Epidermal Differentiation During Ontogeny and After
Hatching in the Snake Liasis fuscus (Pythonidae,
Serpentes, Reptilia), With Emphasis on the Formation
of the Shedding Complex
L. Alibardi
1
* and M.B. Thompson
2
1
Dipartimento di Biologia evoluzionistica sperimentale, University of Bologna, 40126, Bologna, Italy
2
School of Biological Sciences and Wildlife Research Institute, University of Sydney, NSW 2006, Sydney, Australia
ABSTRACT Differentiation and localization of keratin
in the epidermis during embryonic development and up
to 3 months posthatching in the Australian water py-
thon, Liasis fuscus, was studied by ultrastructural and
immunocytochemical methods. Scales arise from dome-
like folds in the skin that produce tightly imbricating
scales. The dermis of these scales is completely differ-
entiated before any epidermal differentiation begins,
with a loose dermis made of mesenchymal cells beneath
the differentiating outer scale surface. At this stage (33)
the embryo is still unpigmented and two layers of su-
prabasal cells contain abundant glycogen. At Stage 34
(beginning of pigmentation) the first layers of cells be-
neath the bilayered periderm (presumptive clear and
oberhautchen layers) have not yet formed a shedding
complex, within which prehatching shedding takes
place. At Stage 35 the shedding complex, consisting of
the clear and oberhautchen layers, is discernible. The
clear layer contains a fine fibrous network that faces the
underlying oberhautchen, where the spinulae initially
contain a core of fibrous material and small beta-keratin
packets. Differentiation continues at Stage 36 when the
beta-layer forms and beta-keratin packets are deposited
both on the fibrous core of the oberhautchen and within
beta-cells. Mesos cells are produced from the germinal
layer but remain undifferentiated. At Stage 37, before
hatching, the beta-layer is compact, the mesos layer
contains mesos granules, and cells of the alpha-layer
are present but are not yet keratinized. They are still
only partially differentiated a few hours after hatching,
when a new shedding complex is forming underneath.
Using antibodies against chick scale beta-keratin re-
solved at high magnification with immunofluorescent or
immunogold conjugates, we offer the first molecular
confirmation that in snakes only the oberhautchen com-
ponent of the shedding complex and the underlying beta
cells contain beta-keratin. Initially, there is little im-
munoreactivity in the small beta-packets of the ober-
hautchen, but it increases after fusion with the under-
lying cells to produce the syncytial beta layer. The beta-
keratin packets coalesce with the tonofilaments,
including those attached to desmosomes, which rapidly
disappear in both oberhautchen and beta-cells as differ-
entiation progresses. The labeling is low to absent in
forming mesos-cells beneath the beta-layer. This study
further supports the hypothesis that the shedding com-
plex in lepidosaurian reptiles evolved after there was a
segregation between alpha-keratogenic cells from beta-
keratogenic cells during epidermal renewal. J. Morphol.
256:29 – 41, 2003. © 2003 Wiley-Liss, Inc.
KEY WORDS: python; snake; embryogenesis; epidermis;
beta-keratins; immunocytochemistry; ultrastructure; skin
In snakes the epidermis is not continuously re-
newed, as it is in other vertebrates, but cell multi-
plication in the germinal layer takes place during
limited periods called renewal phases (Maderson,
1965a, 1985; Landmann, 1979). During these peri-
ods a new (inner) epidermal generation is produced
beneath the old (outer) generation, which is later
shed (Maderson et al., 1998). In contrast to most
lizards, shedding in all snakes is a single event
resulting in the whole skin being lost in one piece.
Thus, snakes have a perfectly synchronized mecha-
nism of shedding and are among the most special-
ized vertebrates to renew their epidermis in cyclical
phases.
The specialized epidermis of snakes is formed by
numerous layers called oberhautchen, beta, mesos,
alpha, lacunar, and clear (Maderson, 1965a, 1985;
Roth and Jones, 1967, 1970; Landmann, 1979,
1986). Morphological and biophysical studies sug-
gest that the oberhautchen and beta-layers mainly
synthesize beta-keratin, while the remaining layers
synthesize alpha-keratin (Roth and Maderson, 1968;
Contract grant sponsor: University of Bologna grant (segnali mole-
colari dello sviluppo).
*Correspondence to: L. Alibardi, Dipartimento di Biologia evoluzi-
onistica sperimentale, University of Bologna, via Selmi 3, 40126,
Bologna, Italy. E-mail: Alibardi@biblio.cib.unibo.it
DOI: 10.1002/jmor.10071
JOURNAL OF MORPHOLOGY 256:29 – 41 (2003)
© 2003 WILEY-LISS, INC.