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Lungfish fingers and bird fingers
An interesting paper came out last year in a journal that probably not many
paleontologists read:
Zerina Johanson, Jean Joss, Catherine A. Boisvert, Rolf Ericsson, Margareta
Sutija & Per E. Ahlberg (2007): Fish Fingers: Digit Homologues in
Sarcopterygian Fish Fins, Journal of Experimental Biology (Mol Dev Evol)
308B, 757 -- 768 (published online 11 September 2007)
Abstract:
A defining feature of tetrapod evolutionary origins is the transition from
fish fins to tetrapod limbs. A major change during this transition is the
appearance of the autopod (hands, feet), which comprises two distinct
regions, the wrist/ankle and the digits. When the autopod first appeared in
Late Devonian fossil tetrapods, it was incomplete: digits evolved before the
full complement of wrist/ankle bones. Early tetrapod wrists/ankles,
including those with a full complement of bones, also show a sharp pattern
discontinuity between proximal elements and distal elements. This suggests
the presence of a discontinuity in the proximal-distal sequence of
development. Such a discontinuity occurs in living urodeles, where digits
form before completion of the wrist/ankle, implying developmental
independence of the digits from wrist/ankle elements. We have observed
comparable independent development of pectoral fin radials in the lungfish
*Neoceratodus* (Osteichthyes: Sarcopterygii), relative to homologues of the
tetrapod limb and proximal wrist elements in the main fin axis. Moreover, in
the *Neoceratodus* fin, expression of Hoxd13 closely matches late expression
patterns observed in the tetrapod autopod. This evidence suggests that
*Neoceratodus* fin radials and tetrapod digits may be patterned by shared
mechanisms distinct from those patterning the proximal fin/limb elements,
and in that sense are homologous. The presence of independently developing
radials in the distal part of the pectoral (and pelvic) fin may be a general
feature of the Sarcopterygii.
The core of the paper is development genetics of the pectoral fins of the
Australian lungfish.
One conclusion is that three parts can be distinguished in the
cartilaginous/endochondral skeleton of the pectoral extremities of any
sarcopterygian (the dermal skeleton being fin rays and scales):
- the (metapterygial) axis: humerus, ulna, ulnare, and 0 to at least 11 more
elements (0 in rhizodonts and tetrapods, 1 in *Latimeria* and
*Eusthenopteron*, 2 in *Tiktaalik*, 11 in the figured specimen of
*Neoceratodus*). This forms as a continuous spike of prechondral
(pre-cartilage) cells in *Neoceratodus* that segments itself while it grows.
In *Neoceratodus* (and, judging from morphology, other lungfishes and
porolepiforms) it reaches all the way to the tip of the fin.
- 1 to 3 "nonindependent preaxial radials" (perhaps homologous to part of
the mesopterygium of non-sarcopterygian gnathostomes, but that's just my
guess): one articulating with the humerus and consisting of the radius,
radiale, and presumably centrale 1, distal precarpal, and prepollex; one
(absent in *Neoceratodus*) articulating with the ulna and consisting of the
intermedium (and presumably centralia 4 and 2 & 3); and one that articulates
with the ulnare and is only present in *Eusthenopteron* among the taxa
Johanson et al. mention (unless it is centrale 3, but that's unlikely and
was just my guess in the first place). One might think that the axis simply
branches, so that radius and ulna are formed at the same time, but that's
not how it works in *Neoceratodus*: the radius appears, without a connection
to humerus or ulna, after the humerus, ulna, and ulnare have already started
to form. The only "nonindependent preaxial radial" *Neoceratodus* has
(radius and so on) forms, like the axis, as a continuous spike that segments
while it grows.
- the "independently developing radials" which are found on both sides of
the axis in taxa with a long axis (lungfishes, porolepiforms, to a lesser
extent *Tiktaalik*) and mostly distal to the axis in taxa with a short axis
(coelacanths, rhizodonts, *Eusthenopteron*, tetrapods). They are very
variable (between taxa) in number, size, shape, and arrangement and do not
have a consistent relationship with elements of the axis of the
nonindependent preaxial radials. In *Neoceratodus* they start forming after
the axis has grown to at least 6 elements beyond the ulnare, and, just
before they appear, Hoxd13 is expressed, which is exactly what happens just
before the appearance of digits in tetrapods; it is not expressed in the
axis. After appearing, they grow and segment (like the axis and the
nonindependent preaxial radials), and then they form joints with the nearest
elements of the axis.
Before this, in the lengthy introduction, Johanson et al. compare the ankles
of *Acanthostega*, *Ichthyostega*, and the Carboniferous anthracosaur
*Proterogyrinus* (which already has the usual 5 toes). Attention is directed
to the fact that digits + metapodials seem to have evolved before the
centralia were complete: *Acanthostega* has 3 metatarsals articulating
directly with the fibulare; it has an intermedium, a tibiale, and distal
tarsals for 4 or 5 of the remaining 5 metatarsals, and a hole in between
that may have held 1 or 2 unossified centralia, but not 4. *Ichthyostega*
has a completely ossified ankle with a single centrale (and 2 metatarsals
articulating directly with the fibulare, while the remaining 5 metatarsals
have distal tarsals). *Proterogyrinus* has 3 small centralia and no
metatarsals articulating directly with the fibulare. They also point out
that in salamanders "digits develop as individual buds, before the
condensation of the mesopodium [carpus/tarsus]. For example, in
*Desmognathus aenus*, metacarpal II is the first element of the autopodium
[metapodials + phalanges] to condense and chondrify [become cartilaginous]
and is well separated from the only other limb condensations [that exist at
that time], the radius and ulna" (p. 759); in *Ambystoma mexicanum*,
metacarpal I and digit I appear first. Johanson et al. propose that -- see
above -- the digital rays (digits, metapodials, distal carpals/tarsals) are,
in ontogeny and phylogeny, independent of the more proximal elements, that
the distal carpals/tarsals are (in salamanders and stem-tetrapods) proximal
outgrowths of the metapodials, and that the centralia are evolutionarily
more recent outgrowths of the intermedium and radiale/tibiale.
In amniotes and frogs, the limb chondrifies strictly from proximal to
distal, while in salamanders this is not the case (see above). The
traditional assumption is therefore that the salamander condition is
derived. Johanson et al. turn this on its head, based on the evidence from
the development of lungfish fins and from the morphology of tetrapods in
general and *Acanthostega* and *Ichthyostega* in particular: the salamander
condition is plesiomorphic, and the frog + amniote condition is (twice
independently) derived. I wonder if that happened because most frogs and
amniotes use their limbs for terrestrial locomotion soon after the limbs are
formed, so there's no point in regulating a complicated sequence of
chondrification, while salamander larvae grow limbs early and leave the
water (if at all) late...
From pp. 765f.: "The earliest phase of tetrapod evolution shows a
gradual elaboration of the mesopodium after the establishment of the digital
arch [...]. Furthermore, this elaboration involves the addition of new
centrals and distal carpals/tarsals, elements that lie immediately on either
side of the transverse 'discontinuity line' [...] across which it is
impossible to trace one-to-one relationships between elements. This suggests
that the elaboration may have comprised two mirror-image processes of
terminal addition of new elements, one at the distal end of the limb proper,
producing centrals, and one at the proximal ends of the digits [or rather
metapodials], producing distal carpals/tarsals [...]. The fossil evidence
thus implies a degree of digit independence in early tetrapods. We argue
that the early establishment of digits during urodele limb development is a
retained primitive character that has been lost independently in anurans and
amniotes. We note, however, that Cohn et al. [...] questioned the occurrence
of branching mechanisms in the more distal elements of the amniote limb
skeleton. A piece of foil placed within a developing chick wing directly in
front of the most recently condensing element failed to prevent more distal
elements from forming, suggesting some degree of independence of the latter
from the former. Independence of the digits may thus be a general feature,
masked by the proximal-to-distal chondrification sequence within the amniote
paddle." (In amniotes and frogs the limb bud assumes a paddle shape while
the hand/foot forms; that's not the case in salamanders.)
Of course, as Johanson et al. point out, this moreover fits the
well-known fact that the digits ossify before the carpus/tarsus in a wide
variety of tetrapods, including many amniotes as well as fossil
temnospondyls, seymouriamorphs and lepospondyls.
Johanson et al. go on to cite Fröbisch et al. (2007), who report
that the digits of the temnospondyl *Apateon* ossified in the salamander
sequence: first 1 and 2, then 3 and 4, and then (in the foot) 5. This was
originally taken as evidence of close relationship; it may be plesiomorphic
instead.
"These observations imply that the autopod [digits + metapodials]
evolved before the origin of tetrapods, represented by the more distal
region of the sarcopterygian fin, with the 'origin of digits' simply
representing a modest repatterning of this region rather than the origin of
a new structure." (p. 766) The authors also mention the correlation between
late-phase Hoxd13 expression and "radial formation" in the basal
actinopterygian *Polyodon* (Davis et al. 2007); that would mean that, rather
than us gaining digits, the teleosts have lost them.
In their last paragraph Johanson et al. discuss the "primary axis"
hypothesis, whose latest incarnation is Wagner & Larsson (2007). This
hypothesis says that digit IV is the tip of the (metapterygial) axis which
has assumed digit shape because it has grown into digit territory, and that
it is repeated on both sides to initiate the other digits. Wagner & Larsson
go so far as to suggest that digits I and/or II of salamanders, which (see
above) appear first, are in fact digit IV, with the lower-numbered digits
lost and the higher-numbered ones lacking homologues in frogs and
amniotes -- a frameshift much more massive than the one they suggest for
birds. Without mentioning this extreme, Johanson et al. disagree, "because
it does not seem to fit well with the palaeontological or molecular data"
(p. 767) explained above.
To recapitulate, there are as of 2007 three hypotheses on the origin of
digits, and Johanson et al. consider the first two more or less falsified:
- The digital arch: the metapterygial axis runs (forelimb example)
humerus-ulna-ulnare-distal carpal 4-dc3-dc2-dc1. The radius-radiale-who
knows what else branches off preaxially, and so does the intermedium, which
(if I understand it correctly) continues into centralia and digits I and II
of salamanders; dcV is a postaxial branch, and so are all metacarpals +
digits. Illustrated here
http://www.press.uchicago.edu/books/gee/shubin3.jpeg (ignore *Panderichthys*
and the gene expression patterns).
- The primary axis: the metapterygial axis runs
humerus-ulna-ulnare-dc4-mcIV-digit IV; its distal part is repeated to form
the other digits.
- Digits as "radials": the metapterygial axis runs humerus-ulna-ulnare and
then stops in tetrapods and rhizodonts, while it continues in other
sarcopterygians with elements that lack tetrapod homologs; the
radius-radiale-unspecified centralia and the intermedium-unspecified
centralia form independently; and so do the "radials".
Shubin (2002) discusses three modes of reducing the number of elements in
the hands and feet of salamanders:
- Truncation by paedomorphosis: elements are lost because they never form.
This applies to the absence of digits V (foot only), V + IV, or V + IV +
III, and probably to the rare appearance of centrale 3 (traditionally called
"mediale" in salamanders).
- "Fusion" by paedomorphosis: elements that form from a single cluster of
prechondral cells never separate. This applies to the "fusion" of distal
tarsals 4 and 5 (commonly seen in salamanders as inter- and intraspecific
variation), the "fusion" of distal tarsals 3 + 4 + 5 (same, but rarer), to
the rare separation of centrale 1 (traditionally called "element y" in
salamanders) and the distal tarsal of the prehallux, and to the (outside of
hynobiids) rare separation of the intermedium and centrale 4. One cannot
help but suspect that this also accounts for the "basale commune", the fact
that distal carpals/tarsals 1 and 2 are not known to ever separate in any
salamander. "The phylogenetic outcome of this is that patterns of
consolidation of elements involve neighboring elements that lie within one
of the three series of the mesopodium: the preaxial column, the central
series, and the digital arch. Condensations in these zones largely remain
distinct from one another and rarely fuse" (p. 25). In the terms of Johanson
et al., these are the first "nonindependent preaxial radial" (radius,
radiale, etc.), the second "nonindependent preaxial radial" (intermedium
etc.), and the "radials" -- with the only exception that Johanson et al. do
not postulate a connection between the distal carpals/tarsals, but adding
one does not seem to contradict the rest of their model.
- Actual fusion: elementsfirst form and then fuse. Apparently invariably,
they are from different "series". Centrale 2 and dc4 apparently fuse fairly
often, intermedium and ulnare rarely, and that basically was it.
In sum, more support for the model of Johanson et al..
And now I have finally waffled enough about lungfish and salamanders and can
go on to the birds: to the implications of that model on the frameshift
hypothesis (and, of course, at the same time on the BAND hypothesis).
If digit IV is not part of the metapterygial axis, we cannot safely use the
spatial relations between any digits on the one hand and the radius, ulna,
or any proximal or central carpals on the other hand as evidence for the
identity of any digit. Nor can we safely assume that digit IV must be the
first to chondrify; in amniotes that retain 5 digits as adults, it is in all
of the few cases that have been checked, but in salamanders it isn't. In the
absence of more convincing evidence, the most parsimonious option is of
course that the first digit to chondrify in the bird wing is digit IV, but
we can no longer assume that this alone, and/or its position vaguely
opposite the ulna, is stronger evidence than morphology.
I conclude that the only evidence for the frameshift hypothesis so far is,
surprisingly, fossil. It was presented at this year's SVP meeting; I'll post
the abstract later (this e-mail is long enough, and I should go to bed for a
change). But, while suggestive, this, too, is not a clincher (I think I'm
allowed to mention that I talked to the presenter, Jim Clarke, and we agree
it's all very confusing). If the digits really are independent of the
metapterygial axis and the "primary axis" hypothesis is wrong, the
frameshift hypothesis may simply be unnecessary, for birds and for
salamanders, and we can stop feeling guilty about calling the fingers of
birds I, II and III.
Ironically, however, Johanson et al. confirm that an axis can grow into
"radial" territory and have its tip modified into the shape of a "radial":
as mentioned way above, the most proximal preaxial radial of *Neoceratodus*
really does form by segmentation of the radius-radiale-etc. axis (in other
words, *Neoceratodus* has a prepollex...), unlike all other "radials". It's
just not the metapterygial axis, but the first "nonindependent preaxial
radial".
Unsurprisingly, questions remain. Shubin (2002) casually mentions
(especially in fig. 5) that plenty of (at least cryptobranchoid) salamanders
have an extra distal tarsal called the postminimus. What is that? More
evidence that the digits don't care about the rest of the limb when deciding
where to form? Or is it the fourth element of the metapterygial axis,
homologous to the last one in *Latimeria* and *Eusthenopteron*? Shubin
reproduces the only drawing of one of about two decently known fully
ossified temnospondyl feet, that of *Acheloma* (...he uses the junior
synonym *Trematops*). Dt 4 is very large, mt V articulates _between_ dt4 and
dt5, and dt5 is a rounded isosceles triangle, with the tip lying postaxial
to mtV. Isn't that strange? Both dt4 and dt5 lie distal to the fibulare.
Perhaps "dt4" is actually the "fusion" product of dt4 and dt5, and "dt5" is
actually the postminimus? And what is the pisiform (an extra proximal carpal
widespread in mammals, but also captorhinids, diadectomorphs, and many
others) -- an ancient sesamoid, the postminimus, or what? And what about the
toes in *Acanthostega* and *Ichthyostega* that articulate directly with the
fibulare? Not to mention the finger of *Tulerpeton* that articulates
directly with the ulna -- not the ulnare, but the ulna? (Illustrated here
http://www.press.uchicago.edu/books/gee/shubin3.jpeg and
http://www.nature.com/nature/journal/v440/n7085/fig_tab/nature04637_F4.html
here.) To what extent are digits of Devonian tetrapods homologous to digits
of pentadactyl tetrapods or to those of other Devonian tetrapods -- is it
all just an unspecified mess of "radials" that grew wherever there was space
for them? And to what extent are _bird_ fingers homologous to anything,
then...?
All that makes me tired. It's a quarter to three at night. I'm going to bed.
==== References ====
Davis C, Dahn RD, Shubin NH. 2007. An autopodial-like pattern of _Hox_
expression in the fins of a basal actinopterygian fish. Nature 447: 437 --
476.
Fröbisch NB, Carroll RC, Schoch RR. 2007. Limb ossification in the Paleozoic
branchiosaurid *Apateon* (Temnospondyli) and the early evolution of preaxial
dominance in tetrapod limb development. Evolution & Development 9: 69 -- 75.
Shubin NH. 2002. Origin of evolutionary novelty: examples from limbs.
Journal of Morphology 252: 15 -- 28.