INTRODUCTION
Ctenophores have a single body axis (oral-aboral) with two
perpendicular planes of symmetry dividing the embryo into
four quadrants. Each quadrant derives from one blastomere
at the 4-cell stage. These blastomeres undergo two unequal
divisions to give rise to two types of macromere and two
types of micromere at the 16-cell stage. These all have dif-
ferent fates and develop autonomously in classical mosaic
fashion. Two of the eight characteristic rows of ciliated
comb-plates of ctenophores derive from one micromere in
each quadrant (see Reverberi, 1971; Freeman, 1979; Sardet
et al., 1990 for reviews). The high degree of organisation
in cleavage stage embryos becomes established entirely
after fertilisation, the egg having no pre-determined devel-
opmental axis. The position of the oral pole coincides with
the site of initiation of the first cleavage furrow, and not to
the ‘animal pole’ where the polar bodies are emitted (Free-
man, 1977). The site of first cleavage depends in turn on
the position of sperm entry, which can be anywhere over
the egg surface (Freeman, 1977; Carré and Sardet, 1984).
The female pronucleus migrates to join a stationary male
pronucleus, ‘choosing’ one in cases where polyspermy has
occurred (Carré and Sardet, 1984). At this site, the zygote
nucleus forms, first mitosis occurs and the first cleavage
furrow starts, cleavage being unipolar. The planes of sym-
metry of the larvae can be predicted by the orientation of
the first cleavage, and may be related to the path of migra-
tion of the female pronucleus (Carré et al., 1991). Pronu-
clear migration, mitosis and all other cytoplasmic events
occur in a 5-50 μm thick peripheral layer of ‘ectoplasm’
that surrounds a central ball of yolky ‘endoplasm’. This
75
Development 117, 75-87 (1993)
Printed in Great Britain © The Company of Biologists Limited 1993
The single axis (oral-aboral) and two planes of symme-
try of the ctenophore Beroe ovata become established
with respect to the position of zygote nucleus formation
and the orientation of first cleavage. Bisection of Beroe
eggs at different times revealed that differences in egg
organisation are established in relation to the pre-
sumptive oral-aboral axis before first cleavage. Lateral
fragments produced after but not before the time of first
mitosis developed into larvae lacking comb-plates on
one side. Time-lapse video demonstrated that waves of
cytoplasmic reorganisation spread through the layer of
peripheral cytoplasm (ectoplasm) of the egg during the
80 minute period between pronuclear fusion and first
cleavage, along the future oral-aboral axis. These waves
are manifest as the progressive displacement and dis-
persal of plaques of accumulated organelles around
supernumerary sperm nuclei, and a series of surface
movements. Their timing and direction of propagation
suggest they may be involved in establishing cytoplas-
mic differences with respect to the embryonic axis.
Inhibitor experiments suggested that the observed
cytoplasmic reorganisation involves microtubules. Noco-
dazole and taxol, which prevent microtubule turnover,
blocked plaque dispersal and reduced surface move-
ments. The microfilament-disrupting drug cytochalasin
B did not prevent plaque dispersal but induced abnor-
mal surface contractions. We examined changes in
microtubule organisation using immunofluorescence on
eggs fixed at different times and in live eggs following
injection of rhodamine-tubulin. Giant microtubule
asters become associated with each male pronucleus
after the end of meiosis. Following pronuclear fusion
they disappear successively, those nearest the zygote
nucleus shrinking first, to establish gradients of aster
size within single eggs. Regional differences in micro-
tubule behaviour around the time of mitosis were
revealed by brief taxol treatment, which induced the for-
mation of small microtubule asters in the region of the
nucleus or spindle during both first and second cell
cycles. The observed wave of change may thus reflect
the local appearance and spreading of mitotic activity
as the zygote nucleus approaches mitosis.
Key words: cleavage, ctenophore, embryonic axis, microtubule,
mitosis, aster
SUMMARY
Axis establishment and microtubule-mediated waves prior to first
cleavage in Beroe ovata
Evelyn Houliston, Danièle Carré, Jennifer A. Johnston
1
and Christian Sardet
Unité de Biologie Cellulaire Marine (URA 671 CNRS/Université Paris VI), Observatoire de Villefranche-sur-mer, Station
Zoologique, 06230 Villefranche-sur-mer, France
1
Department of Biological Science, Dartmouth College, 306 Gilman, Hanover, NH 03755-1893, USA