243
Thus, although a general correlated trend in the reduction
of development time with egg enlargement seems to exist in
gymnolaemate bryozoans, the situation is less than straightforward, being strongly complicated by the large variation in
egg size and duration of development in both brooders and
broadcasters.
Interestingly, the above facts show that the shortest
embryogenesis among brooding gymnolaemates is
observed in the species with the least-derived reproductive
traits, including small numerous oocytes and primitive
brooding modes, that is, in the cheilostome Tendra zostericola and the ctenostome Triticella fl ava . In more advanced
gymnolaemates with larger oocytes or with relatively small
oocytes and matrotrophy, embryogenesis is noticeably longer. Also, the fully formed larvae of Triticella , which have
a body shape reminiscent of cyphonautes larvae and a nonfunctioning gut, reportedly lived in the aquarium for a further month, gradually becoming smaller (Ström 1969 ).
Similar examples are known among asteroids with lecithotrophic larvae (discussed in Emlet et al. 1987 ). It is
unclear if this ability for prolonged starvation is an
advanced trait connected with accumulation of extra
reserves in the egg, or a primitive character state inherited
from a cyphonautes larval form adapted to a non-stable
food supply.
The examples of Tendra and Triticella indicate the possibility of the following scenario. In the evolution of gymnolaemate bryozoans, the duration of embryogenesis was at
fi rst considerably reduced following the transition to
lecithotrophy owing to an accumulation of additional nutrients in the oocytes. One may suggest that the fi rst lecithotrophic larvae with a rudimentary gut, resembling those of
Tendra and Triticella , developed from small oocytes (similar
in size to the oocytes of the ancestors with planktotrophic
larvae). Since these larvae did not have to feed, they achieved
a competent state much faster than did cyphonautes larvae.
Later in evolution, however, oocytes increased in size by
accumulating additional nutrients and this was accompanied
by secondary prolongation of the duration of endotrophic
larval development. As a result, there are species with lecithotrophic larvae and prolonged development (e.g.
Cryptosula pallasiana ), comparable with that of long-lived
planktotrophic larvae.
Hoegh-Guldberg and Pearse ( 1995 ) suggested that, given
the same temperature and food availability for planktotrophic larvae, the latter would develop at approximately the
same rate as lecithotrophic ones owing to the general dependence of metabolic rates on water temperature. The authors
concluded that any kind of feeding (acquisition of food or the
use of the already-available resources) does not signifi cantly
infl uence the evolution of development rates. As a critical
remark, it can be said that while rates of development of exoand endotrophic larvae are probably similar, their periods of
development are usually quite different (see above). A planktotrophic larva not only acquires energy during feeding but
also spends it on food capture and locomotion. Throughout
their (often quite long) life span, such larvae spend up to half
of their total energy on food acquisition, which may be irregular (Hoegh-Guldberg and Emlet 1997 ). Lecithotrophic larvae are entirely “carefree” in this respect and could accelerate
their development, in particular, by means of heterochronies,
“skipping” certain (usually, early) stages of embryogenesis
and reaching a competent state faster (Raff 1996 ). It should
be noted that Hoegh-Guldberg and Emlet ( 1997 ) demonstrated experimentally a higher level and rates of metabolic
activity in lecithotrophic larvae as compared to planktotrophic ones in Heliocidaris sea urchins.
3.1.2.4 Changes in Ovary Structure
All gymnolaemates are characterized by a common basic
plan of organisation of the female gonad (Reed 1991 ; pers.
obs.), its variants (see Chap. 1 ) presumably refl ecting the
stages of evolution of this organ. Evolutionary changes in
oogenesis would inevitably have been accompanied by
changes in gonad structure. Compared to species with reproductive pattern I, those with patterns II and IV have a more
compact ovary and a more distinct intraovarian zone, which
corresponds to the sequential formation of a few large gametes. The compact ovary of bryozoans with patterns III and V
(Dyrynda and King 1982 ) consists of a few cells and has a
barely discernible intraovarian zone. Such a structure results
from the formation of a few oligo- or mesolecithal eggs in
these ovaries. Therefore, the difference in the structure of the
female gonad in species with different reproductive patterns
may be explained by the difference in the mode of gamete
production. This was fi rst noticed by Waters ( 1912 , 1913 ; see
Sect. 1.3.3 ), who categorised ovaries of different species into
two groups based on oocyte size and number. Although not
describing (but illustrating) ovarian structure itself, Waters
correctly noted that ovaries contain 2–3 small oocytes in
bugulids (pattern III), whereas many eggs, one of which
reached a considerable size, were seen in the candids studied
(pattern II).
3.2
Early Fertilization and Origin
of Nurse Cells
The relationship between sperm morphology and the circumstances of fertilization have been broadly discussed
(Franzén 1956 ; Kasyanov 1989 ; Ryland and Bishop 1993 ;
Drozdov and Ivankov 2000 ). The sperm of all three classes
of bryozoans are considered to be highly modifi ed compared
to the primitive sperm of animal groups with external fertilization (Franzén 1956 , 1970 , 1987 ; Woollacott 1999 ), indicating that internal fertilization emerged early in the evolution
3.2 Early Fertilization and Origin of Nurse Cells
Thus, although a general correlated trend in the reduction
of development time with egg enlargement seems to exist in
gymnolaemate bryozoans, the situation is less than straightforward, being strongly complicated by the large variation in
egg size and duration of development in both brooders and
broadcasters.
Interestingly, the above facts show that the shortest
embryogenesis among brooding gymnolaemates is
observed in the species with the least-derived reproductive
traits, including small numerous oocytes and primitive
brooding modes, that is, in the cheilostome Tendra zostericola and the ctenostome Triticella fl ava . In more advanced
gymnolaemates with larger oocytes or with relatively small
oocytes and matrotrophy, embryogenesis is noticeably longer. Also, the fully formed larvae of Triticella , which have
a body shape reminiscent of cyphonautes larvae and a nonfunctioning gut, reportedly lived in the aquarium for a further month, gradually becoming smaller (Ström 1969 ).
Similar examples are known among asteroids with lecithotrophic larvae (discussed in Emlet et al. 1987 ). It is
unclear if this ability for prolonged starvation is an
advanced trait connected with accumulation of extra
reserves in the egg, or a primitive character state inherited
from a cyphonautes larval form adapted to a non-stable
food supply.
The examples of Tendra and Triticella indicate the possibility of the following scenario. In the evolution of gymnolaemate bryozoans, the duration of embryogenesis was at
fi rst considerably reduced following the transition to
lecithotrophy owing to an accumulation of additional nutrients in the oocytes. One may suggest that the fi rst lecithotrophic larvae with a rudimentary gut, resembling those of
Tendra and Triticella , developed from small oocytes (similar
in size to the oocytes of the ancestors with planktotrophic
larvae). Since these larvae did not have to feed, they achieved
a competent state much faster than did cyphonautes larvae.
Later in evolution, however, oocytes increased in size by
accumulating additional nutrients and this was accompanied
by secondary prolongation of the duration of endotrophic
larval development. As a result, there are species with lecithotrophic larvae and prolonged development (e.g.
Cryptosula pallasiana ), comparable with that of long-lived
planktotrophic larvae.
Hoegh-Guldberg and Pearse ( 1995 ) suggested that, given
the same temperature and food availability for planktotrophic larvae, the latter would develop at approximately the
same rate as lecithotrophic ones owing to the general dependence of metabolic rates on water temperature. The authors
concluded that any kind of feeding (acquisition of food or the
use of the already-available resources) does not signifi cantly
infl uence the evolution of development rates. As a critical
remark, it can be said that while rates of development of exoand endotrophic larvae are probably similar, their periods of
development are usually quite different (see above). A planktotrophic larva not only acquires energy during feeding but
also spends it on food capture and locomotion. Throughout
their (often quite long) life span, such larvae spend up to half
of their total energy on food acquisition, which may be irregular (Hoegh-Guldberg and Emlet 1997 ). Lecithotrophic larvae are entirely “carefree” in this respect and could accelerate
their development, in particular, by means of heterochronies,
“skipping” certain (usually, early) stages of embryogenesis
and reaching a competent state faster (Raff 1996 ). It should
be noted that Hoegh-Guldberg and Emlet ( 1997 ) demonstrated experimentally a higher level and rates of metabolic
activity in lecithotrophic larvae as compared to planktotrophic ones in Heliocidaris sea urchins.
3.1.2.4 Changes in Ovary Structure
All gymnolaemates are characterized by a common basic
plan of organisation of the female gonad (Reed 1991 ; pers.
obs.), its variants (see Chap. 1 ) presumably refl ecting the
stages of evolution of this organ. Evolutionary changes in
oogenesis would inevitably have been accompanied by
changes in gonad structure. Compared to species with reproductive pattern I, those with patterns II and IV have a more
compact ovary and a more distinct intraovarian zone, which
corresponds to the sequential formation of a few large gametes. The compact ovary of bryozoans with patterns III and V
(Dyrynda and King 1982 ) consists of a few cells and has a
barely discernible intraovarian zone. Such a structure results
from the formation of a few oligo- or mesolecithal eggs in
these ovaries. Therefore, the difference in the structure of the
female gonad in species with different reproductive patterns
may be explained by the difference in the mode of gamete
production. This was fi rst noticed by Waters ( 1912 , 1913 ; see
Sect. 1.3.3 ), who categorised ovaries of different species into
two groups based on oocyte size and number. Although not
describing (but illustrating) ovarian structure itself, Waters
correctly noted that ovaries contain 2–3 small oocytes in
bugulids (pattern III), whereas many eggs, one of which
reached a considerable size, were seen in the candids studied
(pattern II).
3.2
Early Fertilization and Origin
of Nurse Cells
The relationship between sperm morphology and the circumstances of fertilization have been broadly discussed
(Franzén 1956 ; Kasyanov 1989 ; Ryland and Bishop 1993 ;
Drozdov and Ivankov 2000 ). The sperm of all three classes
of bryozoans are considered to be highly modifi ed compared
to the primitive sperm of animal groups with external fertilization (Franzén 1956 , 1970 , 1987 ; Woollacott 1999 ), indicating that internal fertilization emerged early in the evolution
3.2 Early Fertilization and Origin of Nurse Cells