240
a dozen larvae. For instance, in the cheilostome Celleporella
hyalina , a single female zooid subsequently brooded four
larvae during 76 days of observations before its senescence
(Hughes 1987 ). Corrêa ( 1948 ) noted that fertile zooids of
Bugula foliolata (as B . fl abellata ) produce three larvae on
average (i.e. during the reproductive season). The same is
probably true of most brooding Ctenostomata.
Considering oocyte size, in the vast majority of cheilostome brooders (66 species studied with patterns II and IV)
oocyte diameter is larger than in broadcasters, ranging from
100 to 400 μm, while 32 species have eggs of 160 μm and
larger. Only eight species have oocytes smaller than 90 μm
(see Sect. 1.2.4 and Table 1.6 ). Thus, when comparing broadcasters (pattern I) with brooders (patterns II and IV), one can
see a clear bias towards a decrease in the number of oocytes,
accompanied by their enlargement in Cheilostomata. This
trend also exists in ctenostomes, but the correlation between
oocyte size and number is not so strict (see also Sect. 3.4.4 ).
The data presented here for oocyte size/number in gymnolaemate bryozoans with contrasting patterns of sexual
reproduction can be considered as evidence of gradual rather
than abrupt changes in oogenesis during transition from
broadcasting to brooding. Although the limited capacity of
brood chambers restricts larval production, several brooders
still produce large numbers of oocytes. Why such a situation
is still relatively common among the Ctenostomata is unclear
since such large oocyte production is clearly redundant in
brooders. It is rare in Cheilostomata, however, most of which
form a small number of large oocytes.
In addition it can be said that oocytes that become richer
in yolk might stay longer in the ovary. In broadcasting malacostegines maintained in experimental culture, the development of oocytes in the ovary took less time, on average, than
oogenesis in brooding species (Silén 1945 , 1966 ; Dyrynda
and King 1983 ; Temkin, M.H., 2002, personal communication). So, it seems that the change in oogenesis resulted in a
decrease in the number of oocytes, which became larger and
took longer to form than in broadcasters.
3.1.2.2 Transition to Sequential Maturation
of Oocytes
In broadcasting bryozoans oocytes develop, reach maturity
and ovulate in cohorts (Hageman 1983 ; Temkin 1996 ). In
contrast, in most brooders oocytes mature, ovulate and are
moved to the brood chamber sequentially. Thus, the change
in oogenesis mode (decrease in egg number, increase in egg
size) and the transition from reproductive pattern I to pattern
II were also accompanied by sequential egg maturation.
Silén ( 1945 ) wrote that the emergence and development
rate of the new oocytes in the ovary of Callopora dumerilii
directly depends on the development rate of the leading
oocyte doublet. Thus, the presence of this physiologically
very active cell pair appears to slow down or even block the
division of oogonia and the growth of younger doublets in
the ovary. Besides, it seems that considerable limitations on
the number of simultaneously produced eggs are imposed by
the carrying capacity of the brood chamber: almost all cheilostomes incubate one embryo at a time (see above).
The developing ovary in a young zooid contains, as a rule,
a few oogonia, which divide to form primary oocytes. In
brooding cheilostomes from one to several oocyte doublets
are formed in a young ovary in the early stages of oogenesis,
entering the phase of previtellogenic growth sequentially. It
is unknown whether this sequence is associated with the age
of the doublets, but it may be suggested that the older the
doublet and the larger its cells, the more likely it is to lead
the sequence and to continue to grow at a higher rate than
the others. This may be directly associated with its size: the
greater the surface area and the volume of the female cell the
more substances can be transported into and synthesized in
it. Such a doublet might block the accumulation of nutrients
in younger oocytes (those that appear later) as well as mitoses in oogonia (for instance, by hormonal regulation). The
leading oocyte doublet may be compared to a powerful
pump channelling the transport of nutrients in the ovary.
After the ovulation of the leading doublet its place is occupied by the second largest (and possibly the second oldest)
doublet. It may be also assumed that for some time following
ovulation the conditions in the ovary become favourable for
new oogonial divisions.
The fi nding in the ovaries of at least 18 brooding cheilostomes of two or more (up to six in Quadriscutella papillata )
vitellogenic (i.e. growing) doublets, indicates that oogenesis
with sequential formation of oocytes originated from the
more ancient variant of oogenesis with simultaneous formation of several oocytes. In Eurystomella foraminigera and
Bostrychopora dentata all doublets in the ovary (up to three)
are vitellogenic. Further, in both these species yolk granules
are contained not only in oocytes but also in nurse cells.
This indicates that, initially, nutrient reserves accumulate in
both siblings (see below). The fact that in some species
( Nematofl ustra fl abellata , Isosecurifl ustra angusta ,
Columnella magna ) a pair of vitellogenic doublets at early
stages develops more or less synchronously is reminiscent of
oogenesis in broadcasters (Hageman 1983 ) and, thus, may
indicate the connection between reproductive patterns I and
II. It is only somewhat later that development becomes asynchronous, with one of the doublets considerably outstripping
the other.
The only known ctenostome brooder with numerous ovulated oocytes is Triticella fl ava , which externally broods
numerous embryos. Small cohorts of simultaneously developing eggs are recorded in those ctenostome brooders that
simultaneously incubate one or several embryos. In contrast,
in the majority of species with only one embryo incubated at
a given time, oocyte development, maturation and ovulation
3 Evolution of Reproductive Patterns in Cheilostomata
a dozen larvae. For instance, in the cheilostome Celleporella
hyalina , a single female zooid subsequently brooded four
larvae during 76 days of observations before its senescence
(Hughes 1987 ). Corrêa ( 1948 ) noted that fertile zooids of
Bugula foliolata (as B . fl abellata ) produce three larvae on
average (i.e. during the reproductive season). The same is
probably true of most brooding Ctenostomata.
Considering oocyte size, in the vast majority of cheilostome brooders (66 species studied with patterns II and IV)
oocyte diameter is larger than in broadcasters, ranging from
100 to 400 μm, while 32 species have eggs of 160 μm and
larger. Only eight species have oocytes smaller than 90 μm
(see Sect. 1.2.4 and Table 1.6 ). Thus, when comparing broadcasters (pattern I) with brooders (patterns II and IV), one can
see a clear bias towards a decrease in the number of oocytes,
accompanied by their enlargement in Cheilostomata. This
trend also exists in ctenostomes, but the correlation between
oocyte size and number is not so strict (see also Sect. 3.4.4 ).
The data presented here for oocyte size/number in gymnolaemate bryozoans with contrasting patterns of sexual
reproduction can be considered as evidence of gradual rather
than abrupt changes in oogenesis during transition from
broadcasting to brooding. Although the limited capacity of
brood chambers restricts larval production, several brooders
still produce large numbers of oocytes. Why such a situation
is still relatively common among the Ctenostomata is unclear
since such large oocyte production is clearly redundant in
brooders. It is rare in Cheilostomata, however, most of which
form a small number of large oocytes.
In addition it can be said that oocytes that become richer
in yolk might stay longer in the ovary. In broadcasting malacostegines maintained in experimental culture, the development of oocytes in the ovary took less time, on average, than
oogenesis in brooding species (Silén 1945 , 1966 ; Dyrynda
and King 1983 ; Temkin, M.H., 2002, personal communication). So, it seems that the change in oogenesis resulted in a
decrease in the number of oocytes, which became larger and
took longer to form than in broadcasters.
3.1.2.2 Transition to Sequential Maturation
of Oocytes
In broadcasting bryozoans oocytes develop, reach maturity
and ovulate in cohorts (Hageman 1983 ; Temkin 1996 ). In
contrast, in most brooders oocytes mature, ovulate and are
moved to the brood chamber sequentially. Thus, the change
in oogenesis mode (decrease in egg number, increase in egg
size) and the transition from reproductive pattern I to pattern
II were also accompanied by sequential egg maturation.
Silén ( 1945 ) wrote that the emergence and development
rate of the new oocytes in the ovary of Callopora dumerilii
directly depends on the development rate of the leading
oocyte doublet. Thus, the presence of this physiologically
very active cell pair appears to slow down or even block the
division of oogonia and the growth of younger doublets in
the ovary. Besides, it seems that considerable limitations on
the number of simultaneously produced eggs are imposed by
the carrying capacity of the brood chamber: almost all cheilostomes incubate one embryo at a time (see above).
The developing ovary in a young zooid contains, as a rule,
a few oogonia, which divide to form primary oocytes. In
brooding cheilostomes from one to several oocyte doublets
are formed in a young ovary in the early stages of oogenesis,
entering the phase of previtellogenic growth sequentially. It
is unknown whether this sequence is associated with the age
of the doublets, but it may be suggested that the older the
doublet and the larger its cells, the more likely it is to lead
the sequence and to continue to grow at a higher rate than
the others. This may be directly associated with its size: the
greater the surface area and the volume of the female cell the
more substances can be transported into and synthesized in
it. Such a doublet might block the accumulation of nutrients
in younger oocytes (those that appear later) as well as mitoses in oogonia (for instance, by hormonal regulation). The
leading oocyte doublet may be compared to a powerful
pump channelling the transport of nutrients in the ovary.
After the ovulation of the leading doublet its place is occupied by the second largest (and possibly the second oldest)
doublet. It may be also assumed that for some time following
ovulation the conditions in the ovary become favourable for
new oogonial divisions.
The fi nding in the ovaries of at least 18 brooding cheilostomes of two or more (up to six in Quadriscutella papillata )
vitellogenic (i.e. growing) doublets, indicates that oogenesis
with sequential formation of oocytes originated from the
more ancient variant of oogenesis with simultaneous formation of several oocytes. In Eurystomella foraminigera and
Bostrychopora dentata all doublets in the ovary (up to three)
are vitellogenic. Further, in both these species yolk granules
are contained not only in oocytes but also in nurse cells.
This indicates that, initially, nutrient reserves accumulate in
both siblings (see below). The fact that in some species
( Nematofl ustra fl abellata , Isosecurifl ustra angusta ,
Columnella magna ) a pair of vitellogenic doublets at early
stages develops more or less synchronously is reminiscent of
oogenesis in broadcasters (Hageman 1983 ) and, thus, may
indicate the connection between reproductive patterns I and
II. It is only somewhat later that development becomes asynchronous, with one of the doublets considerably outstripping
the other.
The only known ctenostome brooder with numerous ovulated oocytes is Triticella fl ava , which externally broods
numerous embryos. Small cohorts of simultaneously developing eggs are recorded in those ctenostome brooders that
simultaneously incubate one or several embryos. In contrast,
in the majority of species with only one embryo incubated at
a given time, oocyte development, maturation and ovulation
3 Evolution of Reproductive Patterns in Cheilostomata