270
phylactolaemates possibly have nurse cells (Marcus 1934 ;
see also Sect. 3.2 ).
I would like to note that the data presented in this book
call for a reconsideration of the defi nitions of reproductive
patterns II, III and IV. In Gymnolaemata, pattern II should
include all cases of non-matrotrophic brooding, and patterns
III and IV all cases of placental brooding combined with,
correspondingly, oligo-/meso- and macrolecithal oogenesis.
At the same time, the number of oocytes may vary
considerably.
As for the class Stenolaemata, the reproductive pattern of
Recent Cyclostomata (viviparity) is similar to pattern V in
the cheilostome family Epistomiidae. Undoubtedly, this is an
example of convergence. Having found that ancestrula size is
similar in Recent and fossil stenolaemates, Pachut and
Fisherkeller ( 2010 ) suggested that polyembryony is a monophyletic trait in this class. This leads to the conclusion that
incubation and the endotrophic larva in general have evolved
in the class only once.
Branching structures in Cystoporata, stenolaemates from
the Late Ordovician, are considered as chambers for embryonic incubation (Buttler 1991 ; see also Taylor and Larwood
1990 ). If so, non-feeding larvae evolved at least by the Late
Ordovician in stenolaemates. Chambers for embryonic incubation (termed ovicells) have often been reported in
Fenestrata (Stratton 1975 , 1981 ; Southwood 1985 ; Bancroft
1986 ; Morozova 2001 ). However, judging from their structure and the suggested relationships between these two
Paleozoic stenolaemate orders (McKinney 2000 ), they are
unlikely to be homologous with the putative incubation
chambers of cystoporates. In Cyclostomata, zooids for
embryonic incubation (gonozooids) originated as late as the
Late Triassic (Taylor and Michalik 1991 ). Thus, incubation
structures seem to be not homologous within this class.
On the other hand, incubation itself would have originated
only once. Early stenolaemates, including Paleozoic cyclostomes, could have retained non-feeding larvae in the peristome, the distal part of the cylindrical autotozooid (Borg
1926 ; Taylor and Larwood 1990 ). If so, and if endotrophy
evolved only once in Stenolaemata (or was inherited from an
ancestor), embryonic incubation in the specialized chambers
originated independently at different times in different
stenolaemate orders on the basis of incubation in nonmodifi ed zooids. Of course, this conclusion would also hold
true if the endotrophic larva evolved several times in stenolaemates, as was apparently the case in gymnolaemates.
It is not known if Paleozoic cyclostomes incubated their
progeny, allowing the possibility that they might have
evolved an endotrophic larva much later, when gonozooids
evolved. Before that their larvae may have been planktotrophic, as indicted by the low taxonomic diversity of this group
in the Paleozoic (Ernst and Schäfer 2006 ). In contrast, other
Paleozoic stenolaemate orders were rather species-rich and
hence possibly had a non-feeding larva. Finally, cyclostomes
may be polyphyletic; they may have evolved from two different ctenostome ancestors (Ernst and Schäfer 2006 ), and
those that evolved in the Mesozoic would then have newly
acquired gonozooids, endotrophy and polyembryony.
Whatever the case, Cyclostomata evolved viviparity, that
is, intracoelomic incubation of embryos accompanied by
extraembryonic nutrition. The sequence of evolutionary
events may have been similar to the case of Ctenostomata
(see above), involving external brooding by means of adhesion of embryos to the lophophore, retraction of embryos
into the introvert (“mixed” brooding), obligatory brooding in
the tentacle sheath accompanied by polypide degeneration
and, fi nally, embryonic development in the coelomic cavity
of the zooids and then in the ovary. A similar scenario (except
for brooding in the tentacle sheath) appears possible in the
Epistomiidae, whose ancestors probably brooded their
embryos in ovicells.
The presence of only one or two oocytes in the ovary may
indicate that viviparity was accompanied by a decrease in the
number of eggs, initially numerous in cyclostomes. It is diffi cult to say whether this decrease was the consequence of
oocyte enlargement during transition to a non-feeding larva,
or suppression of oogonial division in the ovary during the
shift to intraovarian embryogenesis, or both. In the former
case, viviparity could result from a stepwise change from
simple to complex forms of embryonic incubation accompanied by gradual increase in the amount of reserves in the
oocytes and reduction in their numbers (as in gymnolaemates). In the latter case, early onset of oocyte division in the
ovary would have also resulted in a reduction in oocyte number. Actually, both mechanisms could have been involved,
and subsequent evolution of matrotrophy might have promoted a return to yolk-poor eggs. A transition from postovulatory intracoelomic fertilization to an early intraovarian
mode could have induced the beginning of division directly
in the ovary.
If these assumptions are correct, then evolution of the
reproductive pattern in Cyclostomata could have followed
the same trajectory as the transition from reproductive pattern II (as described for cheilostomes) to pattern III. A transition from pattern I is unlikely. In my opinion, the characteristic
set of “cyclostome” reproductive traits, involving intraovarian embryogenesis and polyembryony, merits the status of a
separate reproductive pattern VI.
An embryo developing in the ovary could be provided
with additional nutrients; instead of forming new oocytes,
the ovary “feeds” a single embryo. Moreover, because the
cylindrical zooids of cyclostomes can elongate over an
extended period, the developing embryos would be afforded
more space relative to the brood chambers of gymnolaemates. Both of these factors could precondition the origin of
polyembryony in Cyclostomata. This event could have
3 Evolution of Reproductive Patterns in Cheilostomata
phylactolaemates possibly have nurse cells (Marcus 1934 ;
see also Sect. 3.2 ).
I would like to note that the data presented in this book
call for a reconsideration of the defi nitions of reproductive
patterns II, III and IV. In Gymnolaemata, pattern II should
include all cases of non-matrotrophic brooding, and patterns
III and IV all cases of placental brooding combined with,
correspondingly, oligo-/meso- and macrolecithal oogenesis.
At the same time, the number of oocytes may vary
considerably.
As for the class Stenolaemata, the reproductive pattern of
Recent Cyclostomata (viviparity) is similar to pattern V in
the cheilostome family Epistomiidae. Undoubtedly, this is an
example of convergence. Having found that ancestrula size is
similar in Recent and fossil stenolaemates, Pachut and
Fisherkeller ( 2010 ) suggested that polyembryony is a monophyletic trait in this class. This leads to the conclusion that
incubation and the endotrophic larva in general have evolved
in the class only once.
Branching structures in Cystoporata, stenolaemates from
the Late Ordovician, are considered as chambers for embryonic incubation (Buttler 1991 ; see also Taylor and Larwood
1990 ). If so, non-feeding larvae evolved at least by the Late
Ordovician in stenolaemates. Chambers for embryonic incubation (termed ovicells) have often been reported in
Fenestrata (Stratton 1975 , 1981 ; Southwood 1985 ; Bancroft
1986 ; Morozova 2001 ). However, judging from their structure and the suggested relationships between these two
Paleozoic stenolaemate orders (McKinney 2000 ), they are
unlikely to be homologous with the putative incubation
chambers of cystoporates. In Cyclostomata, zooids for
embryonic incubation (gonozooids) originated as late as the
Late Triassic (Taylor and Michalik 1991 ). Thus, incubation
structures seem to be not homologous within this class.
On the other hand, incubation itself would have originated
only once. Early stenolaemates, including Paleozoic cyclostomes, could have retained non-feeding larvae in the peristome, the distal part of the cylindrical autotozooid (Borg
1926 ; Taylor and Larwood 1990 ). If so, and if endotrophy
evolved only once in Stenolaemata (or was inherited from an
ancestor), embryonic incubation in the specialized chambers
originated independently at different times in different
stenolaemate orders on the basis of incubation in nonmodifi ed zooids. Of course, this conclusion would also hold
true if the endotrophic larva evolved several times in stenolaemates, as was apparently the case in gymnolaemates.
It is not known if Paleozoic cyclostomes incubated their
progeny, allowing the possibility that they might have
evolved an endotrophic larva much later, when gonozooids
evolved. Before that their larvae may have been planktotrophic, as indicted by the low taxonomic diversity of this group
in the Paleozoic (Ernst and Schäfer 2006 ). In contrast, other
Paleozoic stenolaemate orders were rather species-rich and
hence possibly had a non-feeding larva. Finally, cyclostomes
may be polyphyletic; they may have evolved from two different ctenostome ancestors (Ernst and Schäfer 2006 ), and
those that evolved in the Mesozoic would then have newly
acquired gonozooids, endotrophy and polyembryony.
Whatever the case, Cyclostomata evolved viviparity, that
is, intracoelomic incubation of embryos accompanied by
extraembryonic nutrition. The sequence of evolutionary
events may have been similar to the case of Ctenostomata
(see above), involving external brooding by means of adhesion of embryos to the lophophore, retraction of embryos
into the introvert (“mixed” brooding), obligatory brooding in
the tentacle sheath accompanied by polypide degeneration
and, fi nally, embryonic development in the coelomic cavity
of the zooids and then in the ovary. A similar scenario (except
for brooding in the tentacle sheath) appears possible in the
Epistomiidae, whose ancestors probably brooded their
embryos in ovicells.
The presence of only one or two oocytes in the ovary may
indicate that viviparity was accompanied by a decrease in the
number of eggs, initially numerous in cyclostomes. It is diffi cult to say whether this decrease was the consequence of
oocyte enlargement during transition to a non-feeding larva,
or suppression of oogonial division in the ovary during the
shift to intraovarian embryogenesis, or both. In the former
case, viviparity could result from a stepwise change from
simple to complex forms of embryonic incubation accompanied by gradual increase in the amount of reserves in the
oocytes and reduction in their numbers (as in gymnolaemates). In the latter case, early onset of oocyte division in the
ovary would have also resulted in a reduction in oocyte number. Actually, both mechanisms could have been involved,
and subsequent evolution of matrotrophy might have promoted a return to yolk-poor eggs. A transition from postovulatory intracoelomic fertilization to an early intraovarian
mode could have induced the beginning of division directly
in the ovary.
If these assumptions are correct, then evolution of the
reproductive pattern in Cyclostomata could have followed
the same trajectory as the transition from reproductive pattern II (as described for cheilostomes) to pattern III. A transition from pattern I is unlikely. In my opinion, the characteristic
set of “cyclostome” reproductive traits, involving intraovarian embryogenesis and polyembryony, merits the status of a
separate reproductive pattern VI.
An embryo developing in the ovary could be provided
with additional nutrients; instead of forming new oocytes,
the ovary “feeds” a single embryo. Moreover, because the
cylindrical zooids of cyclostomes can elongate over an
extended period, the developing embryos would be afforded
more space relative to the brood chambers of gymnolaemates. Both of these factors could precondition the origin of
polyembryony in Cyclostomata. This event could have
3 Evolution of Reproductive Patterns in Cheilostomata