258
evolution towards intracoelomic incubation is problematic
because of the need for the larva to escape from the zooid.
Fertilized oocytes should exit the zooidal cavity before the
onset of brooding, otherwise the exit of a large, “solid” larva
would need to be accompanied by rupture of the cystid wall.
Intracoelomic fertilization should dramatically increase the
chances of oocytes to be fertilized but would require a physiological mechanism preventing cleavage before oviposition.
Such a mechanism must have evolved in phylactolaemates
and most gymnolaemates.
Cyclostomes and epistomiid cheilostomes, on the other
hand, were not handicapped by such apparent inherent diffi -
culties and succeeded in evolving intracoelomic incubation.
In the former, the isolation of the gonozooid coelomic cavity
during larval release appears to be ensured by the structure of
the vestibulum and the membranous sac (see Borg 1926 ).
Also, larvae are fl exible enough to squeeze through the narrow tube of the ooeciostome. In epistomiids, maternal zooids
do not develop polypides and cease to function after larval
release (Dyrynda and King 1982 ).
3.4.3 Oviposition in Cheilostome Brooders
Bryozoan polypides exhibit a broad range of “individual” and
collective behaviours associated with feeding, cleaning the
lophophore and the colony, avoidance of unfavourable external factors and gamete release (Cook 1977a , 1980 ; Winston
1977 , 1978 ; Shunatova and Ostrovsky 2001 , 2002 ; Ostrovsky
and Shunatova 2002 ; Ostrovsky et al. 2002 , 2008a ). To place
a fertilized oocyte into the ovicell, the polypide has to perform a complex behavioural act, transferring it from the coelomic cavity of the maternal zooid into the cavity of the brood
chamber via the supranerval pore or, in some species, the
intertentacular organ (see also Sects. 1.3.7 and 1.3.9 ).
Compared to the spawning of eggs via the intertentacular
organ in broadcasting species (Silén 1966 ; Temkin 1994 ), the
act of oviposition is much more complex. Apparently, it
evolved in cheilostomes at about the same time as brooding.
The origin of brooding must have resulted in the loss of
the intertentacular organ. Perhaps the removal of large eggs
from the coelom of maternal zooids was fraught with more
diffi culties than oviposition via the supraneural pore. This
limitation does not seem to apply to Tendra zostericola , in
which the mature oocytes are relatively small, and to
Thalamoporella evelinae , whose female zooids have a very
large intertentacular organ and brood cavity. In the event, an
analogue of the intertentacular organ evolved in two
Schizoporella species (see Sect. 1.3.9 , also discussed in
Ostrovsky and Porter 2011 ).
The evolutionary scenario may be sketched as follows.
In the fi rst brooding cheilostomes with primitive endotrophic
larvae the zygotes were attached to the distal zooid, surrounded
by a sticky fertilization envelope as in some ctenostomes
(see Ström 1969 ). Upon leaving the maternal zooid, zygotes
remained between the mural spines on the proximal gymnocyst of the distal zooid. The chances of becoming attached to
this particular area of the distal zooid were high, since the
coelomopore is placed between distomedial tentacles and the
introvert of the expanded polypide is often inclined in this
direction. Oviposition can also be accompanied by polypide
tilting. It is also rather probable that such species still had an
intertentacular organ, involved in oviposition. Such specialized behaviour is characteristic of some ctenostomes (see
Sect. 3.4.4 ).
Following the evolution of skeletal brood chambers from
the mural spines, the fertilized oocyte had to be placed into
the brood cavity. It was presumably at that evolutionary
moment that the fi rst ovicelled cheilostome lost the intertentacular organ.
Judging from the descriptions of oviposition in the literature, large eggs are removed from the visceral coelom in
brooding bryozoans by means of (1) increased pressure of
the coelomic fl uid of the maternal zooid and (2) high plasticity (fl exibility) of the oocytes (see Sect. 1.3.7 ). Coelomic
fl uid pressure is increased by contraction of parietal muscles,
which lower the frontal membrane or expand the ascus. The
polypide is automatically protruded in the process but the
supraneural pore is situated much higher than the entrance of
the brood chamber. To transfer an egg into the brood cavity,
therefore, the lophophore should be protruding only partially, so that the base of the tentacle crown and its coelomopore are just opposite the ovicell entrance. The ovulated
oocyte should by that time be near the supraneural pore.
Presumably, when this latter condition is in place, the pressure of the coelomic fl uid is increased by appropriate contraction of parietal muscles, resulting not in full protrusion of
the polypide but in the extrusion of the large oocyte from the
maternal body cavity. The polypide remains in this position
for several minutes, until the zygote is transferred into the
brood chamber. Oviposition under a closed operculum
appears to be secondary development, evolving after the origin of cleithral ovicells (see Sect. 1.3.7 ).
It follows that this process of oviposition must have
evolved within the order Cheilostomata as many times as
skeletal brood chambers did.
3.4.4 Evolution of Sexual Reproduction
Within the Order Ctenostomata
3.4.4.1 Reproductive Patterns and Evolutionary
Trends
Analysis of the relevant literature shows that the general evolutionary direction of the reproductive patterns in ctenostomes was the same as in cheilostomes. Most ctenostomes
3 Evolution of Reproductive Patterns in Cheilostomata
evolution towards intracoelomic incubation is problematic
because of the need for the larva to escape from the zooid.
Fertilized oocytes should exit the zooidal cavity before the
onset of brooding, otherwise the exit of a large, “solid” larva
would need to be accompanied by rupture of the cystid wall.
Intracoelomic fertilization should dramatically increase the
chances of oocytes to be fertilized but would require a physiological mechanism preventing cleavage before oviposition.
Such a mechanism must have evolved in phylactolaemates
and most gymnolaemates.
Cyclostomes and epistomiid cheilostomes, on the other
hand, were not handicapped by such apparent inherent diffi -
culties and succeeded in evolving intracoelomic incubation.
In the former, the isolation of the gonozooid coelomic cavity
during larval release appears to be ensured by the structure of
the vestibulum and the membranous sac (see Borg 1926 ).
Also, larvae are fl exible enough to squeeze through the narrow tube of the ooeciostome. In epistomiids, maternal zooids
do not develop polypides and cease to function after larval
release (Dyrynda and King 1982 ).
3.4.3 Oviposition in Cheilostome Brooders
Bryozoan polypides exhibit a broad range of “individual” and
collective behaviours associated with feeding, cleaning the
lophophore and the colony, avoidance of unfavourable external factors and gamete release (Cook 1977a , 1980 ; Winston
1977 , 1978 ; Shunatova and Ostrovsky 2001 , 2002 ; Ostrovsky
and Shunatova 2002 ; Ostrovsky et al. 2002 , 2008a ). To place
a fertilized oocyte into the ovicell, the polypide has to perform a complex behavioural act, transferring it from the coelomic cavity of the maternal zooid into the cavity of the brood
chamber via the supranerval pore or, in some species, the
intertentacular organ (see also Sects. 1.3.7 and 1.3.9 ).
Compared to the spawning of eggs via the intertentacular
organ in broadcasting species (Silén 1966 ; Temkin 1994 ), the
act of oviposition is much more complex. Apparently, it
evolved in cheilostomes at about the same time as brooding.
The origin of brooding must have resulted in the loss of
the intertentacular organ. Perhaps the removal of large eggs
from the coelom of maternal zooids was fraught with more
diffi culties than oviposition via the supraneural pore. This
limitation does not seem to apply to Tendra zostericola , in
which the mature oocytes are relatively small, and to
Thalamoporella evelinae , whose female zooids have a very
large intertentacular organ and brood cavity. In the event, an
analogue of the intertentacular organ evolved in two
Schizoporella species (see Sect. 1.3.9 , also discussed in
Ostrovsky and Porter 2011 ).
The evolutionary scenario may be sketched as follows.
In the fi rst brooding cheilostomes with primitive endotrophic
larvae the zygotes were attached to the distal zooid, surrounded
by a sticky fertilization envelope as in some ctenostomes
(see Ström 1969 ). Upon leaving the maternal zooid, zygotes
remained between the mural spines on the proximal gymnocyst of the distal zooid. The chances of becoming attached to
this particular area of the distal zooid were high, since the
coelomopore is placed between distomedial tentacles and the
introvert of the expanded polypide is often inclined in this
direction. Oviposition can also be accompanied by polypide
tilting. It is also rather probable that such species still had an
intertentacular organ, involved in oviposition. Such specialized behaviour is characteristic of some ctenostomes (see
Sect. 3.4.4 ).
Following the evolution of skeletal brood chambers from
the mural spines, the fertilized oocyte had to be placed into
the brood cavity. It was presumably at that evolutionary
moment that the fi rst ovicelled cheilostome lost the intertentacular organ.
Judging from the descriptions of oviposition in the literature, large eggs are removed from the visceral coelom in
brooding bryozoans by means of (1) increased pressure of
the coelomic fl uid of the maternal zooid and (2) high plasticity (fl exibility) of the oocytes (see Sect. 1.3.7 ). Coelomic
fl uid pressure is increased by contraction of parietal muscles,
which lower the frontal membrane or expand the ascus. The
polypide is automatically protruded in the process but the
supraneural pore is situated much higher than the entrance of
the brood chamber. To transfer an egg into the brood cavity,
therefore, the lophophore should be protruding only partially, so that the base of the tentacle crown and its coelomopore are just opposite the ovicell entrance. The ovulated
oocyte should by that time be near the supraneural pore.
Presumably, when this latter condition is in place, the pressure of the coelomic fl uid is increased by appropriate contraction of parietal muscles, resulting not in full protrusion of
the polypide but in the extrusion of the large oocyte from the
maternal body cavity. The polypide remains in this position
for several minutes, until the zygote is transferred into the
brood chamber. Oviposition under a closed operculum
appears to be secondary development, evolving after the origin of cleithral ovicells (see Sect. 1.3.7 ).
It follows that this process of oviposition must have
evolved within the order Cheilostomata as many times as
skeletal brood chambers did.
3.4.4 Evolution of Sexual Reproduction
Within the Order Ctenostomata
3.4.4.1 Reproductive Patterns and Evolutionary
Trends
Analysis of the relevant literature shows that the general evolutionary direction of the reproductive patterns in ctenostomes was the same as in cheilostomes. Most ctenostomes
3 Evolution of Reproductive Patterns in Cheilostomata