55
brachiopods, echinoderms, crustaceans and many insects,
though their distribution in these groups is very patchy
(Raven 1961 ; Wourms 1987 ; Adiyodi and Adiyodi 1983 ;
Schmidt-Rhaesa 2007 ). Nurse cells have often been described
in sponges, but nutrimentary oogenesis in this group does not
involve the formation of siblings (Fell 1983 ; Ereskovsky
2010 ) and thus the term “nurse cells” as defi ned above is not
applicable. The same is true of some cnidarians (Wourms
1987 ). In the other groups mentioned, oocytes and nurse
cells originate from oogonia by incomplete cytokinesis.
Oocyte doublets, consisting of an oocyte and its nurse
cell, were observed in Cheilostomata as early as in the nineteenth century (Smitt 1865 ; Claparède 1871 ; Repiachoff
1876 ; Joliet 1877 ; Vigelius 1884b , 1886 ; Jullien 1888 ;
Pergens 1889 ; Calvet 1900 ). For example, Claparède noted
differences in the development of paired oocytes (“gepaarte
Eizellen”) in the ovary of Scrupocellaria scruposa – one of
them rapidly increased in size and became bright red while
the other remained small and colourless. Vigelius ( 1886 , pl.
26, fi g. 4) depicted a mature oocyte doublet in Bugula calathus , in which the nurse cell, most of it occupied by the
nucleus, was much smaller than its sibling. Calvet ( 1900 )
suggested that oocytes grow at the expense of degenerating
ones.
Nevertheless, these authors had no inkling of the existence of oocyte doublets, taking them to be successively
developing independent oocytes. The fi rst researcher to
apply the term nurse cell (or “nurse-cell”) to bryozoans and
describe the relationship of this cell to the oocyte was Marcus
( 1941a ). While investigating oogenesis in Thalamoporella
evelinae , he noticed that oocytes develop in pairs, one cell of
the pair acting as a “nurse”. According to his description, it
fused with the oocyte as soon as both reached a diameter of
20–30 μm, after which fertilization occurred. The doublet
then grew and, when its maximum size was reached, the
nucleus of the nurse cell migrated across the cytoplasm of
the oocyte to the vegetative pole, where it was removed from
the oocyte. Earlier, Marcus ( 1934 ) had described and
depicted “nourishing cells” (“Nährzellen”), which he considered to be abortive oocytes, in the ovaries of the phylactolaemate Lophopus crystallinus . The small size and large
nucleus of these cells and their position (pressed to the
oocyte) indicate their potential as nurse cells, but the presence of a cytoplasmic bridge has yet to be confi rmed.
Subsequent research confi rmed the existence of oocyte
doublets in cheilostomes, though the interactions of the
paired cells as described by Marcus in Thalamoporella need
to be verifi ed. Dyrynda ( 1981 ) was the fi rst to mention a syncytial doublet consisting of an oocyte and a nurse cell when
briefl y describing reproduction in Chartella papyracea .
Somewhat later, Dyrynda and Ryland ( 1982 ) and Dyrynda
and King ( 1983 ) noted that oocyte doublets result from
incomplete cytokinesis of the oogonium, remaining connected by a cytoplasmic bridge. It was shown in Bugula
fl abellata that oocyte doublets are connected not only by
cytoplasmic bridges but also by plate desmosomes. The presence of oocyte doublets was later shown in several other species (Temkin 1996 ; Ostrovsky 1998 , 2009 ). So far, the
maximum number of doublets observed was eight, in
Dendrobeania lichenoides (Temkin 1996 ). According to my
observations, up to 25 doublets may develop in the ovary of
Margaretta barbata , although some of them, as noted above,
may be oogonial doublets.
Synthetic activity in nurse cells and transport of reserve
nutrients, ribonucleoproteins and sometimes cell organelles
across cytoplasmic bridges, have been observed in scyphomedusae, ctenophores, rotifers, annelids and insects (see
reviews of Wourms 1987 ; Adiyodi and Adiyodi 1983 ).
Synthetic activity in cheilostome nurse cells was studied by
Dyrynda and King ( 1983 ). In C . papyracea , nurse-cell nuclei
enlarge considerably, their envelope forming numerous
folds. In the course of vitellogenesis, nurse cells actively produce ribosomes, agglomerations of which appear on both
sides of the cytoplasmic bridge, apparently indicating that
they are transported into the oocyte. Nurse cells also form
yolk granules, but their transport was never demonstrated. In
Bugula fl abellata nurse cells contain a very large nucleolus,
while their nuclear envelope is folded. They form few yolk
granules and “aggregations of possible RNA material”
(Dyrynda and King 1983 , p. 485). According to Hughes
( 1987 ), the accumulation of yolk at early stages of vitellogenesis in the oocytes in Celleporella hyalina may also result
from the activity of the nurse cell.
My data on the structure and function of nurse cells are in
complete agreement with previous descriptions but considerably supplement them. The structure of nurse cells indicates
their enhanced synthetic activity during the vitellogenic
period. The presence of a very large vesicular nucleus
(sometimes deformed) and a large nucleolus (more rarely
nucleoli) with inclusions (Figs. 1.6A , 1.7C , 1.8 inset, 1.10C ,
1.11A , 1.13B , 1.17 inset, 1.18F , 1.24 inset, 1.27B , 1.29A and
1.33D ) point to active synthesis of RNA. Moreover, it cannot
be excluded that bryozoan nurse cells are polyploid, similar
to the nurse cells of some polychaetes and insects (Wourms
1987 ). In the course of my research I found yolk granules not
only in oocytes but also in the nurse cells of at least 27 species
(Figs. 1.6D , 1.8 inset and 1.33D ; see also Table 1.7 ). This
previously overlooked phenomenon is likely to be much more
widespread. In some cases, granules can only be seen by
TEM; for instance, Dyrynda and King ( 1983 ) recorded yolk
granules in the nurse cells of B . fl abellata only after resorting
to ТЕМ.
In Bugulopsis monotrypa and Hippoporina reticulatopunctata , the cytoplasm of nurse cells in an early vitellogenic doublet contains dark granules, presumably of yolk.
At the same time, no such granules were found in the narrow
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata
brachiopods, echinoderms, crustaceans and many insects,
though their distribution in these groups is very patchy
(Raven 1961 ; Wourms 1987 ; Adiyodi and Adiyodi 1983 ;
Schmidt-Rhaesa 2007 ). Nurse cells have often been described
in sponges, but nutrimentary oogenesis in this group does not
involve the formation of siblings (Fell 1983 ; Ereskovsky
2010 ) and thus the term “nurse cells” as defi ned above is not
applicable. The same is true of some cnidarians (Wourms
1987 ). In the other groups mentioned, oocytes and nurse
cells originate from oogonia by incomplete cytokinesis.
Oocyte doublets, consisting of an oocyte and its nurse
cell, were observed in Cheilostomata as early as in the nineteenth century (Smitt 1865 ; Claparède 1871 ; Repiachoff
1876 ; Joliet 1877 ; Vigelius 1884b , 1886 ; Jullien 1888 ;
Pergens 1889 ; Calvet 1900 ). For example, Claparède noted
differences in the development of paired oocytes (“gepaarte
Eizellen”) in the ovary of Scrupocellaria scruposa – one of
them rapidly increased in size and became bright red while
the other remained small and colourless. Vigelius ( 1886 , pl.
26, fi g. 4) depicted a mature oocyte doublet in Bugula calathus , in which the nurse cell, most of it occupied by the
nucleus, was much smaller than its sibling. Calvet ( 1900 )
suggested that oocytes grow at the expense of degenerating
ones.
Nevertheless, these authors had no inkling of the existence of oocyte doublets, taking them to be successively
developing independent oocytes. The fi rst researcher to
apply the term nurse cell (or “nurse-cell”) to bryozoans and
describe the relationship of this cell to the oocyte was Marcus
( 1941a ). While investigating oogenesis in Thalamoporella
evelinae , he noticed that oocytes develop in pairs, one cell of
the pair acting as a “nurse”. According to his description, it
fused with the oocyte as soon as both reached a diameter of
20–30 μm, after which fertilization occurred. The doublet
then grew and, when its maximum size was reached, the
nucleus of the nurse cell migrated across the cytoplasm of
the oocyte to the vegetative pole, where it was removed from
the oocyte. Earlier, Marcus ( 1934 ) had described and
depicted “nourishing cells” (“Nährzellen”), which he considered to be abortive oocytes, in the ovaries of the phylactolaemate Lophopus crystallinus . The small size and large
nucleus of these cells and their position (pressed to the
oocyte) indicate their potential as nurse cells, but the presence of a cytoplasmic bridge has yet to be confi rmed.
Subsequent research confi rmed the existence of oocyte
doublets in cheilostomes, though the interactions of the
paired cells as described by Marcus in Thalamoporella need
to be verifi ed. Dyrynda ( 1981 ) was the fi rst to mention a syncytial doublet consisting of an oocyte and a nurse cell when
briefl y describing reproduction in Chartella papyracea .
Somewhat later, Dyrynda and Ryland ( 1982 ) and Dyrynda
and King ( 1983 ) noted that oocyte doublets result from
incomplete cytokinesis of the oogonium, remaining connected by a cytoplasmic bridge. It was shown in Bugula
fl abellata that oocyte doublets are connected not only by
cytoplasmic bridges but also by plate desmosomes. The presence of oocyte doublets was later shown in several other species (Temkin 1996 ; Ostrovsky 1998 , 2009 ). So far, the
maximum number of doublets observed was eight, in
Dendrobeania lichenoides (Temkin 1996 ). According to my
observations, up to 25 doublets may develop in the ovary of
Margaretta barbata , although some of them, as noted above,
may be oogonial doublets.
Synthetic activity in nurse cells and transport of reserve
nutrients, ribonucleoproteins and sometimes cell organelles
across cytoplasmic bridges, have been observed in scyphomedusae, ctenophores, rotifers, annelids and insects (see
reviews of Wourms 1987 ; Adiyodi and Adiyodi 1983 ).
Synthetic activity in cheilostome nurse cells was studied by
Dyrynda and King ( 1983 ). In C . papyracea , nurse-cell nuclei
enlarge considerably, their envelope forming numerous
folds. In the course of vitellogenesis, nurse cells actively produce ribosomes, agglomerations of which appear on both
sides of the cytoplasmic bridge, apparently indicating that
they are transported into the oocyte. Nurse cells also form
yolk granules, but their transport was never demonstrated. In
Bugula fl abellata nurse cells contain a very large nucleolus,
while their nuclear envelope is folded. They form few yolk
granules and “aggregations of possible RNA material”
(Dyrynda and King 1983 , p. 485). According to Hughes
( 1987 ), the accumulation of yolk at early stages of vitellogenesis in the oocytes in Celleporella hyalina may also result
from the activity of the nurse cell.
My data on the structure and function of nurse cells are in
complete agreement with previous descriptions but considerably supplement them. The structure of nurse cells indicates
their enhanced synthetic activity during the vitellogenic
period. The presence of a very large vesicular nucleus
(sometimes deformed) and a large nucleolus (more rarely
nucleoli) with inclusions (Figs. 1.6A , 1.7C , 1.8 inset, 1.10C ,
1.11A , 1.13B , 1.17 inset, 1.18F , 1.24 inset, 1.27B , 1.29A and
1.33D ) point to active synthesis of RNA. Moreover, it cannot
be excluded that bryozoan nurse cells are polyploid, similar
to the nurse cells of some polychaetes and insects (Wourms
1987 ). In the course of my research I found yolk granules not
only in oocytes but also in the nurse cells of at least 27 species
(Figs. 1.6D , 1.8 inset and 1.33D ; see also Table 1.7 ). This
previously overlooked phenomenon is likely to be much more
widespread. In some cases, granules can only be seen by
TEM; for instance, Dyrynda and King ( 1983 ) recorded yolk
granules in the nurse cells of B . fl abellata only after resorting
to ТЕМ.
In Bugulopsis monotrypa and Hippoporina reticulatopunctata , the cytoplasm of nurse cells in an early vitellogenic doublet contains dark granules, presumably of yolk.
At the same time, no such granules were found in the narrow
1.3 Comparative Analysis of Sexual Reproduction in Cheilostomata