ISSN 10623604, Russian Journal of Developmental Biology, 2015, Vol. 46, No. 4, pp. 222–230. © Pleiades Publishing, Inc., 2015.
Published in Russian in Ontogenez, 2015, Vol. 46, No. 4, pp. 267–276.
It is known that, in snake prenatal ontogeny, as in
other vertebrates, the first primordia of chondrocra
nium to appear are the basic structures: trabeculae cra
nii, parachordals and polar cartilages (de Beer, 1937;
Kamal and Hammouda, 1965c; Bellairs and Kamal,
1981; Kuratani, 1999; Yaryhin, 2009; Sheverdyukova,
In just oviposed eggs, the embryos of oviparous
snakes are at stage 27 (Korneva, 1969; Jackson, 2002;
Boughner et al., 2007; Boback et al., 2012) according
to the table of normal development, proposed by
D. Zehr (1962). All studies on snake skull embryogen
esis start with this or later stages of development
(Parker, 1878; Brock, 1929;
1954; Kamal and Hammouda, 1965a, 1965b, 1965c;
ElToubi et al., 1970, 1973; Haluska and Alberch,
1983; Deiques, 2004).
Snake skull is characterized by highly developed
kineticism, whose origin is associated with the skull
adaptation to swallow a large prey (Dullemejer, 1956;
Albright, 1959; Gans, 1959; Frazzetta, 1966; Iordan
sky, 1978; Cundall and Greene, 2000). The significant
reduction of the orbital region in snake chondrocra
nium is associated with the formation of the
skull. The reduced orbital cartilages are
The article was translated by the authors.
described only in some species (Parker, 1878; Bellairs,
1949; Kamal and Hammouda, 1965b).
The purposes of our investigation are to study the
dynamics of Grass snake
(Serpentes, Colubridae), chondrocranium formation
at the early stages of development and to attract the
attention of embryologists to the studying of early
stages of skull embryogenesis in other vertebrates.
MATERIALS AND METHODS
females were caught in their
natural habitat and were put in terrariums, where they
laid eggs. We incubated egg clutches in wetted vermic
ulite at the temperature
. Two embryos were
withdrawn from the clutch every day. In such a way, we
obtained embryos at 27 and succeeding developmental
stages. To obtain embryos at the earlier stages of devel
opment, caesarean sections of
done a few days before natural oviposition. The tech
nique of caesarean section we used was designed espe
cially for snakes (Clark, 1937).
Anesthesia and immobilization of the animals were
carried out according to the techniques developed spe
cially for reptiles (Vasiliev and Timerina, 2000). To
preserve the females’ ability to produce progeny, the
eggs were removed from the upper oviduct. All the
embryos obtained from one female were externally
anatomically identical and belonged to the same stage
Early Stages of Skull Embryogenesis in the Grass Snake,
F. Kovtun and H. V. Sheverdyukova
Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine,
ul. Khmelnitsky 15, Kyiv, UA01601, Ukraine
Received May 29, 2014; in final form, January 19, 2015
—Studies of previous authors on snake skull embryogenesis have been performed on embryos
obtained from eggs after oviposition. The aim of this study was to investigate the initial stages of chondrocra
nium development in Grass snake
Linnaeus, 1758, embryos before oviposition.
embryos at early developmental stages (24–27 according to the table of normal development by D. Zehr
(1962)) were obtained by means of caesarean section. At developmental stages 25–27, previously undescribed
structures were found in the region of future skull formation. These structures exist during one or two stages
and then disappear. Therefore, we call them “temporary structures.” The assumption about the nature of
these structures is based on their topography and comparison with the structures of developing or fully formed
chondrocranium in other vertebrates. It is hypothesized that the temporary structures in
drocranium are vestiges of primary chondrocranium of ancestral vertebrate forms, and they indicate the exist
ence of several variants in the formation of chondrocranium in the historical vertebrates’ development.
: chondrocranium, embryogenesis, temporary vestiges,
ONTOGENESIS AND EVOLUTION