261
1960 ; Hayward 1985 ). Because the polypide degenerates,
the mature oocyte is not released in the environment and gets
from the maternal coelom into the pouch via the ciliated funnel that is formed.
Judging from the distribution of the reproductive patterns across the Ctenostomata, brooding in the introvert has
also independently evolved in several other ctenostome
superfamilies: Vesicularioidea (described in Bowerbankia
gracilis , B . pustulosa , B . imbricata , Amathia lendigera , A .
semiconvoluta , Vesicularia spinosa , Buskia nitens ),
Walkerioidea ( Walkeria ), Terebriporoidea ( Terebripora sp.,
Spathipora comma , S . mazatlanica ) and Victorelloidea
( Immergentia suecica ) (Joliet 1877 ; Braem 1951 ; Reed
1988 ; Calvet 1900 ; Bobin and Prenant 1954 ; Prenant and
Bobin 1956 ; Soule and Soule 1969a , 1975 , 1976 ; Ström
1977 ; Hayward 1985 ). All these species brood one embryo
at a time.
The brooding of embryos in introverts, as with brooding in invaginations of the body wall, is a precursor to
matrotrophy. Increase in embryo size is known in Walkeria
uva and Bantariella cookae (Walkerioidea) and in
Zoobotryon verticillatum (Vesicularioidea) (Joliet 1877 ;
Waters 1900 ; Zirpolo 1933 ; Banta 1968 ; Ström 1977 ;
Ostrovsky et al. 2008a ; Ostrovsky and Schwaha 2011 ).
Judging from the considerable enlargement of their
embryos during brooding, these species have reproductive
pattern III. Embryo enlargement has also been noted in
Flustrellidra hispida (Alcyonidioidea), in which 4–8
embryos develop in the introvert (Prouho 1889 ; Pace
1906 ; Hayward 1985 ) but this species has macrolecithal
(though not large) oocytes and thus conforms to reproductive pattern IV.
(4) Boring ctenostomes of the genus Penetrantia
(Penetrantiina) evolved yet another incubational variant,
brooding embryos one at a time in an unusual outer embryo
sac of which the structure and development are poorly known
(Silén 1947 ; Soule 1950b ; Soule and Soule 1969a , b , 1975 ;
Ström 1977 ). Also, data on oogenesis in this group are virtually non-existent.
Thus, the trends in the evolution of sexual reproduction in
Ctenostomata associated with brooding were as follows:
• an increase in oocyte size – from small oocytes (30–
90 μm) in broadcasters towards larger ones (65–370 μm)
in brooders (and, as a consequence, a transition from
planktotrophic to lecithotrophic larvae);
• an overall decrease in the number of gametes formed in
the ovary as well as a decrease in the number of maturing
oocytes;
• a transition from a group mode to an “individual” mode of
oocyte maturation, ovulation and release/oviposition;
• a transition from external to “mixed” brooding and to
internal brooding in the introvert, or from external brooding to brooding in an invagination of the body wall;
• the origin of extraembryonic nutrition.
Apart from the trends associated with the evolution of
brooding, this list closely resembles those in the order
Cheilostomata (see Sects. 3.1 and 3.3 ).
The diversity of brooding modes in the order Ctenostomata
illustrates two trends in the evolution of parental care (Braem
1951 ; Ström 1977 ; Jebram 1985 ; Smith et al. 2003 ).
Ctenostomes lack both a rigid skeleton and structures that
could serve as a basis for the formation of protective brood
chambers. This may be the reason why their brooding evolved
towards “intrazooidal” incubation, that is, (1) transfer of
embryos into body-wall invaginations or (2) the introvert cavity. Interestingly, no viviparous ctenostomes have been found.
The simplest and least-reliable brooding mode is that of
attaching adhesive fertilization envelopes of the released
oocytes to the cystid or the introvert of the maternal zooid.
This primitive variant was the basis for the evolution of two
more-advanced ones, when oocytes attached to the cystid
wall are submerged into its invaginations or are transferred
into the vestibulum cavity during retraction of the polypide.
The origin of such specialized behaviour as the polypide
attaching eggs specifi cally to the protruding introvert in
Bulbella abscondita , Tanganella muelleri and Alcyonidium
duplex (see Prouho 1892 ; Braem 1951 ) was a prerequisite of
“internal” brooding, since the retraction of the polypide
entailed transfer of the attached eggs into the vestibulum
cavity. In T . muelleri , embryos are in addition submerged
into the vestibulum wall, after which the polypide degenerates. “Mixed” brooding, exemplifi ed by B . abscondita and A .
duplex , characterizes an intermediate stage in the evolution
of “internal” brooding (see Braem 1951 ); the polypide continues to function and the embryos remain in the vestibulum
only when the polypide is retracted. Additionally it should
be stressed here that these two species possess an intertentacular organ, the larva of B . abscondita has a rudimentary
gut and the gutless larva of A . duplex has a triangular
cyphonautes shape (Prouho 1892 ; Braem 1951 ; Zimmer and
Woollacott 1977a ), all clearly pointing to an independent
transition to lecitotrophy accompanied by the evolution of
embryonic brooding.
Thus, fertilized ovulated eggs were initially transferred
into the introvert cavity by the polypide. In the more advanced
variant, oocytes were transferred into the brood cavity without leaving the cystid. Polypide degeneration and obligatory
brooding (either in the vestibulum cavity or in a specialized
chamber substituting for the introvert) resulted in physical
isolation of the embryo from a range of impacts. Some
ctenostomes brood several embryos at a time whereas in others a single large embryo develops in the introvert. These
differences appear to be explained by differences in oogenesis and in the capacity of the introvert – the more nutrients
are accumulated in oocytes, the fewer eggs may be formed
and brooded in a zooid. In Alcyonidium gelatinosum the
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata
1960 ; Hayward 1985 ). Because the polypide degenerates,
the mature oocyte is not released in the environment and gets
from the maternal coelom into the pouch via the ciliated funnel that is formed.
Judging from the distribution of the reproductive patterns across the Ctenostomata, brooding in the introvert has
also independently evolved in several other ctenostome
superfamilies: Vesicularioidea (described in Bowerbankia
gracilis , B . pustulosa , B . imbricata , Amathia lendigera , A .
semiconvoluta , Vesicularia spinosa , Buskia nitens ),
Walkerioidea ( Walkeria ), Terebriporoidea ( Terebripora sp.,
Spathipora comma , S . mazatlanica ) and Victorelloidea
( Immergentia suecica ) (Joliet 1877 ; Braem 1951 ; Reed
1988 ; Calvet 1900 ; Bobin and Prenant 1954 ; Prenant and
Bobin 1956 ; Soule and Soule 1969a , 1975 , 1976 ; Ström
1977 ; Hayward 1985 ). All these species brood one embryo
at a time.
The brooding of embryos in introverts, as with brooding in invaginations of the body wall, is a precursor to
matrotrophy. Increase in embryo size is known in Walkeria
uva and Bantariella cookae (Walkerioidea) and in
Zoobotryon verticillatum (Vesicularioidea) (Joliet 1877 ;
Waters 1900 ; Zirpolo 1933 ; Banta 1968 ; Ström 1977 ;
Ostrovsky et al. 2008a ; Ostrovsky and Schwaha 2011 ).
Judging from the considerable enlargement of their
embryos during brooding, these species have reproductive
pattern III. Embryo enlargement has also been noted in
Flustrellidra hispida (Alcyonidioidea), in which 4–8
embryos develop in the introvert (Prouho 1889 ; Pace
1906 ; Hayward 1985 ) but this species has macrolecithal
(though not large) oocytes and thus conforms to reproductive pattern IV.
(4) Boring ctenostomes of the genus Penetrantia
(Penetrantiina) evolved yet another incubational variant,
brooding embryos one at a time in an unusual outer embryo
sac of which the structure and development are poorly known
(Silén 1947 ; Soule 1950b ; Soule and Soule 1969a , b , 1975 ;
Ström 1977 ). Also, data on oogenesis in this group are virtually non-existent.
Thus, the trends in the evolution of sexual reproduction in
Ctenostomata associated with brooding were as follows:
• an increase in oocyte size – from small oocytes (30–
90 μm) in broadcasters towards larger ones (65–370 μm)
in brooders (and, as a consequence, a transition from
planktotrophic to lecithotrophic larvae);
• an overall decrease in the number of gametes formed in
the ovary as well as a decrease in the number of maturing
oocytes;
• a transition from a group mode to an “individual” mode of
oocyte maturation, ovulation and release/oviposition;
• a transition from external to “mixed” brooding and to
internal brooding in the introvert, or from external brooding to brooding in an invagination of the body wall;
• the origin of extraembryonic nutrition.
Apart from the trends associated with the evolution of
brooding, this list closely resembles those in the order
Cheilostomata (see Sects. 3.1 and 3.3 ).
The diversity of brooding modes in the order Ctenostomata
illustrates two trends in the evolution of parental care (Braem
1951 ; Ström 1977 ; Jebram 1985 ; Smith et al. 2003 ).
Ctenostomes lack both a rigid skeleton and structures that
could serve as a basis for the formation of protective brood
chambers. This may be the reason why their brooding evolved
towards “intrazooidal” incubation, that is, (1) transfer of
embryos into body-wall invaginations or (2) the introvert cavity. Interestingly, no viviparous ctenostomes have been found.
The simplest and least-reliable brooding mode is that of
attaching adhesive fertilization envelopes of the released
oocytes to the cystid or the introvert of the maternal zooid.
This primitive variant was the basis for the evolution of two
more-advanced ones, when oocytes attached to the cystid
wall are submerged into its invaginations or are transferred
into the vestibulum cavity during retraction of the polypide.
The origin of such specialized behaviour as the polypide
attaching eggs specifi cally to the protruding introvert in
Bulbella abscondita , Tanganella muelleri and Alcyonidium
duplex (see Prouho 1892 ; Braem 1951 ) was a prerequisite of
“internal” brooding, since the retraction of the polypide
entailed transfer of the attached eggs into the vestibulum
cavity. In T . muelleri , embryos are in addition submerged
into the vestibulum wall, after which the polypide degenerates. “Mixed” brooding, exemplifi ed by B . abscondita and A .
duplex , characterizes an intermediate stage in the evolution
of “internal” brooding (see Braem 1951 ); the polypide continues to function and the embryos remain in the vestibulum
only when the polypide is retracted. Additionally it should
be stressed here that these two species possess an intertentacular organ, the larva of B . abscondita has a rudimentary
gut and the gutless larva of A . duplex has a triangular
cyphonautes shape (Prouho 1892 ; Braem 1951 ; Zimmer and
Woollacott 1977a ), all clearly pointing to an independent
transition to lecitotrophy accompanied by the evolution of
embryonic brooding.
Thus, fertilized ovulated eggs were initially transferred
into the introvert cavity by the polypide. In the more advanced
variant, oocytes were transferred into the brood cavity without leaving the cystid. Polypide degeneration and obligatory
brooding (either in the vestibulum cavity or in a specialized
chamber substituting for the introvert) resulted in physical
isolation of the embryo from a range of impacts. Some
ctenostomes brood several embryos at a time whereas in others a single large embryo develops in the introvert. These
differences appear to be explained by differences in oogenesis and in the capacity of the introvert – the more nutrients
are accumulated in oocytes, the fewer eggs may be formed
and brooded in a zooid. In Alcyonidium gelatinosum the
3.4 Causes, Stages and Consequences of Transition to Endotrophy in Cheilostomata and Ctenostomata