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Reinventing the prepollex: yet another bird finger embryology paper
-- Prof. Jacques Gauthier at the First International Meeting on
Phylogenetic Nomenclature (2004 in Paris), announcing that the lunch break
Googling for "Eutetrapoda" just brought me this:
Monique C. M. Welten, Fons J. Verbeek, Annemarie H. Meijer & Michael K.
Richardson: Gene expression and digit homology in the chicken embryo wing,
Evolution & Development 7(1), 18 -- 28 (January 2005)
_SUMMARY_ The bird wing is of special interest to students of homology
and avian evolution. Fossil and developmental data give conflicting
indications of digit homology if a pentadactyl "archetype" is assumed.
Morphological signs of a vestigial digit I are seen in bird embryos, but
no digit-like structure develops in wild-type embryos. To examine the
developmental mechanisms of digit loss, we studied the expression of the
high-mobility group box containing Sox9 gene, and bone morphogenetic
protein receptor 1b (bmpR-1b)?markers for precondensation and
prechondrogenic cells, respectively. We find an elongated domain of Sox9
expression, but no bmpR-1b expression, anterior to digit II. We interpret
this as a digit I domain that reaches precondensation, but not
condensation or precartilage stages. It develops late, when the tissue in
which it is lodged is being remodeled. We consider these findings in the
light of previous Hoxd-11 misexpression studies. Together, they suggest
that there is a digit I vestige in the wing that can be rescued and
undergo development if posterior patterning cues are enhanced. We observed
Sox9 expression in the elusive "element X" that is sometimes stated to
represent a sixth digit. Indeed, incongruity between digit domains and
identities in theropods disappears if birds and other archosaurs are
considered primitively polydactyl. Our study provides the first gene
expression evidence for at least five digital domains in the chick wing.
The failure of the first to develop may be plausibly linked to attenuation
of posterior signals.
Apart from the visualization of some gene expression, the actual findings
are pretty standard. No new digits are identified. What is new is largely
Alternatives to the Frame Shift and bilateral reduction models [see near
the end of this post] can be considered:
- The anterior vestige in the chicken embryo wing is not a digit but some
other structure or primordium;
- Birds are not a clade within the theropods;
- Digit identities are not meaningful units of homology; rather, they are
emergent patterns generated nonspecifically by interactions between
developmental mechanisms (Goodwin and Trainor 1983); and
- The pentadactyl "archetype" is false and the archosaur limb may in fact
be primitively polydactylous.
We will discuss the polydactyly model in some detail -- not because we
consider it the most parsimonious explanation, but because it has scarcely
been discussed in the context of avian evolution for many decades. It also
has the unique virtue of providing continuity between digit position and
digit identity across archosaur phylogeny.
If the vestigial digit I domain of chicks is primitive for
archosaurs, then the "vestigial digits IV and V" of *Herrerasaurus* and
other archosaurs are in fact digits V and VI (Fig. 2). This would mean
that birds could also have a vestigial digit VI as Schestakowa (1927)
suggested. Element X or the pisiform are potential candidates for such a
vestige. Bardeleben (1889) considered the pisiform of mammals to be a
vestige of a sixth digit. This opinion was also held by Holmgren (1952),
who viewed the tetrapod limb as primitively seven-fingered, on the basis
of his extensive developmental studies. Studies in other taxa predict that
digital loss should be bilateral, affecting digit I as well as posterior
digits (Alberch and Gale 1983). This has always made the asymmetric
reduction in archosaurs (affecting digits IV and V) seem anomalous.
However, if archosaurs are polydactyl, and have a vestigial digit I domain
in their embryos, then there is no anomaly (Fig. 2).
Polydactyly is not robustly supported at this time. Most evidence for
digit I in birds, and for extra digits generally, is of the "nodules and
shadows" type, where morphological vestiges in adults, or histological
traces in embryos, are interpreted as recapitulated digits. Other
difficulties with a polydactyly theory are: embryos from nonavian
theropods are not available for study; no adult archosaur has six distinct
digits; there is no evidence for a vestigial digit I in archosaurs outside
birds; and we saw no evidence of more than five digital domains of Sox9
expression in the chick foot in this study.
Examples of supposed extra digital elements are seen in other
Eutetrapoda, and include the claimed "postminimus" in the pes of some
salamanders (e.g., Hynobius lichenatus; Hasumi and Iw[a?]sawa 2004), and
polydactyly in humans (Biesecker 2002). Late Devonian tetrapods were
certainly polydactylous (Coates and Clack 1990) and the Early
Carboniferous tetrapod *Pederpes finneyae* is speculated to have had a
hexadactylous manus (Clack 2002) [wrong, generally polydactyl, not
necessarily hexa-]. However, *Casineria kiddi*, possibly an early amniote,
has a pentadactyl manus (Paton et al. 1999).
In summary, we have found molecular evidence of a digit I domain in
the chicken wing that is specified by early patterning mechanisms, but
fails to undergo terminal differentiation. In the light of previous
studies where Hoxd-11 was misexpressed, we suggest that the digit I domain
can be rescued by increasing the strength of posterior patterning signals.
Conflicts between fossil and developmental data can be eliminated by a
Frame Shift, by bilateral reduction, or by assuming that archosaurs are
primitively polydactyl. On the basis of current data, no one model of
digit homology is more parsimonious than others.
Of course, if "digits I through VI" are relabeled "prepollex and digits I
through V", then we get a pretty standard framework...
Now for the interesting comparisons.
I have a few pages from this treatise about vertebrate anatomy:
Dietrich Starck: Vergleichende Anatomie der Wirbeltiere auf
evolutionsbiologischer Grundlage, 2: Das Skeletsystem [sic]: Allgemeines,
Skeletsubstanzen [sic], Skelet [sic] der Wirbeltiere einschließlich
Lokomotionstypen, Springer 1979
Citing some work from the 1930s, this book has a few interesting ideas.
For example, it says that what is nowadays called "element X" (the thing
that replaces the ulnare in birds -- the true ulnare just disappears,
compare *Allosaurus* which apparently has a big gaping hole in that place)
is "the base of the fifth ray". This fits the suggestion by Welten et al.
that "element X" could be a place to look for the "sixth" finger.
According to the same book, the condensation called "digit V" by Welten et
al., Feduccia & Nowicki and most of the rest of the recent neontological
literature is the distal carpal and metacarpal IV, and what they all call
"digit I" is the prepollex. Of course, in the 30s and even in the 70s the
staining methods (for example) were in the Stone Age, and there was zero
knowledge on developmentary genetics, so the neat line drawings in that
book may not be all that reliable. But...
Neda Nikbaht & John C. McLachlan: Restoring avian wing digits, Proceedings
of the Royal Society of London B -- Biological Sciences 266, 1101 -- 1104
(7 July 1999)
Have a look of fig. 3 e) of that paper. Isn't it intriguing? By implanting
a bead soaked with FGF-4 in the wrist of a chicken embryo, they have
managed to make it grow an "element" caudal to "element 5". Based on
comparisons with "ceratosaurs", I'd say that "element 5" is metacarpal IV,
and that's also what Starck and his ref say. In that case it is logical to
assume that the "element" caudal to it (or rather, proximal -- as
expected) is the normally suppressed number V. Isn't this a more
parsimonious interpretation than having to call it a postminimus?
The resulting hypothesis that bird embryos have a prepollex and adults
have I-II-III leads to the following question: Why is the prepollex much
more easily visible than the 5th finger, considering the fact that the
prepollex disappeared much earlier in tetrapod evolution than the 5th
I guess the answer it could be related to the general archosaurian,
dinosaurian, saurischian, theropod and coelurosaur emphasis on the cranial
edge of the hand over the caudal one. The thumb is so well developed that
enough growth signals are available for the prepollex to grow bigger 5th
digital ray, of which only the base seems to persist. This idea should be
_In principle_, hands of adult tetrapods where the first four conventional
digits plus an ossified prepollex are present while the 5th finger is
completely absent have been known for a long time. Plenty of frogs have
that condition. Some burrowing frogs have extra-large prehalluces as well
that broaden their feet for digging.
Let's return to Welten et al.:
_Frame shift and bilateral ("pyramid") reduction hypotheses_
Our findings cannot distinguish between the Frame Shift and Pyramid
Reduction hypotheses because both of those models accept a vestigial
anterior digit in the chick.We are impressed, however, by the rescue of
the digit I domain in the chick by Hoxd-11 misexpression (Morgan et al.
1992). This is consistent with the idea that a shift in anteroposterior
positional signaling has occurred in the evolution of birds, such that
digit I no longer receives an adequate threshold of posteriorizing
signals. One could of course argue that the "rescued" digit I in those
experiments was in fact a reduplicated digit II produced by localized
mimicking of polarizing activity. However, because expression of the Hoxd
-11-RCAS construct was ubiquitous in the limb bud, and not localized to
the anterior border, we think this objection is unlikely.
I'll need to find that paper. Who says the "rescued digit I" isn't a
But first I need to ask the authors what they mean by "Eutetrapoda". That
term seems to have two meanings, one of which (Säve-Söderbergh 1934,
believing in the diphyly of Tetrapoda) is obviously not meant here, while
the other is apparently extremely rare and is not something I'd expect in
a neontological paper! :-)
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