163
which occurred independently in several cheilostome clades
(Ostrovsky et al. 2006 ).
Interestingly, some families with internal brooding, e.g.,
Cryptosulidae, contain both species with sexual zooidal
dimorphism ( Harmeria ) and without it ( Cryptosula ). This
may also be true of Watersiporidae; Uscia mexicana colonies
form heteromorphic zooids but it is not known if they are
sexual (female) or defensive (avicularian). At the same time,
there are no polymorphs in Watersipora .
The origin of intracoelomic embryo incubation in the
Epistomiidae remains an open question (Marcus 1941b ;
Dyrynda 1981 ; Dyrynda and King 1982 ). This variant may
have evolved through the loss of brooding in ovicells or
internal sacs and a transition to viviparity when cleavage
starts in the ovary. This shift might have somewhat accelerated reproduction, which is important for ephemeral species
such as epistomiids (see Chap. 3 ).
2.4.8.6 Change in the Method of Ovicell Closure
Analysis of the literature supports my own data on the
existence of different modes of ovicell closure in the same
family or genus. For instance, acleithral and cleithral ovicells
are known in the Calloporidae, Flustridae, Bugulidae,
Romancheinidae and Smittinidae. These facts point to
another evolutionary trend frequently manifested within the
Cheilostomata – a change in the ovicell closure mechanism.
One can suggest that the non-cleithral character state
(if not secondary, see below) is plesiomorphic and that
cleithral is apomorphic, whereas all the other states represent
intermediate stages (and their variants) in the evolution of
ovicell closure for better protection of the embryo. The calcifi ed unitary ooecium certainly protects the embryo better
than spinose, and the most vulnerable aspect is the broodchamber opening. The fi rst step towards an acleithral ovicell
(Fig. 2.8A ) was probably the plugging of this opening. The
ooecial vesicle as a protective structure could have evolved
as an outgrowth of the non-calcifi ed wall of the maternal
zooid distal to the operculum. Its musculature should then be
homologous with the distalmost parietal muscles of the
zooidal frontal wall.
Acleithral ovicells appear to have evolved early. Judging
from the arrangement of skeletal elements, the ooecial vesicle may have been already present in Wilbertopora and in
several Late Cretaceous cribrimorphs ( Leptocheilopora ,
Pancheilopora , Eucheilopora , Aeolopora ) (see illustrations
in Lang 1921 ).
The next step could be the origin of a cleithral ovicell –
instead of an elastic membrane, the brood-chamber opening
was closed by the operculum of the maternal zooid
(Fig. 2.8B ). This transformation involved the displacement
of the zooidal operculum relative to the ooecium. In the light
of this, it is logical to conclude that semicleithral ovicells
(Figs. 2.7a (I), 2.8C , and 2.28B ) illustrate an intermediate
stage between acleithral and cleithral. Ryland ( 1968 ) had
also considered cleithral ovicell as advanced. Subcleithral
ovicells, in which the operculum lowers to open the entrance
of the ovicell, may be regarded as a cleithral variant
(Fig. 2.8D ). The pseudocleithral ovicell, which Ryland
( 1968 ) considered to be primitive, is a variant of the acleithral
type (Fig. 2.8F ).
It is likely that the ooecial vesicle became less important once the cleithral ovicell appeared. It is the transition
from acleithral to cleithral that may explain a certain
diminution of the ooecial vesicle in Corbulella maderensis compared to Callopora and Tegella ; the ooecial vesicle has a contributory role in ovicell closure in the former,
but closure is most effectively performed by a strongly
cuticularized operculum (Ostrovsky et al. 2009a ) (see
also Fig. 2.22 ). The ooecial vesicle merely isolates the
ovicell cavity from the environment during feeding
excursions of the polypide. In some species with cleithral
and subcleithral ovicells the ooecial vesicle is mostly or
completely reduced.
That the loss of the ooecial vesicle might have been secondary was fi rst mentioned by Santagata and Banta ( 1996 ).
In non-cleithral ovicells the opening should be closed by the
protruding introvert during polypide feeding and open at all
other times. Sections of species with such brood chambers
show that the operculum of the maternal zooid is located
much more proximally than the ovicell opening and cannot
close it (Figs. 2.6b (F), 2.8E , and 2.42 ) (Banta 1977 ). The
reason why some ascophorans abandoned ovicell closure
remains unclear. In some groups this might have been associated with modifi cation of the ovicell opening, such as fl attening (some Phidoloporidae and Celleporidae) or incorporation
into a peristome. In both cases the potential predator is much
less likely to be able to thrust its mouth parts into the brood
cavity. This cannot be said, however, of Lepraliella contigua
and Sinuporaria sp. (Lepraliellidae) – their large brooded
embryos partly protrude from the opening of non-cleithral
ovicells. Note, however, that in species with such brood
chambers the embryos are as a rule surrounded by an especially thick fertilization envelope. Whatever the case, further
evidence supporting the idea that the transition to
non- cleithral ovicells was secondary is the age of the families in which these ovicells occur. The earliest, Lepraliellidae,
evolved in the Santonian, while the next such family,
Phidoloporidae, appeared in the Danian.
The broad occurrence of the ooecial vesicle, its musculature and sclerite in cheilostomes indicates that these three
characters may be synapomorphies of Flustrina. An early
origin of these structures is also indicated by the fact that
2.4 Evolution of Brood Chambers in Cheilostomata
which occurred independently in several cheilostome clades
(Ostrovsky et al. 2006 ).
Interestingly, some families with internal brooding, e.g.,
Cryptosulidae, contain both species with sexual zooidal
dimorphism ( Harmeria ) and without it ( Cryptosula ). This
may also be true of Watersiporidae; Uscia mexicana colonies
form heteromorphic zooids but it is not known if they are
sexual (female) or defensive (avicularian). At the same time,
there are no polymorphs in Watersipora .
The origin of intracoelomic embryo incubation in the
Epistomiidae remains an open question (Marcus 1941b ;
Dyrynda 1981 ; Dyrynda and King 1982 ). This variant may
have evolved through the loss of brooding in ovicells or
internal sacs and a transition to viviparity when cleavage
starts in the ovary. This shift might have somewhat accelerated reproduction, which is important for ephemeral species
such as epistomiids (see Chap. 3 ).
2.4.8.6 Change in the Method of Ovicell Closure
Analysis of the literature supports my own data on the
existence of different modes of ovicell closure in the same
family or genus. For instance, acleithral and cleithral ovicells
are known in the Calloporidae, Flustridae, Bugulidae,
Romancheinidae and Smittinidae. These facts point to
another evolutionary trend frequently manifested within the
Cheilostomata – a change in the ovicell closure mechanism.
One can suggest that the non-cleithral character state
(if not secondary, see below) is plesiomorphic and that
cleithral is apomorphic, whereas all the other states represent
intermediate stages (and their variants) in the evolution of
ovicell closure for better protection of the embryo. The calcifi ed unitary ooecium certainly protects the embryo better
than spinose, and the most vulnerable aspect is the broodchamber opening. The fi rst step towards an acleithral ovicell
(Fig. 2.8A ) was probably the plugging of this opening. The
ooecial vesicle as a protective structure could have evolved
as an outgrowth of the non-calcifi ed wall of the maternal
zooid distal to the operculum. Its musculature should then be
homologous with the distalmost parietal muscles of the
zooidal frontal wall.
Acleithral ovicells appear to have evolved early. Judging
from the arrangement of skeletal elements, the ooecial vesicle may have been already present in Wilbertopora and in
several Late Cretaceous cribrimorphs ( Leptocheilopora ,
Pancheilopora , Eucheilopora , Aeolopora ) (see illustrations
in Lang 1921 ).
The next step could be the origin of a cleithral ovicell –
instead of an elastic membrane, the brood-chamber opening
was closed by the operculum of the maternal zooid
(Fig. 2.8B ). This transformation involved the displacement
of the zooidal operculum relative to the ooecium. In the light
of this, it is logical to conclude that semicleithral ovicells
(Figs. 2.7a (I), 2.8C , and 2.28B ) illustrate an intermediate
stage between acleithral and cleithral. Ryland ( 1968 ) had
also considered cleithral ovicell as advanced. Subcleithral
ovicells, in which the operculum lowers to open the entrance
of the ovicell, may be regarded as a cleithral variant
(Fig. 2.8D ). The pseudocleithral ovicell, which Ryland
( 1968 ) considered to be primitive, is a variant of the acleithral
type (Fig. 2.8F ).
It is likely that the ooecial vesicle became less important once the cleithral ovicell appeared. It is the transition
from acleithral to cleithral that may explain a certain
diminution of the ooecial vesicle in Corbulella maderensis compared to Callopora and Tegella ; the ooecial vesicle has a contributory role in ovicell closure in the former,
but closure is most effectively performed by a strongly
cuticularized operculum (Ostrovsky et al. 2009a ) (see
also Fig. 2.22 ). The ooecial vesicle merely isolates the
ovicell cavity from the environment during feeding
excursions of the polypide. In some species with cleithral
and subcleithral ovicells the ooecial vesicle is mostly or
completely reduced.
That the loss of the ooecial vesicle might have been secondary was fi rst mentioned by Santagata and Banta ( 1996 ).
In non-cleithral ovicells the opening should be closed by the
protruding introvert during polypide feeding and open at all
other times. Sections of species with such brood chambers
show that the operculum of the maternal zooid is located
much more proximally than the ovicell opening and cannot
close it (Figs. 2.6b (F), 2.8E , and 2.42 ) (Banta 1977 ). The
reason why some ascophorans abandoned ovicell closure
remains unclear. In some groups this might have been associated with modifi cation of the ovicell opening, such as fl attening (some Phidoloporidae and Celleporidae) or incorporation
into a peristome. In both cases the potential predator is much
less likely to be able to thrust its mouth parts into the brood
cavity. This cannot be said, however, of Lepraliella contigua
and Sinuporaria sp. (Lepraliellidae) – their large brooded
embryos partly protrude from the opening of non-cleithral
ovicells. Note, however, that in species with such brood
chambers the embryos are as a rule surrounded by an especially thick fertilization envelope. Whatever the case, further
evidence supporting the idea that the transition to
non- cleithral ovicells was secondary is the age of the families in which these ovicells occur. The earliest, Lepraliellidae,
evolved in the Santonian, while the next such family,
Phidoloporidae, appeared in the Danian.
The broad occurrence of the ooecial vesicle, its musculature and sclerite in cheilostomes indicates that these three
characters may be synapomorphies of Flustrina. An early
origin of these structures is also indicated by the fact that
2.4 Evolution of Brood Chambers in Cheilostomata