then accepted that the anatomy really was
uniquely different from that of other vertebrates.
A couple of years ago I discovered that all of Sollas's material was
still in the Oxford University Museum. He had sectioned several
specimens at about 0.25-millimeter intervals and photographed the
cut and polished surfaces using superb lenses, so that each was
preserved as a glass-plate negative. Naturally I had the idea that
modern computer manipulations of his sections would give us a better
reconstruction of the anatomy. My assistant Bethia Thomas set to work.
But I was wrong. Sollas had captured just about every detail that
was available. However, postdoctoral fellow Mark Sutton had been
working with my colleague Derek Siveter on magnificent computer
reconstructions of far more minutely sectioned Silurian
invertebrates. So I asked Mark if he would like to have a go at
Palaeospondylus, making new sections at only 30-micron
intervals. The Natural History Museum in London gamely offered up
three specimens to be sacrificed—eventually to reappear in
virtual form. This time the result was amazing. One of the specimens
was preserved relatively uncrushed and undistorted, and at last we
had a new look at its structure. There were the tauidion, gammation
et cetera in all their glory. But still the question
remained: how to interpret such a set of structures apparently
unlike those in any known fish?
Head Case
The possibility that Palaeospondylus was a larval form had
always been rejected because of the well-formed vertebral column and
what seemed to be a good bony skeleton. A larval skeleton should
have been cartilaginous and therefore would not have survived.
Unfortunately, our new sections confirmed that, as Sollas had
already discovered, no histological details are preserved in the
bituminized material (although, significantly, cellular details are
preserved in the bones of other, definitely adult, fishes from
Achanarras). But several Palaeospondylus specimens show
evident cartilage and even connective tissue in the curious
apparatus at the front of the head. Some retain an outline of the
body. So the fact that the "bones" were well preserved did
not necessarily prove that they were made of "bone."
A prominent feature of the head of every specimen is a pair of
strange rods, the occipital lamellae, projecting from the back of
the cranium alongside the vertebrae. In our new reconstruc-tion, the
shape of the articular facets showed that (as Dean had guessed) in
life they were oriented backward and downward. They are identical
with the cranial ribs found elsewhere only in lungfish. Kerr had
pointed that out in 1930, but no one had listened until Forey and
Gardiner revived his suggestions.
The next breakthrough came with the curious apparatus on the snout
that had confused so many authors, including the most recent ones. A
reasonable explanation was that it had something to do with the
nasal apparatus: either the complex nasohypophysial structure found
in lampreys and hagfish or the nasal capsules of a gnathostome.
However, I recalled that in 1879 Alexander Agassiz had described the
development of the gar Lepisosteus, a primitive teleost
that has an almost identical feature to the anterior structure in
Palaeospondylus. It is an attachment organ, a larval
adaptation lost in later life.
If the rostral apparatus is identified as a larval attachment organ,
interpretation of the rest of the head falls neatly into place. The
hemidomes are the nasal capsules and the computer images show that
Sollas's hemidome septa were their perforated dorsal walls, just as
in modern larval lungfishes. The ampyx is the paired premaxillae,
and the tauidion is the vomer. In that case, the big, chunky
gammation has to be the palato-quadrate. And the first
post-branchial plate is the dorsal part of the hyoid arch. The new
reconstructions also show that the enigmatic anterior trapezoidal
bar articulates with the front of the gammation. If the gammation is
the palato-quadrate, then the trapezial bar is possibly a rudiment
of Meckel's cartilage—the embryological basis of the lower
jaw. Suddenly, nothing present on the fossil was unaccounted for and
it was all consistent with Palaeospondylus being a larval lungfish.
The Oldest Vertebrate Larva
One of the difficulties about Palaeospondylus has always
been that obvious vertebrate features such as the dermal skeleton
are missing. However, Palaeospondylus also lacks the teeth,
proper jaws and all the gill apparatus behind the first arch. It has
rudiments of the limb girdles, but no fins. We also have to explain
why Palaeospondylus specimens do not become progressively
more similar to adult lungfish as they become bigger (an early
argument against larval status).
All this makes sense if Palaeospondylus is a true larva
with a sharp metamorphosis in the life history, rather than the sort
of juvenile that slowly morphs into an adult. As a true larval
stage, it would require special adaptations—to compensate, for
example, for the absence of teeth and jaws. Among those is,
obviously enough, the anterior attachment organ. We may then
suggest, although we cannot prove, that Palaeospondylus was
a larval form spending its life in shallow waters, attached to
either a substrate or a plant. Like larval Lepisosteus (and
modern larval lungfish where the attachment organ is on the throat),
it lived partially from the reserves in the yolk sac, and partially
as a detritus feeder on the attached surfaces.
There is only one species of adult lungfish in the Achanarras
beds—Dipterus valenciennesi, a handsome fish
reaching to 30 centimeters or more—but it is never found
smaller than about 60 millimeters. Somewhere there must exist very
young Dipterus fossils or very old Palaeospondylus
that would settle the question. Or are there yet other explanations
still waiting to be explored? The anterior attachment organ might be
consistent with Palaeospondylus being a parasite. In which
case it would not represent the oldest known fossil vertebrate
larva, but the oldest known vertebrate parasite. Or even both. One
of the things that keeps paleontologists (and palaeontologists)
going is the possibility that just around the corner is a deposit
with some superb new material that will answer all our prayers. Or
start another controversy.