Reinventing the prepollex: yet another bird finger embryology paper

[David Marjanovic <david.marjanovic@gmx.at>]

"Showtaaam!"
-- Prof. Jacques Gauthier at the First International Meeting on 
Phylogenetic Nomenclature (2004 in Paris), announcing that the lunch break 
was over.
----------------------------------------------------

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 
the interpretation:

>>
_Alternative models_

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 
finger?

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 
testable.

_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 
prepollex...?

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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