271
eventually resulted in the origin of specialized gonozooids
– infl ated voluminous chambers for embryonic incubation.
At the same time, the paleontological record contains indications that stenolaemates may have evolved polyembryony
much earlier. Buttler ( 1991 ) suggested that the shape and
size of putative brood chambers in Cystoporata could indicate polyembryony. McKinney ( 1981 ) found several colonies of Permian fenestrates that were the product of fusion
of two individuals, each presumably originating from a
genetically identical larva, suggesting the existence of polyembryony (although the skeletal brood chambers of fenestrates are not very large). Pachut and Fisherkeller ( 2010 ),
however, have argued that polyembryony evolved only
once. At the same time, polyembryony, as well as endotrophy with brooding, could have evolved independently in different stenolaemate orders.
To note, polyembryony resulted in a reduction of the
number of reproducing zooids. Most cyclostome colonies
have only a single gonozooid (Borg 1926 ; Hayward and
Ryland 1985 ; Schäfer 1991 ; Ostrovsky and Taylor 1996 ;
Ostrovsky 1998a , b ), and all the free resources of the colony
are probably channelled towards its needs. Instead of forming and supporting numerous small incubation chambers,
most of these bryozoans form a single one or just a few.
The above examples indicate that almost all variants of
embryonic incubation found in phylactolaemates, cyclostomes and ctenostomes are either intracoelomic or intrazooidal. In other words, it seems that the evolution of
incubation in these groups was predetermined by the
absence of structures that could be used for “constructing”
external brood chambers. Curiously, subsequent to the evolution of external brooding in cheilostomes, there have been
multiple transitions to internal brooding in this order
(Ostrovsky et al. 2009c ).
It is important to stress here that extraembryonic nutrition
and placental analogues evolved in all bryozoan classes.
They are found in all living Cyclostomata and Phylactolaemata
as well as in many Ctenostomata and Cheilostomata.
Jablonski et al. ( 1997 ) posited that Taylor’s ( 1988a )
hypothesis concerning the role of the endotrophic larva in
cheilostome evolution is contradicted by the fact that cyclostome bryozoans, having acquired a gonozooid (and hence
an endotrophic larva) in the Late Triassic, later underwent
only a modest diversifi cation (see also Taylor and Larwood
1990 ; Lidgard et al. 1993 ). Nevertheless, judging from
published data (Taylor and Larwood 1990 ; Lidgard et al.
1993 ; Jablonski et al. 1997 ; McKinney et al. 1998 ; Sepkoski
et al. 2000 ), this diversifi cation was the most dramatic evolutionary event in the whole history of the order. McKinney
and Taylor ( 2001 ) showed that the rates of increase of taxonomic diversity in the Cyclostomata and Cheilostomata in
the Late Cretaceous were similar. In the opinion of Taylor
and Larwood ( 1990 ), there were three major radiations in
the history of the phylum – in the Ordovician (Stenolaemata),
the Middle Mesozoic (Cyclostomata) and the Late
Mesozoic (Cheilostomata). These authors speculated that
all three radiations may have been the consequence of the
origin of a lecithotrophic larva. As shown above, the origin
of structures for embryonic incubation (both putative and
real) is generally in concert with this hypothesis, however
our present knowledge is not suffi cient to venture any further guesses.
3.6
Conclusion
Several reproductive patterns evolved during the history of
the bryozoan order Cheilostomata. The transition from
planktotrophy to lecithotrophy (from pattern I to pattern II)
was based on modifi cation of oogenesis, expressed in
increased oocyte size resulting from accumulation of
more nutrients. Additional consequences of this transition
were a decrease in the number of maturing oocytes formed
by a zooid, a shift to sequential (asynchronous) maturation, a
change in ovarian structure and a change in larval structure
and life span.
The structure of the brood chambers shows that within
this order parental care evolved independently during the rise
of the families Aeteidae, Scrupariidae (possibly twice),
Calloporidae, Tendridae, Thalamoporellidae and Alysidiidae
as well as in “ Carbasea ” indivisa and Bellulopora . This
means that suborder Flustrina is not monophyletic. Since
there are no known cheilostomes combining both the broadcasting reproductive pattern and non-feeding larva, in all of
the above examples their ancestors should be non-brooding
malacostegans with a planktotrophic larva (or possibly a
ctenostome in the case of Aeteidae). Thus, lecithotrophy also
evolved in the Cheilostomata numerous times. Accordingly,
three new suborders Tendrina, Thalamoporellina and
Belluloporina have been newly introduced herein. Alysidiidae
and “ C .” indivisa most likely deserve the same treatment.
The evolution of brooding always accompanied a shift to
lecithotrophy, possibly compensating for the reduction in the
number of offspring. Some of the groups later independently
evolved extraembryonic nutrition, which also entailed modifi cation of oogenesis, shifting from pattern II to pattern IV
and the latter to pattern III. Additionally, the transition from
intracoelomic to early intraovarian fertilization took place,
becoming the trigger for vitellogenesis. The acquisition of
nurse cells may have been the consequence of a transition to
early syngamy, which precluded the completion of oogonial
cytokinesis.
Brood chambers evolved in Cheilostomata repeatedly, on
the basis of modifi cations to spines, kenozooids, outgrowths
(outfolds) of the zooidal wall or the fertilization envelope. In
almost all cheilostome ovicells ooecia are not heterozooids
3.6 Conclusion
eventually resulted in the origin of specialized gonozooids
– infl ated voluminous chambers for embryonic incubation.
At the same time, the paleontological record contains indications that stenolaemates may have evolved polyembryony
much earlier. Buttler ( 1991 ) suggested that the shape and
size of putative brood chambers in Cystoporata could indicate polyembryony. McKinney ( 1981 ) found several colonies of Permian fenestrates that were the product of fusion
of two individuals, each presumably originating from a
genetically identical larva, suggesting the existence of polyembryony (although the skeletal brood chambers of fenestrates are not very large). Pachut and Fisherkeller ( 2010 ),
however, have argued that polyembryony evolved only
once. At the same time, polyembryony, as well as endotrophy with brooding, could have evolved independently in different stenolaemate orders.
To note, polyembryony resulted in a reduction of the
number of reproducing zooids. Most cyclostome colonies
have only a single gonozooid (Borg 1926 ; Hayward and
Ryland 1985 ; Schäfer 1991 ; Ostrovsky and Taylor 1996 ;
Ostrovsky 1998a , b ), and all the free resources of the colony
are probably channelled towards its needs. Instead of forming and supporting numerous small incubation chambers,
most of these bryozoans form a single one or just a few.
The above examples indicate that almost all variants of
embryonic incubation found in phylactolaemates, cyclostomes and ctenostomes are either intracoelomic or intrazooidal. In other words, it seems that the evolution of
incubation in these groups was predetermined by the
absence of structures that could be used for “constructing”
external brood chambers. Curiously, subsequent to the evolution of external brooding in cheilostomes, there have been
multiple transitions to internal brooding in this order
(Ostrovsky et al. 2009c ).
It is important to stress here that extraembryonic nutrition
and placental analogues evolved in all bryozoan classes.
They are found in all living Cyclostomata and Phylactolaemata
as well as in many Ctenostomata and Cheilostomata.
Jablonski et al. ( 1997 ) posited that Taylor’s ( 1988a )
hypothesis concerning the role of the endotrophic larva in
cheilostome evolution is contradicted by the fact that cyclostome bryozoans, having acquired a gonozooid (and hence
an endotrophic larva) in the Late Triassic, later underwent
only a modest diversifi cation (see also Taylor and Larwood
1990 ; Lidgard et al. 1993 ). Nevertheless, judging from
published data (Taylor and Larwood 1990 ; Lidgard et al.
1993 ; Jablonski et al. 1997 ; McKinney et al. 1998 ; Sepkoski
et al. 2000 ), this diversifi cation was the most dramatic evolutionary event in the whole history of the order. McKinney
and Taylor ( 2001 ) showed that the rates of increase of taxonomic diversity in the Cyclostomata and Cheilostomata in
the Late Cretaceous were similar. In the opinion of Taylor
and Larwood ( 1990 ), there were three major radiations in
the history of the phylum – in the Ordovician (Stenolaemata),
the Middle Mesozoic (Cyclostomata) and the Late
Mesozoic (Cheilostomata). These authors speculated that
all three radiations may have been the consequence of the
origin of a lecithotrophic larva. As shown above, the origin
of structures for embryonic incubation (both putative and
real) is generally in concert with this hypothesis, however
our present knowledge is not suffi cient to venture any further guesses.
3.6
Conclusion
Several reproductive patterns evolved during the history of
the bryozoan order Cheilostomata. The transition from
planktotrophy to lecithotrophy (from pattern I to pattern II)
was based on modifi cation of oogenesis, expressed in
increased oocyte size resulting from accumulation of
more nutrients. Additional consequences of this transition
were a decrease in the number of maturing oocytes formed
by a zooid, a shift to sequential (asynchronous) maturation, a
change in ovarian structure and a change in larval structure
and life span.
The structure of the brood chambers shows that within
this order parental care evolved independently during the rise
of the families Aeteidae, Scrupariidae (possibly twice),
Calloporidae, Tendridae, Thalamoporellidae and Alysidiidae
as well as in “ Carbasea ” indivisa and Bellulopora . This
means that suborder Flustrina is not monophyletic. Since
there are no known cheilostomes combining both the broadcasting reproductive pattern and non-feeding larva, in all of
the above examples their ancestors should be non-brooding
malacostegans with a planktotrophic larva (or possibly a
ctenostome in the case of Aeteidae). Thus, lecithotrophy also
evolved in the Cheilostomata numerous times. Accordingly,
three new suborders Tendrina, Thalamoporellina and
Belluloporina have been newly introduced herein. Alysidiidae
and “ C .” indivisa most likely deserve the same treatment.
The evolution of brooding always accompanied a shift to
lecithotrophy, possibly compensating for the reduction in the
number of offspring. Some of the groups later independently
evolved extraembryonic nutrition, which also entailed modifi cation of oogenesis, shifting from pattern II to pattern IV
and the latter to pattern III. Additionally, the transition from
intracoelomic to early intraovarian fertilization took place,
becoming the trigger for vitellogenesis. The acquisition of
nurse cells may have been the consequence of a transition to
early syngamy, which precluded the completion of oogonial
cytokinesis.
Brood chambers evolved in Cheilostomata repeatedly, on
the basis of modifi cations to spines, kenozooids, outgrowths
(outfolds) of the zooidal wall or the fertilization envelope. In
almost all cheilostome ovicells ooecia are not heterozooids
3.6 Conclusion