262
brood cavity is enlarged by means of a voluminous brood
pouch developed in place of the degenerated tentacle sheath.
In addition, this species has a ciliated funnel facilitating the
transfer of oocytes to the place of brooding.
Imperfect as it may have been, attachment of zygotes to
the surface of the spinose distal zooid in primitive brooding
cheilostomes undoubtedly provided a degree of protection
and may thus be considered as a form of parental care.
Perhaps the presence of spines may have prevented cheilostomes from evolving brooding within the introvert. On the
other hand, should we consider the attachment of oocytes to
a spineless zooidal surface, as occurs in some cheilostome
and ctenostome species, a form of brooding? Such attachment provides no mechanical protection but may ensure, for
instance, that the zygotes do not fall onto an inhospitable
substratum prior to becoming motile (Note that, in contrast
to the embryos of endotrophic larvae, those of planktotrophic larvae become motile very soon). In Bulbella abscondita ,
zygotes detached from the zooid reportedly cease to develop
(Braem 1951 ), but the reasons for this are unknown and the
data need verifying. In the ctenostome Triticella fl ava and
the cheilostome Tendra zostericola , eggs develop normally
even after removal from the brood chamber (Ström 1969 ;
Braiko 1967 ), but such zygotes would have little chance of
surviving in nature and any form of brooding is likely to
result in a considerably higher survival rate.
It is suggested here that the adhesive properties of the fertilization envelope that sticks to the zooidal wall after egg
release could be a result of changes in the chemical composition of oocytes during transition to a new mode of oogenesis.
Such adhesive envelopes are known in different groups of vertebrates and invertebrates (Adiyodi and Adiyodi 1989 , 1990 ;
Lombardi 1998 ). In malacostracan crustaceans, for instance,
such eggs are brooded and develop into late larvae (Adiyodi
and Subramoniam 1983 ), testifying to the high nutrient content in oocytes. In bryozoans, oocytes with an increased
amount of yolk (the basis for transition to endotrophy) could
adhere to the maternal colony to develop on its surface. As
noted above, bryozoans with this type of brooding, as well as
all the other brooding species, have non- feeding larvae. The
subsequent emergence of brood chambers in cheilostomes,
and brooding in the modifi ed introvert or body-wall invaginations in ctenostomes, facilitated better protection of embryos.
Thus, modifi cation of oogenesis would be conducive to retention of embryos in the colony as a precondition for the origin
of brooding – supporting the hypothesis that modifi cation of
oogenesis preceded the origin of brooding.
3.4.4.2 Parallel Evolution of Sexual Reproduction
in Different Superfamilies of
Ctenostomata
The general trends that have emerged so far – the shift from
broadcasting to brooding and the increase in oocyte size
accompanied by decrease in oocyte number – give insight
into the evolution of sexual reproduction in the different
superfamilies of Ctenostomata.
The known ctenostome superfamilies apparently differentiated as early as the lower Paleozoic – in the Early
Ordovician according to Todd ( 2000 ). The distribution of
larval types and modes of parental care within these superfamilies, as well as their positions in the phylogenetic tree,
show that ctenostomes evolved lecithotrophic larvae and
brooding several times [at least fi ve times judging from the
data in Ström ( 1977 ), Zimmer and Woollacott ( 1977a ) and
Todd ( 2000 )]. The superfamilies Alcyonidioidea (one of the
basal groups), Victorelloidea and Walkerioidea (terminal
groups) comprise both brooders and species with
cyphonautes larvae, with brooders constituting the majority.
According to Todd ( 2000 ), Walkerioidea and Victorelloidea
are sister groups of the superfamily Vesicularioidea, which
comprises brooders only. If so, then the common ancestor of
these three families had a planktotrophic larva that was lost
independently (in connection with the evolution of brooding) in each of the clades. Unfortunately, almost nothing is
known about reproduction in the superfamilies Hislopioidea
and Arachnidioidea apart from the facts that the freshwater
genus Hislopia has a cyphonautes larva (Wood 2008 ) and
Cryptoarachnidium argilla has an intertentacular organ, i.e.
is supposedly a broadcaster (Banta 1967 ); thus both superfamilies comprise species with a planktotrophic larva and
reproductive pattern I. In the superfamily Paludicelloidea,
only primitive external brooding has been described (Braem
1896 ). Thus, parental care has been recorded in representatives of fi ve out of seven ctenostome superfamilies, as well
as in Labiostomella , which according to Todd ( 2000 ) groups
with Protoctenostomata. Three of them include species with
embryonic incubation as well as broadcasting, pointing to at
least three instances of independent evolution of parental
care and non-feeding larvae among ctenostomes. However,
since such groups have both basal (Alcyonioidea) and terminal (Walkerioidea, Victorelloidea) positions on the ctenostome phylogenetic tree, it seems that this happened six
times in this order.
Within the Alcyonidioidea, independently evolved lecithotrophy and brooding characterizes the family Alcyonidiidae
and the genus Alcyonidium . The latter is a very rare example
of a bryozoan genus with both planktotrophic and lecithotrophic larvae and patterns I and II. Moreover, in Alcyonidium
duplex , a brooder with a lecithotrophic larva, oviposition
occurs via the intertentacular organ, as in non- brooding bryozoans, and its larva has a triangular cyphonautes shape (Farre
1837 ; Prouho 1892 ). Alcyonidium species also demonstrate
two brooding variants (brooding in the introvert and “mixed”
brooding) and different modes of oogenesis, corresponding to
the above-discussed trends towards the formation of fewer,
larger oocytes. Flustrellidra hispida (Flustrellidridae), which
3 Evolution of Reproductive Patterns in Cheilostomata
brood cavity is enlarged by means of a voluminous brood
pouch developed in place of the degenerated tentacle sheath.
In addition, this species has a ciliated funnel facilitating the
transfer of oocytes to the place of brooding.
Imperfect as it may have been, attachment of zygotes to
the surface of the spinose distal zooid in primitive brooding
cheilostomes undoubtedly provided a degree of protection
and may thus be considered as a form of parental care.
Perhaps the presence of spines may have prevented cheilostomes from evolving brooding within the introvert. On the
other hand, should we consider the attachment of oocytes to
a spineless zooidal surface, as occurs in some cheilostome
and ctenostome species, a form of brooding? Such attachment provides no mechanical protection but may ensure, for
instance, that the zygotes do not fall onto an inhospitable
substratum prior to becoming motile (Note that, in contrast
to the embryos of endotrophic larvae, those of planktotrophic larvae become motile very soon). In Bulbella abscondita ,
zygotes detached from the zooid reportedly cease to develop
(Braem 1951 ), but the reasons for this are unknown and the
data need verifying. In the ctenostome Triticella fl ava and
the cheilostome Tendra zostericola , eggs develop normally
even after removal from the brood chamber (Ström 1969 ;
Braiko 1967 ), but such zygotes would have little chance of
surviving in nature and any form of brooding is likely to
result in a considerably higher survival rate.
It is suggested here that the adhesive properties of the fertilization envelope that sticks to the zooidal wall after egg
release could be a result of changes in the chemical composition of oocytes during transition to a new mode of oogenesis.
Such adhesive envelopes are known in different groups of vertebrates and invertebrates (Adiyodi and Adiyodi 1989 , 1990 ;
Lombardi 1998 ). In malacostracan crustaceans, for instance,
such eggs are brooded and develop into late larvae (Adiyodi
and Subramoniam 1983 ), testifying to the high nutrient content in oocytes. In bryozoans, oocytes with an increased
amount of yolk (the basis for transition to endotrophy) could
adhere to the maternal colony to develop on its surface. As
noted above, bryozoans with this type of brooding, as well as
all the other brooding species, have non- feeding larvae. The
subsequent emergence of brood chambers in cheilostomes,
and brooding in the modifi ed introvert or body-wall invaginations in ctenostomes, facilitated better protection of embryos.
Thus, modifi cation of oogenesis would be conducive to retention of embryos in the colony as a precondition for the origin
of brooding – supporting the hypothesis that modifi cation of
oogenesis preceded the origin of brooding.
3.4.4.2 Parallel Evolution of Sexual Reproduction
in Different Superfamilies of
Ctenostomata
The general trends that have emerged so far – the shift from
broadcasting to brooding and the increase in oocyte size
accompanied by decrease in oocyte number – give insight
into the evolution of sexual reproduction in the different
superfamilies of Ctenostomata.
The known ctenostome superfamilies apparently differentiated as early as the lower Paleozoic – in the Early
Ordovician according to Todd ( 2000 ). The distribution of
larval types and modes of parental care within these superfamilies, as well as their positions in the phylogenetic tree,
show that ctenostomes evolved lecithotrophic larvae and
brooding several times [at least fi ve times judging from the
data in Ström ( 1977 ), Zimmer and Woollacott ( 1977a ) and
Todd ( 2000 )]. The superfamilies Alcyonidioidea (one of the
basal groups), Victorelloidea and Walkerioidea (terminal
groups) comprise both brooders and species with
cyphonautes larvae, with brooders constituting the majority.
According to Todd ( 2000 ), Walkerioidea and Victorelloidea
are sister groups of the superfamily Vesicularioidea, which
comprises brooders only. If so, then the common ancestor of
these three families had a planktotrophic larva that was lost
independently (in connection with the evolution of brooding) in each of the clades. Unfortunately, almost nothing is
known about reproduction in the superfamilies Hislopioidea
and Arachnidioidea apart from the facts that the freshwater
genus Hislopia has a cyphonautes larva (Wood 2008 ) and
Cryptoarachnidium argilla has an intertentacular organ, i.e.
is supposedly a broadcaster (Banta 1967 ); thus both superfamilies comprise species with a planktotrophic larva and
reproductive pattern I. In the superfamily Paludicelloidea,
only primitive external brooding has been described (Braem
1896 ). Thus, parental care has been recorded in representatives of fi ve out of seven ctenostome superfamilies, as well
as in Labiostomella , which according to Todd ( 2000 ) groups
with Protoctenostomata. Three of them include species with
embryonic incubation as well as broadcasting, pointing to at
least three instances of independent evolution of parental
care and non-feeding larvae among ctenostomes. However,
since such groups have both basal (Alcyonioidea) and terminal (Walkerioidea, Victorelloidea) positions on the ctenostome phylogenetic tree, it seems that this happened six
times in this order.
Within the Alcyonidioidea, independently evolved lecithotrophy and brooding characterizes the family Alcyonidiidae
and the genus Alcyonidium . The latter is a very rare example
of a bryozoan genus with both planktotrophic and lecithotrophic larvae and patterns I and II. Moreover, in Alcyonidium
duplex , a brooder with a lecithotrophic larva, oviposition
occurs via the intertentacular organ, as in non- brooding bryozoans, and its larva has a triangular cyphonautes shape (Farre
1837 ; Prouho 1892 ). Alcyonidium species also demonstrate
two brooding variants (brooding in the introvert and “mixed”
brooding) and different modes of oogenesis, corresponding to
the above-discussed trends towards the formation of fewer,
larger oocytes. Flustrellidra hispida (Flustrellidridae), which
3 Evolution of Reproductive Patterns in Cheilostomata